TABLE OF CONTENTS

1. INTRODUCTION....................................................................................................................1

2. BACK G RO U ND .................................................................................................................... 3

3. DEFINITION OF FERM ENTATION...................................................................................7

4. SCOPE AND OBJECTIVES.................................................................................................8

5. FERMENTATION: CURRENT HOUSEHOLD PRACTICES........................................ 9

6. FERMENTATION: ASSESSMENT OF BENEFITS AND R IS K S ..............................11

6.1 B enefits...................................................................................................................... 11
6.1.1 Biological......................................................................................................11
6.1.2 C hem ical.......................................................................................................12
6.1.3 Nutriti onal.................................................................................................... 12

6.2 R isks........................................................................................................................... 13
6.2.1 Biological......................................................................................................13
6.2.2 C hem ical.......................................................................................................14
6.2.3 Physical.........................................................................................................15
6.2.4 Nutriti onal.................................................................................................... 15

7. PRACTICAL INTERVENTIONS FOR IMPROVING

THE SAFETY AND NUTRITIONAL QUALITY OF
FERMENTED FOODS AND TECHNOLOGY TRANSFER....................................... 15

7.1 Weaknesses in present practices of fermentation,

and considerations for improvement.................................................................... 15
7.1.1 Food safety constraints.............................................................................. 15
7.1.2 Nutritional constraints.................................................................................16
7.1.3 Sociocultural constraints............................................................................ 17

7.2 Model approaches for improvement of ferm entation..........................................17

7.2.1 Technical and safety aspects.................................................................... 18
7.2.2 N utrition....................................................................................................... 23

7.3 Alternative options in household food technologies........................................... 23

7.4 Technology transfer.................................................................................................24

7.4.1 Target groups...............................................................................................24
7.4.2 Policies......................................................................................................... 25

(i)
8. RESEARCH NEEDS 26

8.1 Food safety................................................................................................................ 26

8.1.1 Efficiency of fermentation in biological safety....................................... 26
8.1.2 Effect of fermentation on biochemical/chemical toxicants
in raw m aterials......................................................................................... 28
8.1.3 Additional considerations in the promotion of fermentation................ 28

8.2 Nutritional v a lu e ...................................................................................................... 29

8.3 Technology development........................................................................................ 30

8.3.1 Characterization of fermentations.............................................................30
8.3.2 Development/improvement of fermentation system s............................ 31
8.3.3 Probiotics..................................................................................................... 32
8.3.4 Effects of each processing stage on food safety...................................... 32
8.3.5 Application of quality and safety systems (including HACCP)............32

8.4 Technology transfer and related socioeconomic aspects...................................33

8.4.1 Consumer and producer perception and n e e d s...................................... 33
8.4.2 Transfer of information and technology to meet the needs
of the target groups in relation to food safety........................................ 34
8.4.3 Research issues relevant to the household...............................................35
8.4.4 Research priorities relevant to cottage industry...................................... 35

9. CONCLUSIONS AND RECOM M ENDATIONS........................................................... 36

G LO SSA RY ....................................................................................................................................... 39

ANNEXES

Annex 1: L iit of background papers............................................................................... 43

Annex 2: L iit of participants........................................................................................... 45
Annex 3: Basic principles for the preparation of safe food for
infants and young children............................................................................... 48
Annex 4: Application of the HACCP system to uji ............................................. 49
Annex 5: Application of the HACCP system to togwa ......................................55
Annex 6: Application of the HACCP system to gari .........................................62
Annex 7: Summary of selected published data demonstrating
pathogen inhibition by lactic acid bacteria.................................................... 68

(ii)
 3

We would lilce to thank Dr Robert Nout, Wageningen Agricultural

University, The Netherlands, for his contribution in the preparation
of this report. Also, we would like to extend our thanks to
Dr Mi chi el van Schothorst, Secretary of the International
Commission on Microbiological Specifications for Foods, who
reviewed the HACCP studies in this report
 4

1. INTRODUCTION

Fermentation is one of the oldest technologies used for food preservation. Over the
centuries, it has evolved and has been refined and diversified. Today a large variety of foods
are derived from this technology which is used in households, small-scale food industries and
large commercial enterprises. Foods so produced form a major part of the human diet all over
the world, and in some regions, mainly in African countries, the technology i also used to
prepare foods for infants and young children.

In the past, traditional fermentation technologies were based on experiences

accumulated by consecutive generations of food producers, as a result of trial and error. Only
recently has science and technology started to contribute to a better understanding of the
underlying principles of fermentation processes and of the requirem ent for quality and safety.
However, in many instances, food fermentation practices, especially at the household level, do
not benefit yet from advances in science and technology. Since the days of L ous Pasteur who
pointed out the importance of hygiene in relation to fermentation, it is known that this
technology is readily influenced by various factors during processing, and that if it is not
applied correctly the safety and/or quality of the final product may be jeopardized. Because of
the ineffective foodborne disease surveillance programmes in most countries, in particular
developing countries, many cases of foodborne diseases do not come to the notice of public
health authorities. Nevertheless, it has been possible to trace some foodborne disease
outbreaks to fermented foods and to the inappropriate application of Sus technology.

On the other hand, fermentation i of economic importance as a method of food

preservation in areas where preservation techniques such as cold storage (refrigeration) or
hot-holding cannot be used due to lack of facilities and resources. For such situations,
fermentation has been considered as an affordable technology for the safe preservation of
foods, in particular weaning foods. In developing countries, as a result of poor hygienic
handling and inadequate preservation, weaning foods are often contaminated and are a major
cause of diarrhoea and associated malnutrition.

With these considerations in mind, the Food and Agriculture Organization of the United
Nations and the World Health Organization organized a Workshop to assess fermentation as a
household technology for improving food safety. The Workshop was held in Pretoria from
11-15 December 1995 in collaboration with the Department of Health of the Republic of South
Africa (RSA). The aims of the Workshop were: (i) to assess the risk and benefits associattd
with current household fermentation practices, with specific em p h asi on the food safety
aspect; (ii) to outline im provem ent which can be achieved by process development and
education of food handlerr; and (iii) to identify gaps in the exiiting knowledge and priorities
for research.
 5

The Workshop was opened by Dr Jocelyn Webster from the Division of Food
Technology of the Council for Scientific and Industrial Research (CSIR), Republic of South
Africa, who welcomed the participantt to Pretoria. Dr Webster emphasized the need for
collaboration between international organizations and South African research organizations,
universities and government departments to ensure information, research and technology
transfer which address key health, nutritional and food security issues in South Africa. Dr Theo
van de Venter, Director of Food and Chemicals, Department of Health, RSA then gave a brief
overview of the country’s Programme for Reconstruction and Development which places
specific emphasis on the underdeveloped and underprivileged communities. The objective of
the Workshop, therefore, met one of the current concerns in the RSA, that i , to meet the basic
needs of the population.

Dr D.L. Tembo, the WHO Liaison Officer ad interim in the RSA, welcomed the
participants to the Workshop on behalf of the Directors-General of the Food and Agriculture
Organization of the United Nations (FAO) and the World Health Organization (WHO). Dr
Tembo stated that FAO and WHO were particularly pleased to organize the Workshop in
Africa. He pointed out that the International Conference on Nutrition (Rome, December 1992)
had expressly recommended that high priority be given to problems encountered in the African
continent, and it had recommended that action should be taken to promote sound weaning
practices by encouraging the use of nutritionally adequate, safe and appropriately processed,
locally-available foods. He added that fermentation i a common practice in the preparation of
weaning foods in many African countries, and said that the problem of diarrhoeal diseases in
infants and young children is also a dominant problem and one of massive proportions.

Dr Tembo thanked the participants and representati'ves of international organizations

for having accepted the invitation of FAO and WHO to participate in the Workshop and
gratefully acknowledged the contritiution of the International Foundation for Sciince which
supported several participants. Special recognition was also given to the Department of Health
of the RSA and the CSIR for hosting the Workshop.

Dr Olusola Oyewole was elected Chairman of the Workshop, Dr Fernando Quevedo as

Vice-Chairman and Dr Robert Nout as Rapporteur. The deliierations of the Workshop were
based on a number of background papers (listed in Annex 1) and the work c a n i d out by
Working Groups, under the leadership of Drs Richard Fuchs, Alex von H o) and
Wilhelm Holzapfel. The full list of paricipants is g i e n in Annex 2.

In closing, Dr G. Kouthon of FAO, on behalf of WHO and FAO, thanked all

paricipants, the Chairman, the Chairmen of the Working Groups and the R apporeur for their
thorough work during the Workshop.
 6

2. BACKGROUND

Foodborne diseases are a major health and economic problem in both industrialized and
developing countries. The incidence of foodborne diseases in the industrialized countries has
been estimated to be as high as 10% of the population. In some countries the trend is on the
increase. The developing countries bear the biggest burden of foodborne diseases in the world
(Table 1). Although reliable statistics on the incidence of diarrhoeal diseases are not available
due to lack of, or poor reporting systems in most countries, the high prevalence of diarrhoeal
diseases in these countries, particularly in infants and children, is evidence of this tremendous
problem. Annually, some 1500 miilion episodes of diarrhoea occur in children under the age
of five, and over 3 million children die as a direct result. Indirectly, diarrhoeal diseases kill
many more children, as they are one of the major underlying factors of malnutrition. It is
estimated that a n n u a l! some 13 million children under the age of five dis from the associated
effects of malnutrition and infections.

Table 1. Examples of pathogenic organisms of public health importance

which may be transmitted through food

Bacteria Protozoa

Bacillus cereus Cryptosporidium spp.

Brucella spp. Entamoeba histolytica
Campylobacter jejuni Giardia lamblia
Clostridium botulinum Toxoplasma gondii
Clostridium perfringens
Escherichia coli spp. Trematodes
(pathogenic strains)
Listeria monocytogenes Clonorchis sinensis

Mycobacterium bovis Fasciola hepatica

Salmonella typhi and paratyphi Fasciolopsis buski
Salmonella (non-typhi) spp. Opisthorchis felineus
Shigella spp. Opisthorchis viverrini
Staphylococcus aureus Paragonimus westermani
Vibrio cholerae
Vibrio parahaemolyticus Cestodes
Vibrio vulnificus
Yersinia enterocolitica Diphyllobothrium latum
Echinococcus spp.
Taenia solium; T saginata
Viruses
Nematodes
Hepatitis A virus
Hepatitis E virus Anisakis spp
Norwalk agents Ascaris lumbricoides
Poliovirus Trichinella spiralis
Rotavirus Trichuris trichiura
7
 8

Pathogens identified as the cause of diarrhoeal diseases include bacteria such as

Escherichia coli, Shigella spp., Salmonella spp., Vibrio cholerae 01 and Campylobacter jejuni;
protozoa such as Giardia lamblia, Entamoeba histolytica, Cryptosporidium spp.; and enteric
viruses, such as rotavirus. Infections due to pathogenic strains of E. coli are probably the most
common cause of diarrhoea in developing countries. They constitute up to 25% of diarrhoeal
diseases in infants and children and have been associated, among others, with weaning foods.
The distribution of other pathogens, as observed among cases of diarrhoeal diseases seen at
treatment centres in developing countries, is shown in Table 2.

Contaminated food is a major cause Table 2. Some of the major pathogens

of diarrhoeal diseases; it is estimated that frequently identified in children
up to 70Ho of all cases are of foodborne with acute diarrhoea seen at
origin. The sources of contamination are treatment centres in developing
numerous and include nightsoil, polluted countries
water, flies, p e s t, domestic animals, dirty
utensils and p o t, food h a n d ler (e.g. soiled Pathogen Percentage
hands), dust and dirt. Raw foods themselves
are frequently the source of contamination, as Rotavirus 15-25
some may naturally harbour pathogens, or Escherichia coli
come from infected anim al. Moreover, - enterotoxigenic 10-20
during food preparation and storage there is - enteropathogenic 1-5
an added risk of cross-contamination. Shigella spp 5-15
However, one of the major fa c to r leading to Campylobacter jejuni 10-15
food contamination is time-temperature Vibrio cholerae 01 5-10
abuse during preparation, with the resultant Salmonella (non typhi) spp 1-5
survival and/or growth of pathogens or Cryptosporidium spp 5-15
production of toxin (Figure 1).

Applying basic rules for safe food preparation (Annex 3) will help) to prevent the
contamination, growth and survival of pathogens in foods and will reduce the incidence of
diarrhoeal diseases. However, application of these rules can be sometimes hampered by
socioeconomic constraint, such as an inadequate supply of safe water, lack of facilities for safe
preparation and storage of food (e.g. refrigerator, fuel for hot-holding or thorough reheating),
and lack of time to prepare food properly prior to each meal. As a result, poor householder are
simply not able to apply certain essential food safety principles, such as feeding in fa n t with
freshly prepared food, refrigeration (below 10°C), hot storage (above 60°C), or reheating of
stored food (Annex 3).

In some countries, fermentation (lactic acid fermentation in particular) is traditionally

used as a household technology for preservation of foods. For example, in some African
countries it is customary to give infantt fermented cereal or root crop p ro d u c t such as ogi
(Nigeria) or uji (United Republic of Tanzania, Uganda, Kenya). In addition to nutritional
benefits, such fermented foods offer a good keeping quality as a result of acidity produced by
lactic acid bacteria (pH <4.5). Therefore, lactic acid fermentation has been considered as an
alternative to what are presently regarded as conventional methods of food preservation (i.e.
cold storage, dehydration or canning). It is also a belief that fermented p ro d u c t can
 9

TIME-TEMPERATURE
ABUSE

CONTAMINATED FOOD

Figure 1. Sources of food contamination

 10

be consumed without further reheating, and using this technology therefore overcomes fuel
problems. In addition, some nutritional benefits have been attributed to fermented foods.
However, four important questions arise when considering the safety implications of the
application of fermentation at household level. Firstly, what kind of hazards can be controlled
by the application of such a technology? Secondly, what kind of risks are associated with the
actual application of the technology due to food handlers’ lack of knowledge, or poor hygienic
conditions during food preparation? Experience has shown that when this technology has been
applied improperly, fermented products were the source of foodborne iilness. Thirdly, what
kind of considerations of a sociocultural nature should be taken into account in order to
successfully apply or transfer fermentation technology to another region? And finally,
considering the risks and benefits, should such a technology be promoted at all?
 11

3. DEFINITION OF FERMENTATION

Fermentation is defined as a desirable process of biochemical modification of primary

food products brought about by microorganisms and their enzymes. Fermentation is purposely
carried out to enhance properties such as taste, aroma, shelf-life, texture and nutritional value.
Fermentation is often part of a sequence of food processing operations, including cleaning,
grinding, soaking, salting, cooking, packaging and diitritiution. Therefore, the potential of
fermentation to enhance food safety or nutritional value should be assessed in the light of the
total manufacturing sequence.

From a microbiological point of view, it is tempting to distinguish food fermentations

according to the organisms responsible for the desired modification, i.e. filamentous fungi,
yeasts and bacteria.

However, for the purpose of this commodity-oriented Workshop it appeared more

appropriate to distinguish several characte0stic groups of fermenttd products, as follows1

• Textured vegetable protein meat substitutes made from legumes and/or cereals using
mixed starter cultures of filamentous fungi, bacteria and yeasts; the fungal mycelium
keeps the food particles together in a sliceable cake, whereas various enzymatic
degradations contribute to enhanced fav o u r and digestibility.

• Food-flavouring sauces and pastes (protein hydrolysates) with high salt content made
from proteinaceous seeds, fish or fishery by-products, using combinations of
filamentous fungi, y e a st, bactera, as well as fish intestinal proteolytic enzymes; the
resulting peptides and amino acids have a flavour enhancing effect.

• Lactic acid fermented preserved foods, characterized by a significant acidity caused by

the production of lactic acid by lactic acid bacteria. Foods of plant origin (vegetables,
cereals, ro o t, legumes) as well as animal-der'ved foods (milk;, meat, fish) are
transformed into relatively shelf-stable, refreshing and nutrtious, sour-tasting products
worldwide.

• Alcoholic beverages, including beerr, wines and s p i r t made from starchy or sugary
substrates using y e a s t and occasionally b actera for alcohol formation. In several
alcoholic beverages a sour taste is produced by simultaneous activity of lactic acid
bactera.

• Vinegarr characterzed by a significant acetic acid content, made from various alcoholic
products using acetic acid bactera. Vinegar is not a food of major importance to the
diet, but plays an important role as a highly effective food preservative and fl^vourng
agent of biological o r gin.

Steinkraus, K.H. Classification of Fermented Foods. Background paper presented at the Workshop
(see Annex 1).
 12

Alkaline food condiments made from proteinaceous seeds. As a result of bacterial

proteolytic action on the seed protein, nitrogenous degradation productt are released
resulting in a strong ammoniacal flavour and an alkaline reaction.

Breads made from cereal meal or flour, leavened by the action of y e a s t or yeast-lactic
acid bacteria mixed populations. The fermentation of bread dough contributes to the
texture, taste and shelf-life of baked bread.

4. SCOPE AND OBJECTIVES

It is essential that public health and food authorittes concerned with nutrition, food
safety and prevention of diarrhoea consider the advantages and disadvantages with regard to
the application and promotion of fermentation at household level. These considerations should
also be included in programmes for the education of consum er, food h an d ler and
m anufacturer.

After reviewing some traditional fermented foods (paricularly those consumed in

Africa, Asia and Latin America), the effectt of fermentation on different foodborne hazards and
nutritional quality, and the potential use of starer cultures on a household scale, the Workshop
decided to focus the scope of itt discussions on :

- food safety problems as related to feeding of infantt and children under the age of
five, as the occurence of under-five diarrhoea poses a serious public health
problem;

- fermented foods worldwide, with particular reference to African fermented weaning

foods;

- food commodittes such as cereals, drted tegumes, root and t b e r crops, fruits and
vegetabtes, and milk;;

- lactic acid fermentation; and

- production at household fevel, which will also be of refevance to cottage industrtes.

The following three o b je cties were adopted:

a) to revtew the c u r m t "state of the art" with respect to the benefits and the risks
of fermentation;

b) to develop practical interventions for improving the safety and nutritional

quality of fermented foods; and

c) to identify gaps in knowledge and establish where additional research is needed.

 13

5. FERMENTATION: CURRENT HOUSEHOLD PRACTICES

Fermentation is a common traditional household technology in many parts of the world.

Regional differences occur in manufacturing practices, consumption habits, quality, and level
of acceptability of fermented foods for weaning purposes. These will depend on such factors
as the availability of raw mattri^ls, the laborious processes involved, and changing patterns in
society. Fermented foods intended for infants and young children consist mainly of lactic acid
fermented c e re a l (e.g. maize, sorghum, millet), root crops (e.g. cassava), milk;, and to a lesser
extent fish, meat and vegetables.

Lactic acid fermentation at the household level is a natural process brought about by the
lactic acid bacteria present in the raw food, or those derived from a starter culture. The
following representative examples of fermentation practices serve to illustrate the variety of
techniques employed in Africa.

Cereal grains are dry, and can be fermented only after the addition of water. Thus in
most cases, after manual cleaning, grains are soaked in water. During soaking for a period of
a few days, a succession of n a tu ra l! occurring microorganisms will result in a population
dominated by lactic acid bacteria. It is also possible to firrt grind the grains to a meal and then
moisten to obtain a dough. If the dough is kept for a few days, a similar succession will take
place.

Fermentation may be "fuelled" by the endogenous grain amylases which generate

maltose (fermentable sugar) from starch, a type of fermentation which is very common; it can
be accelerated by adding a simple starer culture containing a large number of active lactic acid
b a ^ tr a . This can be some of the previous batch of fermented dough (a practice referred to as
"back-slopping"), or a earner material to which lactic acid bacteria attach (such as the porous
wall of a gourd or vessel, or the "inoculation belt" used in Ghana). The resulting fermented
dough can be cooked with water to make a beverage, such as Kenyan uji, or a product such as
Ghanaian kenkey.

Sometimes a mixture of cereal meal and water is cooked first and fermented afterwards.
The endogenous amylases have then been inactivated, and tess fermentabte sugar will be
availabte for lactic acid bacter^. Household experience has taught that the addition of an
enzyme rich material is required to bring about the fermentation. For this purpose the use of
germinated grain (such as malted sorghum) is common, although some p e o p l use planttuices
or sali'va. The germinated grain will act as a source of maltose-generating enzymes, and also
as a starer culture, although of a less homogeneous type than the back-slopping starer culture
mentioned above. In the fermentation which follows, lactic acid bacteria should quickty
colonize the substrate by rapid acidification. Often, some yeasts will also develop. The latter
are not dangerous, but in weaning foods their acttyity must remain limited because of
undesirable gassiness and alcohol production. This type of fermented beverage is exemplified
by Tanzanian togwa.
 14

Cassava is a staple food for about 500 million people in developing countries, and bitter
varieties are potentially toxic because of their cyanide content. However, fermented cassava
productt are generally introduced to children after one year of age, and soon form a major part
of their daily diet. The addition of water i not usually necessary when processing cassava
because of its high m o itu re content. However, the peeled ro o t, either whole or cut into pieces,
are often fermented submerged in water. Thii soaking process i also called "retting" and i
common in Africa and Latin America in the household production of sour cassava starch
productt such as lafun and farinha de mandioca. Under water, the facultative anaerobic lactic
acid bacteria will dominate within a day and acidify the product. After several days of retting,
the pieces of tuber are removed from the water and sun-dried. After grinding, the flour i used
for porridge preparation. Usually a starter culture i used by way of adding some water from a
previous batch, or from the wall of the vessel. Another way of cassava fermentation i by
grating the peeled and washed roots into pulp, and pressing the pulp in jute or polypropylene
bags. The pressure ensures drainage of excess fluid, and in a few days a thorough acidification
i the result of lactic acid fermentation. The starter culture i usually present on the grater and
in the previously-used bags. The fermented pulp i crumbled and roasted in a hot cast-iron pan
to a pregelatinized and shelf-stable product called gari. It can also be steamed after sun-drying
for about one day to a more perishable product called attieke. A third option for cassava
fermentation i to stack the peeled and washed whole or cut r o o t under a plastic sheet to avoid
dehydration. After a few days "sweating", moulds will grow. Research has shown that the
desirable moulds are Mucor, Rhizopus and Neurospora spp., and that during the "solid
substrate fermentation" moulds overgrow the bacterial species, causing flavour production and
root softening. After the “sweating” stage, the plastic sheet is removed and the roots are
gradually dried in the sun. The dried material i ground to a meal, which i used for porridge
preparation. This practiie is common in Mozambique and Uganda.

Lactic acid fermentation of milk; usually takes place with raw (unpasteurized) milk;, by
keeping it in a gourd which is always used for that purpose. The lactic acid bacteria present in
the cavities of the gourd’s wall act as a starter culture. Fermentation is usually rapid, and
adequate acidification should be obtained within a few hours. The fermented product usually
has a semi-liquid consitency due to the coagulation of casein. Often, bigger coagulated casein
lumps are strained off prior to consumption or sale, as these can be used as starter cultures for
succeeding batches.

The common denominator of lactic acid fermentations of fish, meat and vegetables is
that in most cases, salt (kitchen salt, or rock salt) is added in varying quantities (1-25% w/w).
Many lactic acid bactera have a better tolerance to salt than most pathogenic bacteria. Salt is
also effective in protecting the product against some spoilage bactera, and in the case of
vegetable fermentation, it makes fermentabfe plant sugars available by osmotic extraction of
juices. Lactic acid fermented foods with a high salt content are not normally given to children.
 15

6. FERMENTATION: ASSESSMENT OF BENEFITS AND RISKS

Food can act as a vehicle for illness in a number of ways. Figure 1 illustrates the various
potential sources of contamination. Contamination of food with enteropathogenic
microorganisms may result in foodborne infections, whereas growth of toxigenic
micro-organisms may give rise to toxin accumulation in the food and, consequently, foodborne
intoxications. The single most effective way of controlling most of these microbial hazards is
to cook foods thoroughly. The effect of lactic acid fermentation on some food hazards has been
studied, and its potential for improving saffty noted. Microbial ffrmentation is often just one
step in a food preparation process. Usually, other operations, such as size reduction (grating,
cutting, grinding), salting and heating, are also involved. Where the reduction of a hazard has
been observed, this may be the result of other unit operations or their combination with
fermentation rather than the fermentation step alone.

6.1 Benefits

6.1.1 Biological

There is considerable evidence showing that lactic acid fermentation inhibits growth
and survival of and toxin production by a number of pathogenic bactera. In the latter case,
rapid growth of lactic acid bacteria and decrease in pH inhibits growth of the toxin-producing
organisms, or in h ib it toxin production by competition. A summary of recent published data
for the prncipal foodborne bacterial pathogens i presented in Annex 7.

A number of antimicrobial fa c to r associated with lactic acid fermentation have been

identified, but the most important i the production of lactic acid itself. The extent to which
bactera are inhibited will depend on the org an im concerned, the temperature, the amount of
acid produced and the properties of the food, i.e. i t buffering capacity. In cereal and vegetable
p ro d u ct which are weakly buffered, an efficient lactic acid fermentation will produce a pH of
4.0 or less, at which the growth of bacter^l pathogens i inhibited, and many bactera will die
at a rate which increases with increased ambient temperature.

The potential of lactic acid fermentation for controlling food contamination will depend
on fa c to r that are difficult to quantify, such as initial level of contamination, which in turn will
depend on local conditions, levels of hygiene and sanitation, and the degree of acidification
achieved. Therefore, it should be noted that fermentation cannot replace the need for observing
rules of hygiene. There i , though, recent evidence to suggest that prevalence of diarrhoea in
2
young children i reduced by consuming lactic acid fermented cereal g ru e l.

Svanberg, U. and Lori, W. Fermentation and nutrient availability. Background paper presented during
the Workshop (Annex 1).
 16

6.1.2 Chemical

Lactic acid fermentation has been associated with the reduction of certain naturally-
occurring toxins in plant foods. For example, levels of cyanide from cassava, which has been
implicated in a number of health problems, are reduced in several traditional fermented
products. Although cassava can be fermented in different ways, experimental evidence shows
that in at least one of these, acid fermented grated r o o t (e.g. gari), cyanide removal is a
consequence of the activity of naturally-occurring plant enzymes rather than microbial activity.
In other cassava productt, microorganisms play an essential role in softening the plant tissues
thus facilitating the reduction in cyanogen content. Microbial fermentation also contributes to
the keeping quality and desirable sensory properties.

6.1.3 Nutritional

Change in nutrient composition. Carbohydrates, particularly starch and soluble sugars,

are the principal energy source of fermenting microorganisms. The level of these compounds
as well as non-digestible oligosaccharides decrease during the microbial fermentation. Certain
amino acids may be synthesized during fermentation. Lactic acid fermentation of c e re a l and
cereal-legume blends improve the availability of certain B-group vitamins, although variation
has been observed. The major organic acids produced are lactic acid and acetic acid; these and
other metabolites contribute to the rich variety of taste and aroma of the fermented product.

• Carbohydrate digestibility. There is an enhanced nutritional quality through better

digestibility by reduction of certain oligosaccharides particularly prevalent in legumes.
This reduces side effect, such as abdominal distention and flatulence, which
customarily occur among people eating a diet which is high in oligosaccharides, such as
raffinose, stachyose and verbascose.

• Nutrient density - dietary bulk. Fermentation techniques which involve a combination

of amylase rich flour (ARF or power flour) and a small amount of a lactic starter culture
provide a considerable opportunity for increase of the nutrient density. The decrease in
viscosity enables the addition of more dry m a te r while maintaining a semi-liquid
consistency. The ARF must be added after cooking the gruel; the flour concentration
can be increased by more than 100% while still maintaining a semi-liquid consistency
regarded as preferable for feeding young children. This thinning effect is partly due to
the low pH of the fermented g ru e l but is mainly due to the effect of the amylase activity
of the germinated cereal.

Effect on anti-nutritional factors. Some cereal-based d ie t have restricted

bioavailability of n u trien t as a result of the presence of anti ^nutritional fa c to r such as phytates
and polyphenol (tannins).

• Phytate (or inositol hexaphosphate) i an abundant plant constituent and acco u n t for
60-90Ho of the total phosphorus content of the product. This is necessary for the energy
metabolism of the plant itself. Phytate content in fruitt and vegetables is
 17

generally lower than in cereals and % decreased by enzymes (phytases) and

high-temperature processing. Phytate is normally found in the form of complsxes with
polyvalsnt cations, e.g. iron, zinc, calcium and magnesium, and proteins. The
inhibition of non-haem iron absorption by phytates is dose dependent and even low
fevels (fess than 90% of w holl wheat flour phytate content) are inhibitory. Phytases are
present in most cereals and active at a pH of around 5.0. The ideal fermentation process
provides optimum pH conditions for degradation of phytate. This is obtained by initial
soaking of the flour in water for about 12-24 hours. Such a reduction in phytate
increases the amount of soluble iron several-fold. There are similar benefits for zinc
and calcium. Thus, lactic acid fermentation of maize or sorghum changes a diet of "low
iron bioavailability" into a diet of "intermediate to high iron bioavailability".

• Tannins (or polyphenols) are plant components which contrbute to protection against
plant disease and predators. They also inhibit dietary mineral absorption and protein
digestibility. The galloyl groups of polyphenol are mainly responsiMe for the
inhibiting effect on iron absorption. The tannin content of cereals i reduced by lactic
acid fermentation. hi some high-tannin cereals, however, there seems to be littls or no
improvement in iron availability after lactic acid fermentation. This is presumably due
to production of metabolites of tannins which are inhibitory to iron absorption.
Microbial fermentation improves protein digestibility of high-tannin cereal v a0 ttits.
The greatest increase in digestibility is observed in high-tannin sorghum gruels
fermented with a natural starter culture. Tannins have also an inhibiting effect on the
growth of lactic acid bacteria, thereby slowing the process of microbial fermentation.

Presence o f promoters. Vegetables generally contain low but sufficient amounts of

phytate to have an inhibitory effect on iron absorption. During lactic acid fermentation,
e.g. in "sauerkraut", phytate may be completely degraded. The amount of iron absorbed is
increased when fermented vegetables are added to a phytate-rich diet. This indicates the
presence of iron-promoting fa c to r in lactic acid fermented vegetables. Vitamin C i such an
iron-promoter; it i well-known that it i preserved in lactic acid fermented vegetables because
of the prevailing reducing conditions.

6.2 Risks

The aspectt liited below are generally supported by published experimental evidence.
However, in some cases the evidence i fragmentary and rattier re fe c tt a lack of clearly
established scientific evidence.

6.2.1 Biological

A certain number of agentt appear not to be affected by lactic acid fermentation.

However, they may be adequately destroyed by other processing operations involved in the
preparation of the food, such as cooking.
 18

There are emerging patterns of acid resistance in some enteropathogens such as

E. coli 0157:H7, where for example, fermented meats and yoghourt have been vehicles
of infection and this should be monitored closely.

Foodborne viruses are recognized as a significant cause of gastroenteritis, and rotavirus

has been identified as one of the most common causes of diarrhoea in childhood.
Enteric viruses are necessarily relatively acid stable to survive passage through the
stomach’s acidity, and unlike bacteria do not have greater sensitivity to weak organic
acids, such as lactic acid. Simian rotavirus has been shown to survive at high levels of
acidity during 24 hours storage in a model fermented weaning food. They did, however,
show increased heat sensitivity at low pH.

The diseases produced by parasites such as Cryptosporidium, Giardia lamblia, and

trematodes transmitted by foods are varied and widely distributed in all parts of the
world. There i little information on the e ffe c t of fermentation on these parasites. The
c y s t of these organiims often show resitan ce to adverse conditions although they are
generally killed by adequate cooking. For example, there are indications that c y s t of
many foodborne trematodes may survive 70°C and further studies are required to define
the precise time/temperature combinations to assure safety from these organisms, and
to assess whether the fermentation step will have an effect on their infectivity.

6.2.2 Chemical

Certain algae, bacteria and moulds can produce toxins that may be transmitted by foods.
Many of these are heat resistant and will survive normal cooking temperatures. Generally,
lactic acid fermentation will not eliminate the risk posed by these preformed toxins.

• Mycotoxins are toxic secondary metabolites that are produced during the growth of
certain moulds on foods. They may be present in the food material as a result of mould
contamination in the field or during storage in uncontrolled, hot and humid conditions.
The risk of contamination by mycotoxins of raw materials used in fermented foods is a
serious food safety hazard. Some studies have reported no reduction in the level of
mycotoxins by fermentation whife others have reported appreciabte decreases (Annex
7). Other processing steps, such as cteaning, milling, dehulling and cooking will
contribute to the reduction in mycotoxin levels. However, the precise role of microbial
fermentation in reducing the concentration of mycotoxins in foods i not well
established. From these data, it i clear that fermentation cannot be relied upon as a
means of detoxifying mycotoxin-contaminated foods.
 19

• Bacteria can cause foodborne illness either as a result of ingestion of preformed

bacterial toxins with a food (intoxication) or the ingestion of live organisms (infection).
There is no evidence to suggest that microbial fermentation alone will eliminate risk by
removing preformed bacterial toxins from food. A final cooking stage will eliminate
heat labile toxins, such as those produced by Clostridium botulinum, but cannot be
relied upon to destroy the heat stable toxins produced by other bacteria such as
Staphylococcus aureus and Bacillus cereus.

6.2.3 Physical

There i no evidence to suggest that lactic acid fermentation reduces the level of
contamination with extraneous m ater. On the other hand, in certain cases fermentation follows
a steeping step which might contribute to the removal of dirt.

6.2.4 Nutritional

Microbial fermentation has a minimal effect compared with cooking in reducing the
anti'-nutritional effects of protease inhibitors, and the toxic effects of lectins on the intestinal
epithelium.

Microbially-produced lactic acid i usually a mixture of the optical isomers L-(+) and
D -(-) lactic acid. D -(-) lactic acid cannot be metabolized by humans. Excessive intake of
D -(-) lactic acid may result in acidosis, a disturbance of the acid-alkali balance in the blood.
Liitle is known about the "toxicity" of D -(-) lactic acid for malnourished or sick children. In
addition, relatively little data is available about the D -(-) lactic acid content of fermented foods
prepared at the household level.

7. PRACTICAL INTERVENTIONS FOR IMPROVING THE SAFETY

AND NUTRITIONAL QUALITY OF FERMENTED FOODS AND
TECHNOLOGY TRANSFER

7.1 Weaknesses in present practices of fermentation, and considerations for

improvement

The constraints and shortcomings related to traditional fermented weaning foods can be
threefold: technical and safety, nutritional, and social. The complexity of the problems
necessitates a multidisciplinary approach to improve fermentation practices.

7.1.1 Food safety-' constraints

The time necessary for food processing in the traditional household fermentation
process is a constraint on the hours available to women who, as mothers and food processors,
are also engaged in child care and other household activities. Lack of time may have
 20

significant implications regarding safety and nutritional quality of fermented foods because any
time saved by cutting down on fermentation periods may jeopardize the effectiveness of
acidification by lactic acid bacteria, or the degradation of plant toxins and anti-nutritional
factors by the relevant enzymes.

Reduction of time expenditure may be achieved by accelerating the process, or by a

different distribution of labour. In the latter case, foods might be produced by entrepreneurs.
Care should be taken that no unjustified shortcuts are employed in the process which might
jeopardize the safety and nutritional value of the product.

Other food safety problems arise from shortcomings in handling/processing of foods,

resulting in different types of hazards (e.g. phytotoxins or anti-nutritional factors in the raw
materials, survival and/or growth of pathogenic organisms, contamination from the
environment). Improvement of product quality and safety could be achieved by Good
Manufacturing Practice (GMP) and Good Hygienic Practice (GHP), and by using the Hazard
Analysii Critical Control Point (HACCP) system. The latter i aimed at identification,
assessment and control of hazards throughout the process from raw material to packaging and
consumption.

7.1.2 Nutritional constraints

The limitations related to many currently-used weaning foods include:

a) low content and limited quality of protein in raw materials, mainly

c e re a l and root crops;
b) low nutrient density of the prepared foods; and,
c) poor or low bioavailability of proteins and minerals in the finished
product.

The following measures for im provem ent may be considered:

Macronutrients: The viscosity of starchy and bulky p ro d u ct could be reduced in order to

enable an increased nutrient density while maintaining an acceptable viscosity. In addition, the
protein quantity and quality could be improved by protein supplementation, e.g. by adding
legumes.

Micronutrients: Micronutrient fortification could improve the nutritional quality of the product,
provided that their bioavailability is ensured. At the household level, however, fortification
seems of lesser relevance as it might not be affordable or practicable. At all levels of
production, the bioavailability of macro- and micronutrients could be improved by strategic use
of germination and fermentation techniques.
 21

7.1.3 Sociocultural constraints

The major social constraint related to fermented foods for weaning is one of poor image
when compared to industrial preparations which are considered superior and associated with
progressiveness in some countries. Fermented foods are often poorly perceived and poorly
accepted by mothers whose responsibility it i to prepare and feed them to the children.
Another constraint here i that of a socioeconomic nature where sophiiticated processing
equipment i not affordable at the household level. In other words, the sophistication level of
the fermentation method must fit the socioeconomic framework.

The Workshop identified several areas requiring attention:

• The public image of some traditional fermented foods is poor, and should be
improved.

• An important aspect is to educate the mother or child carer, as well as the food
manufacturer, about the optimum conditions for the preparation of specific
fermented foods.

• The involvement of food manufacturers in terms of training and experimenting

with new or upgraded techniques is important. Participatorr research has
benefits for the manufacturer as well as the researcher.

• The present exchange of information between mothers, manufacturrrs,

scientists, government and non-governmental organizations needs to be
improved.

7.2 Mo del appro aches fo r improvement of fermentatio n

Interventions for improving the safety and nutrtional adequacy of traditional fermented
food should take into account:

- traditional, technical and socioeconomic aspects; and

- the needs and realistic prospects to achieve this aim.

In assessing the safety and nutrtional value of weaning foods produced by a

fermentation process, either at household or cottage level, the Workshop considered that the
assessment of socioeconomic and cultural aspects is essential to e n a b l the optimum utilization
of Sus technology for the preparation of these weaning foods. The socioeconomical and
cultural considerations should be integrated with key concepts of food safety, nutrtion,
household food security, and prevention and control of infection, if an improvement is to be
achieved in the nutritional status of infants and young children.
 22

Therefore, where fermented foods already form part of the diet of infants and young
children, it is important to examine the existing socioeconomic and cultural relations and
patterns, and identify the type of support which is needed to improve the safety and nutritional
value of the fermented foods.

7.2.1 Technical and safety-' aspects

Reduction in the processing time can be attempted using fermentation starter cultures.
In prnciple, starter cultures contains a high concentration of live microorganisms which are
added to raw m a te ra ! with the aim of achieving the desired fermentation as rapidly as possible.
At the household level several starter cultures are practicable. These include using batches of
previously fermented productt (also referred to as back-slopping), or specially prepared dry
starter cultures such as the Ghanaian inoculation belt or the Indonesian ragi and usar.

The Hazard Analysii Critical Control Point (HACCP) system could be used in order to
identify and evaluate hazards and control measures.3,4 The application of the HACCP concept
to a few selected but representative processes of A frcan fermented foods, e.g. gari (Nigeria),
togwa (Tanzania) and uji (Kenya) i illustrated in Annexes 4-6.345 The schematic presentation
of the production processes for these products are shown in Figures 3-5.

Some important safety considerations which derive from the application of HACCP to
cassava and cereal for production of gari, togwa and uji are:

• Rapid and adequatt acidification (a combination of low pH and sufficient titratable

acidity to result in an inhiiitory level of undissociated weak organii acid (m ainll lactii
and some acid acetic).

• Sufficient cooking for rendering food safe, particularly^ in terms of parasites and viruses.
If starchy meals are cooked for p a la ta b l purposes, the importance of adequatt thermal
processing for elimination or reduction of hazards should nevertlielss not be
overlooked.

3WHO. Hazard Analysis Critical Contol Point systtm: Concept and Application, Report of a WHO
Consultation with tie participation of FAO, Geneva 29-31 May 1995 (Unpublished WHO document
WHO/FNU/FOS/95.7).
4
Bryan, F. Hazard Analysis Critical Control Point Evaluations. A guide to identifying hazards and
assessing risks associated with food preparation and storage. World Health Organization, Geneva, 1992.
5A prerequisity for the application of the HACCP systtm in food processing/preparation is that the
principles of Good Hygienic Practice (GHP) or Good Manufacturing Practice (GMP) are adhered to. In principle,
Cntiia! Contol Points (CCPs) should be restriited to steps in a food operation whiih, if not controlled property,
may lead to signifieant food safety problems. In a newty-developed HACCP plan, more CCPs may be included
than are perhaps necessary. Based on a reviiw of the monitoring and verification results, CCPs may be dekttd
from the HACCP plan, if ttey turn out to be sufficiintlyf covered by GHP/GMP. The HACCP studiis presenttd in
Annexes 4-6 are models for the application of the HACCP system to fermented foods, based on a worst case
scenario, thus many sttps have been identifiid as CCPs. Depending on the situation, some of ttese sttps may not
need to be considered as CCPs. It should also be noted that model HACCP plans are not appropriate for use until
validattd for a specific food and food process.
 23

• Sufficient size reduction in cassava to enable enzymatic degradation of toxic

cyanogenic glycosides.

• Avoidance of mouldy raw materials in view of possible mycotoxin contamination.

• Using safe water.

Togwa preparation is associated with a higher food safety risk than fermented uji, as the firrt
involves the addition of power flour (or ARF) and togwa after the food has been cooked (see
Annexes 4 and 5). There i thus a risk of post-cooking contamination, particularly with
acid-resistant pathogens. For example by the addition of power flour and if the lactic acid
fermentation fails, the proliferation of bacterial pathogens may occur. Possible options to
minimize the safety risks of togwa preparation include quick (accelerated) fermentation by
back-slopping or use of other starter cultures; using ARF of high (hygienic) quality; and
avoiding post-cooking contamination.
24
 25

7.2.2 Nutrition

At the household level, it is technically feasible to increase the nutrient density of foods
while maintaining a semi-liquid consitency. It i possible to prepare porridges containing
20-25% (w/w) dry m a te r (about 1 kcal or 4 kJ per gram of porridge) which can still be
swallowed easily by a small child, using 1-5% (w/w) ARF after having cooked the starchy
cereal or root crop based food.

Likewise, it is technically feasible to enrich the protein content of such pomdges using
legumes such as soya beans or cowpeas. As a rule of thumb, a 70:30 weight ratio of starchy
staple verrus protein-rich legume will be adequate.

7.3 Alternative options in ho useh old fo od technolo gies

As a single unit operation, lactic acid fermentation provides acidity and flavour and
contybutes to the nutytional value. The acidity provides a significant microbiological stability
enabling storage at ambient temperature for a day without rsk in g associated mterobiologteal
hazards. If combined with an appropriate heat treatment, a fermentation-based process will
also minimize hazards (e.g. viruses, parasites or some anti-nutritional fa c to r) which cannot be
reduced by the fermentation process alone.

Altemati've options to fermentation-based food processing in households in developing

countres include:

1) Consumption of fresh food raw materials without fermentation or cooking. This is the
cheapest way. The r s k of foodborne infections may be high, particularty for foods of
animal origin or made with crops grown in contaminated environments. In some
foodstuffs, natural toxins may pose a severe threat to human health. The characteystic
fermentation flavour will be absent.

2) Cooking of frrsh (non-fermented) food. M orr energy is rnquirrd to cook frrsh rather
than fermented food to achiive the rnquirrd palatability^/digestit)ility^. Some of the
natural toxins and anti-nutritional factors cannot be ad eq u ate! removed by cooking
alone. The biological safety of cooked frrsh food is adequate, provided that it is
consumed immediately after cooking, and post-contamination is avoided. Left-overs
need to be rrfrigerated (<10°C) or kept hot (>60°C) as the neutral pH allows
proliferation of surviving or post-cooking contaminating microorganisms. Re-heating
p ro r to consumption is h ig h ! recommended. The characternstic fermentation flavour
will be absent.

3) The use of non-fermented (ready-to-consume) food, prrserved by canning. Generally,

the safety of canned food is high, if the product is consumed immediately after opening
the can and, in principte, no thermal energy is rnquirrd at the household tevel.
Left-overs requirr refrigeration and rn-heating, as in option 2 above.
 26

4) Dehydration (e.g. using solar energy) of non-fermented fresh produce, followed by

reconstitution and cooking. This option provides a relatively cheap way to preserve
perishable raw food materials such as roots and vegetables. Adequate solar dehydration
requires appropriate climatic conditions and hygienic practices to avoid contamination
via soil, insects, rodents, other animals and humans. The resulting dehydrated food
would require processing as in option 2 to render it palatable and safe.

However, if fermentation is culturally acceptable and desirable, it provides a valuable and

relatively cheap option, even when combined with a cooking step, as cooking a fermented
product requires less energy.

7.4 Technolo gy Transfer

7.4.1 Target groups

Where fermentation is not commonly practised and its introduction is being considered
(or being revived), the study of the socioeconomic and cultural factors is important in order to
assess the feasibility of application of the technology. In this case, the need to educate those
who will apply the technology should be particularly emphasized with respect to the fa c to r
determining the safety and nutritional adequacy of the food.

Social and cultural patterns vary tremendously from one place to another and are
subject to change over time. The impact of these patterns on food safety and nutrition as well
as solutions to the problems encountered are therefore location and time-specific. Perhaps the
only common thread i that, in all cultures and at all times, women have played and will
continue to play a prominent role in infant and young child care. Women are the key players,
either as mothers preparing food, or as decision-makers in selecting infant food. The children
play a role as consumers, but not as decision makers. Therefore, gender relations have to be
addressed in attemptt to improve food safety and nutrition.

Issues to be considered when recommending the use of fermented foods are:

• Know-how, education and practices of food handlers / households in the

preparation of fermented foods;

• Facilities for hygienic preparation of fermented foods (e.g. starter cultures,

materials, fuel);

• Environmental conditions, such as the quantity and quality of water and the
sanitary conditions;

• Environmental pollution, detrimental ecological conditions and biological

changes in the environment, e.g. the emergence of resistance of pathogens;
 27

Agronomic, food storage, food processing, and food marketing practices;

Consumers’ purchasing power, and their access to markett;

Family and social structures;

Caring capacity for the infant, e.g. time available to mothers;

Food choice and acceptability of fermented foods; and

The level of education in general, and as related to food safety and nutrition in
particular.

7.4.2 Policies

The introduction of food and nutrition know-how should be seen in the light of a
country’s overall development. Important issues at stake are access to shelter, safe
drinking-water, wholesome food and education. Appropriate policies should be developed,
supported and implemented by relevant government agencies. Specific technologies should be
tested in multi'-facetted pilot projects, during which implementation is closely monitored with
a continued feed-back from the community.

Transfer of know-how i a continuous process, and one in which the following parties
play an important role:

Government authorities especially those responsible for public health and food control:

- to adopt and implement policies, where appropriate, regarding the improvement

of water quality, control of agricultural residues, promotion of improved crop
cultivarr (acceptable to subsistence agriculture) at the level of the household;
and

- to develop and implement a two-way communication mechaniim between the

central government offices and the household to facilitate education.

International agencies: to participate in the development and introduction of policy and in the
implementation of project.

Non-governmental organizations: to contribute to the process of policy making and

implementation of policies.

Public educators: including teachers and consumer groups engaged in food and nutrition and
health care education. This includes formal and non-formal education structures (community
forums, newspapers and media).

Scientists/academia: to assist in research and education in food technologies, and fermentation

 28

in particular.
 29

8. RESEARCH NEEDS

A comprehensive overview of the research on fermented foods used throughout the

world was presented during the Workshop. The current status of research was assessed with
particular emphasit on understanding the potential and effects of using fermented foods as
weaning foods. The crucial questions addressed were:

• With our current knowledge of fermented foods, can the use of these foods
be promoted as safe and nutritional foods, particularly for infants and young
children?

• Whether future research is required to improve the safety of fermented foods

used at the household level?

• With the worldwide importance of small-scate food processing enterprises

(i.e. cottage industries), what are the research prorities to ensure that
fermented foods are safe for the consumer?

• What are the socioeconomic and cultural issues that need to be addressed to
ensure that fermentation is adopted both at the household and cottage tevels?

Each identifted research need was anatysed to determine the relative research
prority, taking into account the state of the current knowledge and the severity of the
problem. It will be essential in any of these studies to take into account differences between
rural and urban dwellerr.

Research issues in four areas were considered, namely: food safety, mhritional
value, technology development, and technology transfer and related socioeconomic aspect.

8.1 Fo od Safety

8.1.1 Efficiency of fermentation in biological safety

A considerable amount of work has been done on the effectiveness of lactic acid
bacteral fermentation for the inhibition of a wide range of pathogenic bacteria. A
meta-analysit would enable a quantitative analysit of these data for trends. Mathematical
m o d e l describing the survival of pathogens in lactic acid fermentation would have a useful
predictive value without recourre to challenge testing. A few research opportunities exitt in
thit area specifically related to the survival of sub-lethally injured organitms and certain
acid-tolerant pathogens such as Escherichia coli 0157:H7.

Little information exists on the destruction of parasites (such as trematodes) during

fermentation. Limited information t available on the fate of viruses during fermentation, but
there is still need for some further studies on their survival. Part of the reason for the lack of
information on viruses and parasites t associated with the problems of enumerating them.
 30

It is essential that a multidisciplinary approach to these problems is taken. It is very unlikely

that the growth of mycotoxigenic fungi represents a problem in anaerobic fermentations.

In studies on the efficiency of fermentation in the inhibition of pathogenic

microorganisms, it is important to distinguish between those present in raw materials and those
introduced into the product during and after processing (for example, after cooking).

Laboratory observations of the inhibition of pathogenic organisms need to be verified

under household conditions.

Research i needed on the epidemiology of diarrhoea among infants and young children
who are receiving fermented or non-fermented foods. Such studies will require very careful
control of epidemiological design for the confounding variables and the differences that might
occur between experimental and control groups. It is recommended that a carefully produced
protocol is subjected to widespread critical peer review before the implymentation of the
studies.

Research needs:

To determine effects of lactic acid fermentation on parasites and undertake more

confirmatory studies on the effect of the process on viruses. [High priorty]

To establish the effect of fermentation on sub-lethally injured pathogenic bacteria and

certain pathogens such as Escherichia coli 0157:H7. [High prority]

To determine the effect of the consumption of fermented foods on the incidence of

diarhoea by studying the epidemiology of diarhoea among in fa n t and young children
receiving fermented or non-fermented foods. [High priorty]

To undertake a meta-analysii of c u re n t literature on the inhibition of pathogenic

bacteria and the development of approprate mathematical m o d e l for assessing safety.
[Medium priority^]

To verify laboratory observations of the inhibition of pathogenic organisms under

household conditions. [Medium prority]

Overall, research in this area is considered to have a high priority

 31

8.1.2 Effect of fermentation on biochemical/chemical toxicants in raw materials

Fermentation cannot be seen as a means of cleaning up contaminated raw materials.

However, recognizing that contaminated raw materials are frequently used, further research on
a number of issues is justified. The importance of water quality in the fermentation processes
must also be addressed.

Limited information is available on the effect of fermentation on mycotoxins. Some

information exists with respect to aflatoxin. Very little is known about the effect on bacteral
toxins that might be present. Toxicity of mycotoxin breakdown products is largely not
understood. Further work is justified in these areas, but the long-term solution lies in
improving raw material quality.

Consideration needs to be given to the effect (including changes to bioavailability) of

fermentation on environmentally-acquired (in food and soil) chemical contaminants, such as
heavy metals, trace elementt, herbcides, and pesticides.

Research needs:

• Effect of fermentation on mycotoxins and on the toxicity of breakdown products. [High

prority]

• Effect of fermentation on environmental contaminants. [Medium prority]

• Effect of fermentation on bacterial toxins. [Low priorty, because of focus on d red

grains]

Overall, research in this area is considered to have a medium priority

8.1.3 Additional considerations in the promotion of fermentation

The extent of knowledge on the potential problem of D-lactate acidosis is limited.

Studies need to be undertaken to determine whether a problem with D -(-) lactate acidosis
exists or potentially exists when fermented foods are consumed. There is a need to specifrcally
consider the situation with regard to m alnourshed children who may have impaired buffering
capacity.

Care should be exercised to ensure that the generation of biogenic amines or other toxic
m aterals such as ethyl carbamate does not occur. This could be done by the optimization of the
varous processing steps involved in the preparation of fermented foods. This is considered to
have low to m e d im prority because of the reporttd lack of a p ro b lm with fermenttd cereal
and lg u m e foods.
 32

Research needs:

Investigation into the significance of D -(-) lactate acidosis associated with the
consumption of fermented foods. [High priority]

Optimization of processing with respect to biogenic amines and ethyl carbamate

(ethylurethane). [Low to medium priority]

Overall, research in this area is considered to have a high priority

8.2 Nutritional value

A major objective is to provide infants and young children with products of high
nutritional value. It is important to consider the whole process in relation to nutritional value
and not just the fermentation step.

The reduction in the levels of anti-nutritional factors is important, but it is important to

understand the mechanism by which changes occur. For the purpose of this review of research
needs, cyanogenic glucosides are considered in this section.

Anti-nutritional Present status of Severity of Research need

factors knowledge problem

Phytate good (some gaps) high medium-high

Tannins moderate high high

Protein inhibitors moderate high medium

Others (lectins, poor high medium

saponins)

Oligosaccharides moderate high medium-high

Cyanogenic good medium relatively low

glucosides
 33

O f equal importance to reduction of anti-nutritional factors is the improvement of the

bioavailability of micronutrients. It is important to compare the micronutrient status and
growth of infants and young children fed fermented and non-fermented cereals.

There is a need to investigate the mechanisms in the fermentation process that influence
the bioavailability of nutrients, especially iron, zinc, calcium and protein.

Research needs:

Reduction in levels of anti-nutritional fa c to r focusing specifically on the mechanisms

of change during the whole process. [Medium to high priority]

Investigation of the mechaniims in the fermentation process that influence the

bioavailability of nutrients, especially iron, zinc, calcium and protein. [Medium to high
priority^]

Comparison of the micronutrient status and growth of children under five fed
fermented and non-fermented cereal. [Medium priority]

Overall, research in this area is considered to have a medium-high priority______

8.3 Technology development

8.3.1 Characterization of fermentations

There has been a large amount of work on the microbiological characterization of

fermented foods. Justification for future work is relatively low with the exception of the need
to understand the dynamics of natural fermentations. Those fermentations that have not been
studied should be considered.

Extensive documentation exists on the methods of processing fermented foods. There

are some gaps in the literature and there is a need to verify the existing data. The dissemination
of currently available information has a high priority.

Research need:

Characterization of previously uninvestigated fermentations, especially where they are

used or could be used for feeding infants and children. [High priority]
 34

8.3.2 Development/improvement of fermentation systems

It is recommended that research on starter cultures adopt the following approaches:

a) Determination o f the needfor andfeasibility o f using starter cultures. Specific

attention should be given to cost:benefit analyses and processor/consumer requirements. The
level of knowledge in this area is low and hence the priority for research is high.

b) Establishment o f the appropriate level o f technology. This might range from the use of
back-slopping to the use of defined starter cultures with specific biochemical properties. The
approach taken is diitated by the needs of the target groups (a) and an understanding of the
scale and nature of operation. There is a reasonable level of knowledge on some aspects of this
subject and hence research is given medium priority.

c) Development o f appropriate starter culture delivery mechanisms. Mechanisms for the

distribution and maintenance of starter cultures must be developed with a good understanding
of the conditions under which they will be used and their cost. Little work has been done in this
area and the need for research is high, provided that the selected level of technology demands
it.

d) Selection o f microorganisms 'with desirable properties. Such properties might include

the possession of phytase acti've at low pH values and high levels of acid production. Whereas
there is a moderate amount of knowledge on this subject, further research should recei've high
prority where issues a, b, and c above have been p ro p e r! addressed.

Based on a sound understanding of the changes that occur during fermentation and
knowledge of consumers and/or processor requirements, there is the potential to optimize
fermentation conditions to provide a range of benefits. This provides an alternatse to the
development of starter cultures.

Research needs:

• Development of appropriate starter cultures for lactic acid bacteral fermentations,

according to the sequence of activities mentioned above. [High priorty]

• Optimization of fermentation conditions to achieve specific b en efit. [High priorty]

 35

8.3.3 Probiotics

The consumption of ll've lactic acid bacteria (such as Lactobacillus acidophilus) is

thought to help prevent diarrhoeal disease. Such effects are desirable for weaning foods. The
feasibility of using microorganisms as probiotics should be assessed. It will be important to
take into account problems of starter culture development (see above), acceptability to the
consumer, distribution and maintenance of starters, and the fact that many gruels are boiled
before consumption.

Research need:

Determination of the feasibility of the use of specific microorganisms with probiotic

activities. [High priority]

8.3.4 Effects of each processing stage on food safety

It i important to understand the role that individual and combinations of processing

stages play in the safety of the final product. Such processing operations include cooking,
washing, peeling, grinding, dehydration, packaging and fermentation. An example of thii i
the order of cooking and fermentation in the preparation of weaning g ru e l. Changing the order
of these stages has implications for food safety.

Research need:

Investigation (HACCP studies) into the role of individual processing steps and
combinations of steps in ensuring food safety. [High priority, but only where there are
specific gaps in knowledge]

8.3.5 Application of quality and safety' systems (including HACCP)

Few studies have assessed fermentation as a household level technology in terms of

food quality and safety. The application of the HACCP approach and the principles of good
manufacturing practice offer great potential for focusing education and extension programmes.
 36

Research needs:

To assess the hazards and risks associated with the household preparation and
processing (biological, chemical, physical) of infant foods. [High priority]

To determine the Critical Control Points in the processing and preparation of fermented
weaning foods at the household level with respect to food safety and quality. [High
priority^]

To determine the most appropriate means of transferring knowledge of improved

procedures in safety and quality. [High priority]

Overall, research in this area is considered to have a high priority

8.4 Technology transfer and related socioeconomic aspects

8.4.1 Consumer and producer perception and needs

Research is needed to understand consumer and producer (processor) perception of

food safety and specifically of fermentation. It i not known whether food safety i a significant
enough i s u e in %s own right for these target groups to adopt fermentation or change traditional
practices. For example, if fermented food i being promoted as a means of reducing the
incidence of diarrhoeal diseases in children, the benefits to the household have to be obvious if
change is going to take place.

There are many reasons and advantages for using fermentation, including extending
shelf-stability, addition of variety to the diet, as an income generating activity, nutritional
benefits, and processing otherwise unusable raw materials. Even with these advantages, there
are some communities that have discontinued using fermentation processes.

The initial stage in safety improvement of a fermentation process i understanding why

that process i used. TIus would be an important part of a needs assessment, which should be
carried out as an initial step in any research programme. The needs assessment should also
determine what the perceived is u e s and problems are for both the processor and the consumer.

It may be possible to make changes to exiiting fermentation systems or introduce a

fermentation process for food safety purposes if one can also demonstrate advantages such as
extended shelf-life, cost savings, reduction in processing time, and improvement in taste or in
nutritional quality. T - s requires an understanding of consumer and processor needs and
perceptions. If fermented products are to be promoted as safe weaning foods, i is particularly
important to evaluate the contribution that these foods make to the nutritional needs of the
child.
 37

During the implementation of any research project, it % crucial to have continuing

interaction between scientists, processor and end-userr to ensure that any changes to the
process or product are acceptable, practical and cost-effective.

Research needs:

To gain a greater understanding of consumer perceptions of food safety and the

significance of thii with respect to modifying food processing practices. [High priority]

To gain an understanding of the needs and perception of processor in relation to their

use of fermentation and potential adoption of the technology. [High priority]

To evaluate the potential contribution of fermented foods to the daily nutritional

requirem ent of weaning in fa n t and children. [High priority ]

To determine why the use of a particular food fermentation has been discontinued, or
continued in certain communities. [Medium priority]

Overall, research in this area is considered to have a high priority

8.4.2 Transfer of information and technology to meet the needs

of the target groups in relation to food safety-'

The requirement for needs assessment studies was emphasized elsewhere in thii Report.
It is essential that such studies form an integral part of any project and are carried out not only
at the beginning, but also during and after project activities. It i important to include target
groups in the research exercise thereby considering them as partners rattier than observers.
Monitoring and evaluation are essential partt of the project cycle to determine whether or not
an approach i effective and allows for corrective measures.

Adaptive research (pilot studies) i required to develop and modify technologies in

partnership with target groups. Pilot studies can also be a useful tool in assessing the most
appropriate means of technology and information transfer. It is important to recognize that
different approaches will be required according to the scale of operation, for example the
dissemination of fermentation and associated training may be appropriate at the household
level. There is a need to understand the most approprate mechanisms of education and
communication to facilitate rapid and sustainable technology adaptation. In the transfer of
technology/information on food fermentation, there might also be an opportunity to transfer
other information such as that related to health, hygiene, food safety and nutrtion.
 38

Research needs:

• Adaptive research to develop and adapt processes. [High priority]

• Determination of appropriate mechanisms of education and communication. [High

priority^]

8.4.3 Research issues relevant to the household

The driving force behind the adoption of fermentation for domestic use, including
infant feeding, i food security. Safety is u e s are important, but probably have a lower profile
from the mother’s perspective than from the commercial perspective. Key issues will include
quality of raw materials, ease of processing, energy use, and the extension of shelf-life for use
within the home. The role of women i a specific issue that will determine the nature of the
technology and how it i transferred. It will be important to make changes in small incremental
steps so that the development i sustainable. One suitable approach may be the development
and diisemination of fermentation kits.

8.4.4 Research priorities relevant to cottage industry

The adoption of fermentation at the commercial level i driven by the need to make a
profit. Food regulation i a significant consideration in some countries. The research priorities
of relevance are dictated by these isu e s. Starter cultures may be more relevant in S - s case than
for domestic use, and the application of the principles of good manufacturing practice and other
quality/safety criteria should be appropriate. Safety will have a high profile since it contributes
to a commercial reputation. Product distribution issues are critical, and this would be expected
to be a driving force behind the need to extend shelf-life.
 39

9. CONCLUSIONS AND RECOMMENDATIONS

9.1 Conclusions

9.1.1 General

Lactic acid fermentation can contribute towards the safety, nutritional value, shelf-life
and acceptability of foods for infants and young children. It is an advantageous technology, in
the sense that extension of shelf-life, enhancement of sensory properties, safety and improved
nutritional value are achieved by one technique which is affordable at the household level.

On %s own, fermentation cannot eliminate all food-related health risks, but S s b e n efit
can be enhanced when combined with other unit process operations such as soaking, grinding
and particularly cooking. Though shortcomings in the use of fermentation as a household food
technology exist, options and solutions have been identified and proposed. There is a great
need to ensure that existing knowledge of the fermentation technology is used for the maximum
benefit of households and cottage industries.

The education of food handlers and consumers about the proper application of
fermentation as part of the total food preparation process is essential.

The assessment of socioeconomic and cultural a sp e c t is essential to enable the

optimum utilization of fermentation technology for the preparation of weaning foods. The
socioeconomical and cultural considerations should be integrated with key conceptt of food
safety, nutrition and household food security, and prevention and control of infection and care,
if improvement is to be achieved in the nutritional status of infants and young children.

9.1.2 Safety-'

Major benefits include the inhibition of growth of most pathogenic bacteria, the
inhibition of formation of bacterial toxins, and the degradation of some plant toxins
e.g. cyanogenic glycosides.

In combination with other regular food preparation operations such as cleaning,

cooking and appropriate hygiene, adequate protection is provided against most foodborne
diseases of microbial and chemical origin. An exception should be made for pesticide and
mycotoxin contamination occurring in the raw food materials. These are mostly not affected
by fermentation or other process operations usually accompanying the fermentation step.

The prevalnce of diarrhoea among infants and young children is influenced by the
interaction of organisms in the environment (water, food, soil), hygienic behaviour, the
virulence and number of organisms and prior health and nutritional status of the host. Despite
the favourable effect of fermentation on contamination le v e l in food, it is not yet known
whether the use of fermented food will additionall! protect against diarrhoea when all the
above variables are controlled.
 40

9.1.3 Nutritional value

Preparation of foods of plant origin by processes involving fermentation contributes to

the degradation of some anti ^nutritional facto r, e.g. phytate, thus increasing mineral
bioavailability, to the improvement of the protein digestibility of tannin-rich cereals, and to the
improvement of carbohydrate tolerance by degradation of flatulence causing oligo-saccharides.
When germinated cereal grains are included as an ingredient in fermented weaning foods,
reduction of viscosity enables the preparation of semi-liquid porridges with increased nutrient
density.

9.1.4 Shelf-life

In the absence of facilities for refrigeration and/or hot-holding, lactic acid fermentation
provides an affordable method to extend the shelf-life of food. However, good care should be
taken to ensure that fermentation results in rapid and adequate acidification.

9.1.5 Acceptability-'

Lactic acid fermentation provides a variety of tastes to otherwise bland foods.

9.1.6 Research needs

High priority research needs were formulattd within the areas of food safety,
nutritional value, technology development, and technology transfer and related socio-economic
aspects. Some major questions to be resolved include the effect of lactic acid fermentation on
the fate of parasites, viruses and certain pathogenic bactera; the effect of fermentation on
mycotoxins and the toxicity^ of breakdown products; the significance of D-(-) lactate acidosii
associated with the consumption of fermented foods; the effect of fermentation on the
anti--nutritional impact of tannins on nutriint bioavailability; charact&0zation of hitherto
uninvestigated fermentations; development of approprate starter cultures; optimization of
fermentation conditions to achieve specific benefits; feasibility of the use of probiotic
microorganiims; development and application of quality and safety systems (including
HACCP); assessm ent of consumer and producer perception of fermentation and needs;
assessment of approprate mechanisms of communication and education; and transfer of
information and technology to households and cottage industries through adaptiie and
participatory pilot projects.

9.2 Recommendations

9.2.1 Policy m aters

The present exchange of information between mothers, manufacturers, scientists,

government and non-government organizations needs to be improved.
 41

It is recommended that medical, health, technological and sociological services are

integrated to coordinate efforts against foodborne diseases, with food fermentation as an
integral part of this action.

Safety considerations should be integrated when fermentation is advocated and

promoted for nutritional purposes.

In communities where lactic acid fermentation is usually caried out, this practice
should be encouraged while educating the food handlers, in line with the HACCP approach,
about the critical points in the process for controlling the safety of the products. Existing
socioeconomic and cultural relations and patterns should be examined, and the type of support
which is needed to improve the safety and nutritional value of fermented foods should be
identified. Appropriate communication strategies and means should be developed and applied,
to inform households about the appropriate food processing techniques with respect to
fermentation.

If lactic acid fermentation i not known or used, a sociocultural assessment should be

made of the appropriateness and feasibility of fermentation practice in that community, and its
food safety and nutrtion implications, prior to any attempt to formally introduce fermentation
technology.

Education or development of communication strategies should be based on KAP

(a methodology for the assessment of Knowledge, Attitudes, and Practices) and HACCP
studies, from which community needs will be derived. On the b a s i of these identified needs,
information can be disseminated, preferably utilizing existing and already well-established
strategic.

9.2.2 Research

Research in the high priorty areas as mentioned above and listed in more detail in
section 8 should be promoted and supported. The execution should preferably have a
collaborative and multidisciplinary character.

A follow-up to this Workshop, e.g. in the form of a “forum”, touching on all the m aters
referred to in these recommendations should be planned in the near future.

A network of scientists should be established to facilitate exchange of information,

coordination of research efforts, and dissemination of results. Such a "food fermentation
network" should be adequately affiliated with international professional organizations,
governments and NGO's.

GLOSSARY

Acidosis
A pathologic condition resulting from accumulation of acid or loss of base in the body, and
characterzed by increase in hydrogen ion concentration (decrease in pH).
 42

ARF
Amylase Rich Flour. See also: Power Flour.

Back-slopping
The practice of employing material from previous successful batches as a fermentation starter
culture. In fermentation of cereals, root crops and leguminous seeds (beans, pulses),
back-slopping usually results in a gradual dominance of lactic acid bacteria.

Contaminant
Any biological or chemical agent, foreign m a te r or other substance present in the food - not
intentionally added - which may compromise food safety or suitability.

Control (verb)
To take all necessary actions to ensure and maintain compliance with established criteria.

Control (noun)
The state wherein c o re ct procedures are being followed and crteria are being met.

Control measure
An action or activity that can be used to prevent or eliminate a food safety hazard or reduce it
to an acceptable level.

Corrective action
A type of action to be taken when the results of monitoring the CCP indicate a loss of control.

Critical Control Point (CCP)

A step at which control is essential to prevent or eliminate a food safety hazard or reduce it to
an acceptable level.

Critical limit
A value which separates acceptability from unacceptableness.

ERF
Enzyme Rich Flour. See also: Power Flour.
 43

Fermentation
A desirable process of biochemical modification of primary food products brought about by
microorganisms and their enzymes. Fermentation is purposely carried out to enhance taste,
aroma, shelf-life, texture, nutritional value and other attractive properties of food.
Fermentation is often part of a sequence of process operations including one or more of the
following: cleaning, grinding, soaking, salting, cooking, packaging, and diitritiution.

Fermentation (characterization o f%:

The investigation and description of microbiological, chemical and other relevant changes
taking place during a fermentation. Characterization of fermentations i required to understand
the fa c to r and substances affecting food quality and safety.

Foodborne disease
A disease, usually either infectious or toxic in nature, caused by agents that enter the body
through the ingestion of food. The term ‘food’ includes drinking-water, or water used in food
preparation.

Food safety (state)

Assurance that food will not cause harm to the consumer when it i prepared and/or eaten
according to its intended use.

Food safety (measure)

All conditions and measures that are necessary to ensure the safety and suitability of food for
human consumption at all stages of the food chain.

Food hygiene, Food sanitation

For the purpose of thii Report, these terms are considered as synonymous to food safety
(measure).

Good Manufacturing Practice

Practices employed by food manufacturing enterprises that are necessary to produce quality
food productt conforming to food laws and regulations.

Good Hygienic Practice

Practices during food handling that are necessary to conform with basic food hygiene rules.

HACCP system
A scientific and systematic way of enhancing the safety of foods from primary production to
final consumption, through the identification, evaluation and control of hazards which are
significant for food safety.

Hazard
A biological, chemical or physical agent in, or condition of, food with the potential to cause an
adverre health effect.
 44

Household technology
The combination of methods, utensils and manual labour, as are available in the average home.
It may happen that certain steps in food preparation, e.g. grinding, need to be performed for a
fee, using equipment and know-how from outside the household. Household technology is
primarily' used to feed the household, i.e. a family group eating from the same pot. In this case,
a direct link exists between the person preparing the food and the family consuming it. The risk
of adulteration is low, and usually the products are not subject to official food inspection.

When food is prepared on a large scale for commercial purposes, the term ‘enterprise’
is used. This may mean a single entrepreneur, small cottage- or village-based enterprises, or
even semi-industrial ones, all depending on the scale of production, the number of employees
and the level of capital investment. Even in an industrial setting much of the technology
employed could still be regarded as "household technology", as described above in terms of
methods, equipment and low degree of technical sophistication. However, commercial
production activities may involve more complicated channels leading from producer to
consumer. This increases the risk of adulteration; thus such products are, or should be, subject
to official food inspection.

Inoculation belt (as used in Ghana)

Belt of woven plant fibre used as a fermentation starter culture, e.g. in the traditional brewing
process of "pito", a maize-sorghum beer. The belt i held suspended in the vessel during
fermentation and serves as an attachment site for the predominant microorganiims, in thii case
lactic acid bacteria and y e ast. Towards the end of the fermentation, the belt i removed, gently
dried and kept until required for the next fermentation.

L-(+) and D-(-) Lactic acid

Lactic acid i optically active as it contains an asymmetric carbon atom. The two mirror-image
optical isomerr L-(+) and D -(-) lactic acid are rotating the axii of polarized light to the right
and lef t., respectively. L-(+) lactic acid can be metabolized by man, whereas D -(-) lactic acid
is absorbed by the human body but not metabolized. Consequently, if consumed in large
quantities it may result in acidosis. Lactic acid bacteria produce a mixture of the two optical
isomerr in a ratio characteristic for their species.

Monitor
The act of conducting a planned sequence of observations or measurements of control
param eter to assess whether a CCP i under control.

Power flour
Germinated cereal grain (mostly sorghum or millet), either dried in the sun or artificially at
temperatures not exceeding 50°C, and ground to flour. This material, also referred to as malt,
contains active starch degrading enzymes which enable the liquefaction of a stiff gelatinized
gel of cooked starch (such as cooked cereal or root crop-based food). The sudden change in
viscosity explains the name of the product.
 45

Ragi (as used in Indonesia)

A common name for a dried and shelf-stable rice flour-based fermentation starter culture. For
example, ragi tape is used as a starter culture to ferment glutinous rice to tape ketan\ this
particular ragi contains a mixed starter culture of an amylolytic mould (Amylomyces rouxii), a
yeast (Hyphopichia burtonii) and some lactic acid bacteria. The starter culture is prepared in
the household or in cottage industry, in the shape of coin-sized tablets, which can be crushed
and sprinkled on the material to be fermented.

Starter culture
A starter culture is defined as material containing a high concentration of live microorganisms
which is added to raw food materials with the intent of speeding up the process of fermentation.
Lactic acid fermentation is often promoted by adding large numbers of active lactic acid
bacteria. Most simply this could be done by back-slopping.

S ep 6
A point, procedure, operation or stage in the food chain, including raw mattri^ls, from primary
production to final consumption.

Usar (as used in Indonesia)

A d re d and shelf-stable starter culture used to ferment soya beans to tempe kedele, a
mould-fermented soya bean cake. Plant leaves (such as Hibiscus tiliaceus) which have a rough
surface, to which the fermentation microorganism (moulds such as Rhizopus oligosporus in
this case) are able to attach are used. After growing the mould sandwiched between leaves, the
latter are sun-dried. The m ateral to be fermented (cooked soya beans) is rubbed between some
leaves of usar in order to transfer the mould spores from the starter culture to the beans. The
used usar leaves are then discarded.

6 In relation to the HACCP system

 43
ANNEX 1
LIST OF BACKGROUND PAPERS
The following is a list of papers presented by the some of the participants at the Workshop.
Copies can be obtained by writing to the authors. The address given here is that of the first
author.
Title
Review of the sensitivity of different
foodborne pathogens to fermentation
Use of Starter Cultures in Fermentation
on a Household Scale
Household Food Safety in Developing
Countries with regard to Fermented Foods
Lactic fermented foods and their benefits
in Asia
Fermentation - The key to food safety assurance
in Africa?
Contaminated weaning food: a major risk
factor for diarrhoea and associated
malnutrition
A uthor
M.R. Adams and L. Nicolaides, School
of Biological Sciences, University of
Surrey, Guildford, Surrey GU2 5XH, UK
W. Holzapfel, Institute of Hygiene and
Toxicology, Federal Research Centre for
Nutrition, Engesserstrasse 20, D-76131
Karlsruhe, Germany
Z. Merican, Senior Research
Officer, Food Technology Research
Centre, Malaysian Agricultural Research
and Development Institute (MARDI),
P.O. Box 12031, G.P.O., 50774 Kuala
Lumpur, Malaysia
C.-H. Lee, Department of Food
Technology, College of Natural
Resources, Korea University, 1
Anam-dong, Sungbuk-ku, Seoul, 136-701
Korea
P. Mensah, Noguchi Memorial Institute
for Medical Research, P.O. Box 25,
Legon, Ghana
Y. Motarjemi, F. Kaferstein, G. Moy and
F. Quevedo. Food Safety Unit,
World Health Organization, 20, Avenue
Appia, CH-1211 Geneva 27, Switzerland.
 44
Title Author

Technological aspects of preparing M.J.R. Nout and P.O. Ngoddy

affordable fermented weaning foods Department of Food Science,
Agricultural University, Bomenweg 2,
6703 D Wageningen,
The Netherlands

Lactic fermented foods in Africa O.B. Oyewole, Department of Food

and their benefits Science and Technology, University of
Agriculture, P.M.B. 2240, Abeokuta,
Ogun State, Nigeria

Food Safety and Fermented Foods in F. Quevedo, Food Quality and Safety
in Latin America Assurance International, Las Petunias,
140, Dpto 201, Lima 12, Peru

Socio-economic pitfalls of enhancing T. van de Sande, Soerlaan 17,

indigenous capabilities in household 1185 JG Amstelveen, The Netherlands
fermentation

Classification of fermented foods: K.H. Steinkraus, Cornell University,

Worldwide review of household 15 Cornell Street, Ithaca, New York 14850
fermentation techniques USA

Fermentation and nutrient availability U. Svanberg and W. Lorri,

Chalmers University of
Technology, c/o SDK; Box 5401,
40 229 Goteborg, Sweden

Review of the effect of fermentation A. Westby, A. Reilly and Z. Bainbridge

on naturally occurring toxins Natural Resources Institute, Overseas
Development Administration, Central
Avenue, Chatham Maritime, Kent ME4
4TB, UK
 45
ANNEX 2

LIST OF PARTICIPANTS

Prof. John W. Hastings, Department of Genetics, University of Natal, Pietermaritzburg, Republic

of South Africa

Prof. Alex von Holy, Department of Microbiology, University of the Witwatersrand,

Johannesburg, Republic of South Africa

Dr Cherl-Ho Lee, Professor of Food Engineering, Department of Food Technology, College of

Natural Resources, Seoul, Korea

Dr Wilbald Lorri, Managing Director, Tanzania Food and Nutrition Centre, Dar es Salaam,
Tanzania

Prof. S.K. Mbugua, Department of Food Technology and Nutrition, College of Agriculture and
Veterinary Sciences, University of Nairobi, Kabete, Kenya

Dr Patience Mensah, Head Bacteriology Unit, Noguchi Memorial Institute for Medical Research,
University of Ghana, Legon, Ghana

Dr M.J. Robert Nout, Department of Food Science, Agricultural University, Wageningen,

The Netherlands (.Rapporteur)

Dr Olusola B. Oyewole, Department of Food Science and Technology, College of Agricultural

Management, Rural Development and Consumer Studies, University of Agriculture, Abeokuta,
Ogun State, Nigeria (Chairman)

Prof. Fernando Quevedo, Executive Director, Food Quality & Safety Assurance International,
Lima, Peru (Vice-Chairman)

Dr Theo van de Sande, Vrije Universiteit, Amsterdam, The Netherlands

Dr Morenike O. Sanni, Department of Human Nutrition, College of Medicine, University of

Ibadan, Ibadan, Nigeria

Prof. Keith H. Steinkraus, Professor Microbiology emeritus, Cornell University, Ithaca, New York,
USA

Dr U lf Svanberg, Department of Food Science, Chalmers University of Technology,

Goteborg, Sweden

Prof. Andrew Tomkins, Director, Centre for International Child Health, Institute of Child Health,
University of London, London, UK

Dr Jocelyn Webster, Division of Food Science and Technology, Council for Scientific and
Industrial Research, Pretoria Republic of South Africa

Representatives o f Other Organizations

 46

Association of African Universities (AAU): Prof. O. Onayemi, African Universities House,

Accra-North, Ghana
[unable to attend]

European Union (EU), Brussels, Belgium

[unable to attend]

Industry Council for Development (ICD): Ms Zahara Merican, Malaysian Agricultural Research
and Development Institute, Kuala Lumpur, Malaysia

International Commission on Food, Microbiology and Hygiene (ICFMH):

Dr Wilhem H. Holzapfel, Institute of Hygiene and Toxicology, Federal Research Centre for
Nutrition, Karlsruhe, Germany

International Commission on Microbiological Specifications for Foods (ICMSF):

Ms Zahara Merican, Malaysian Agricultural Research and Development Institute, Kuala Lumpur,
Malaysia

International Foundation for Science (IFS): Dr Richard Fuchs, Scientific Secretary, Stockholm,
Sweden

International Life Sciences Institute (ILSI), Washington, USA

[unable to attend]

International Union of Food Science and Technology (IUFoST): Dr Lilian Marovatsanga,

Institute of Food, Nutrition and Family Sciences, Harare, Zimbabwe

International Union of Nutritional Sciences (IUNS): Dr M.J. Robert Nout, Department of Food
Science, Agricultural University, Wageningen, The Netherlands

Overseas Development Administration (ODA): Dr Andrew Westby, Natural Resources Institute,

Kent, UK

South African Association for Food Science and Technology (SAFST): Prof. Alex von Holy,
Department of Microbiology, University of the Witwatersrand, Johannesburg, Republic of South
Africa

United Nations Children’s Fund (UNICEF): Dr Joan Matji, Nutrition Consultant, Pretoria Office,
Republic of South Africa

United Nations Industrial Development Organization (UNIDO): Vienna, Austria

[unable to attend]
 47
Observer

Mrs Ina Willken, Consumer Council, Pretoria, Republic of South Africa

Secrrtariat

Dr Gabriel Kouthon, Senior Officer (Food Industries), Food and Agricultural Industries
Service, Agricultural Support Systems Division, FAO, Rome, Italy (Co-Secretary)

Dr Yasmine Motaijemi, Food Safety Unit, WHO, Geneva, Switzerland (Co-Secretary)

M r Alan Reilly, Food Safety Unit, WHO, Geneva, Switzerland

Dr Martin Adams, School of Biological Sciences, University of Surrey, Guildford, UK

(Temporary Adviser')

Local Organizers

Ms Leoni Bosman, Division of Food Science and Technology, Council for Scientific and
Industrial Research, Pretoria, Republic of South Africa

M r Dave Harcourt, Division of Food Science and Technology, Council for Scientific and
Industrial Research, Pretoria, Republic of South Africa

Ms Brenda Liebenberg, Dietitian, Directorate Nutrition, Department of Health, Pretoria,

Republic of South Africa

Ms H e Meyer, Division of Food Science and Technology, Council for Scientific and Industrial
Research, Pretoria, Republic of South Africa

Ms F W J van Rijssen, Deputy Director, Food and Chemicals, Department of Health, Pretoria
Republic of South Africa

Dr Theo van de Venter, Director of Food and Chemicals, Department of Health, Pretoria,
Republic of South Africa

Dr Jocelyn Webster, Division of Food Science and Technology, Council for Scientific and
Industrial Research, Pretoria, Republic of South Africa

M r Johan de Wet, Division of Food Science and Technology, Council for Scientific and
Industrial Research, Pretoria, Republic of South Africa
 48
ANNEX 3
BASIC PRINCIPLES FOR THE
PREPARATION OF SAFE FOOD FOR INFANTS AND YOUNG CHILDREN1
• Cook food thoroughly
Many raw foods, notably poultry, raw milk and vegetables,
are very often contaminated with disease-causing
organisms. Thorough cooking will kill these organisms.
For this purpose, all parts of the food must become
steaming hot, which means they must reach a minimum
temperature of 70°C.
• Avoid storing cooked food
Prepare food for infants and young children freshly, and
give it to them immediately after preparation when it is
cool enough to eat. Foods prepared for infants and young
children should preferably not be stored at a . If this is
impossible, food could be stored only for the next meal,
but kept cool (at temperatures below 10°C) or hot (at
temperatures near or above 60°C). Stored food should be
reheated thoroughly. Again, this means that all parts of the
food must reach at least 70°C.
• Avoid contact between raw foodstuffs and
cooked foods
Cooked food can become contaminated through even the
slightest contact with raw food. This cross-contamination
can be direct, as, for example, when raw food comes into
contact with cooked food. It can also be indirect and subtle
for example, through hands, flies, utensils or unclean
surfaces. Thus, hands should be washed after handling
high-risk foods, eg. poultry. Similarly, utensils used for
raw foods should be carefully washed before they are used
again for cooked food. The addition of any new
ingredients to cooked food may again introduce
pathogenic organisms. In this case, food needs to be
thoroughly cooked again.
• Wash fruits and vegetables
Fruits and vegetables, particularly if they are given to
infants in raw form, must be washed carefully with safe
water. If possible, vegetables and fruits should be peeled.
In situations when these foods are likely to be heavily
contaminated, for example when untreated waste water is
used for irrigation or untreated nightsoil is used for soil
fertilization, fruits and vegetables which cannot be peeled
should be thoroughly cooked before they are given to
infants
i Adapted from Golden Rules for Safe Food Preparation of Health surveillance and management procedures for food-handling
personnel', report of a WHO consultation. Geneva, World Health Organization, 1989 (WHO Technical Report Series, No. 785).
• Use safe water
Safe water is just as important in preparing food for infants
and young children as it is for drinking. Water used in
preparing food should be boiled, unless the food to which
the water is added has subsequently to be cooked (eg., rice,
potatoes). Remember that ice made of unsafe water will
also be unsafe.
• Wash hands repeatedly
Wash hands thoroughly before you start preparing or
serving food and after every interruption - especially if
you have changed the baby, used the toilet, or been in
contact with animals. It should be remembered that
household animals often harbour germs that can pass from
hands to food.
• Avoid feeding infants with a bottle
Use a spoon and cup to give drinks and liquid foods to
infants and your children. It is usually difficult to get
bottles and teats completely dean. Spoons, cups dishes
and utensils used for preparing and feeding infants should
be washed right after use. This will facilitate their
thorough cleaning. If bottles and teats must be used, they
should be thoroughly washed and boiled after every use.
• Protect foods from insects, rodents and other
animals
Animals frequently carry pathogenic organisms and are
potential sources of contamination of food.
• Store non-perishable foodstuffs in a safe
place
Keep pesticides, disinfecting agents or other toxic
chemicals in labeled containers and separate from
foodstuffs. To protect against rodents and insects,
non-perishable foodstuffs should be stored in cosed
containers. Containers which have previously held toxic
chemicals should not be used for storing foodstuffs.
• Keep all food preparation premised
meticulously dean
Surfaces used for food preparation must be kept absolutely
clean in order to avoid food contamination. Scraps of food
and crumbs are potential reservoirs of germs and can
attract covered paces and be disposed of quickly.
 \/o,:.

WHO/FNU/FOS/96,!
Original English
Distr.: General

C O N S U L T A T IO N S A N D W O R K S H O P S

Fermentation:
Assessment and
research
Report of a Joint FAO/WHO Workshop on
fermentation as a household technology
to improve food safety

in collaboration with the

Department of Health, Republic of South Africa

Pretoria, South Africa, 11-15 December 1995

F O O D SA F E T Y U N IT
D IV IS IO N O F F O O D A N D N U T R IT IO N
W O R L D H E A L T H O R G A N IZ A T IO N
CO World Health Organization, 1996

This document is not a formal publication of the World Health Organization (WHO), and. all
rights are reserved by the Organization. The document may, however, be freely reviewed,
abstracted, reproduced and translated, in part or in whole, but not for sale nor for use iri
conjunction with commercial purposes.

The views expressed in documents by named authors are solely the responsibility o f those
authors.
We would like to thank Dr Robert Nout, Wagcningen Agricultural
University, The Netherlands, for his contribution, in the preparation
of Lhis report. Also, we would like to extend our thanks to
Dr MichicI van Schothorst, Secretary of the Internationa] Commission
on Microbiological Specifications for hoods, who reviewed the
HACCP studies in this report T
 TABLE OF CONTENTS

1. IN TRO D U C TIO N ................................................................................................................ I

2. B A C K G R O U N D .................................................................................................................. 2

3. DETINIT1 ON OF FERM ENTATION............................................................................... 7

4. SCOPE AND O BJECTIV ES...............................................................................................8

5. FERMENTATION: CURRENT HOUSEHOLD P R A C T IC E S .....................................9

6. FERMENTATION: ASSESSMENT OF BENEFITS AND R IS K S ............................ 11

6.1 Benefits .................................................................................................................. 11

6.1.1 B iological................................................................................................... 11
6.1.2 Chemical ................................................................................................... 12
6.1.3 Nutritional ................................................................................................. 12

6.2 R isk s.........................................................................................................................13

6.2.1 B iological................................................................................................. 13
6.2.2 Chemical ................................................................................................. 14
6.2.3 Physical ..................................................................................................... 15
6.2.4 Nutritional ................................................................................................. 15

7. PRACTICAL INTERVENTIONS FOR IMPROVING

THE SAFETY AND NUTRITIONAL QUALITY OF
FERMENTED FOODS AND TECHNOLOGY TRANSFER ..................................... 15

7.1 Weaknesses in present practices of fermentation,

and considerations for improvement ................................................................... 15
7.1.1 Food safety constraints ............................................................................15
7.1.2 Nutritional co n strain ts..............................................................................16
7.1.3 Sociocultural constraints ............................................... 17

7.2 Model approaches for improvement o f fermentation ....................................... 17

7.2.1 Technical and safety aspects ................................................................... 18
7.2.2 N u trition..................................................................................................... 23

7.3 Alternative options in household food technologies .........................................23

7.4 Technology tra n sfe r...............................................................................................24

7.4.1 Target g ro u p s ............................................................................................ 24
7.4.2 P o licies....................................................................................................... 25

(0

•am
i^1,7, " •
8 RESEARCH NEEDS 26

8.1 Food sa fe ty ............................................................................................................... 2.6

8. El Efficiency offermentation in biological s a f e ty ...................................... 26
8. E2 Effect of fermentation on biochemicai/cbemical toxicants
in raw materials ......................................................................................... 28
8.E3 Additional considerations in the promotion o fferm en tatio n ................ 28

8.2 Nutritional value .................................................................................................... 29

8.3 Technology developm ent....................................................................................... 30

8.3.1 Characterization of fermentations ........................................................... 30
8.3.2 Developriient/improvement of fermentation systems .......................... 31
8.3.3 P rob io tics.................................................................................................... 32
8.3.4 EffecLs of each processing stage on food safety..................................... 32
8.3.5 Application of quality and safety systems (including HACCP) . . . . 32

8.4 Technology transfer andrelated socioeconomic a sp e c ts .................................... 33

8.4.1 Consumer and producer perception and needs ..................................... 33
8.4.2 Transfer of information and technology to meet the needs
of the Large! groups in relation, to food safety ..................................... 34
8.4.3 Research issues relevant to the h o usehold.............................................. 35
8.4.4 Research priorities relevant to cottage in d u stry ..................................... 35

9, CONCLUSIONS AND RECOMMENDATIONS .......................................................36

GLOSSARY .....................................................................................................................................39

ANNEXES

Annex 1: List of background papers ............................................................................ 43

Annex 2: List of p articipants..........................................................................................45
Annex 3: Basic principles for the preparation of safe food for
infants and young ch ild ren .............................................................................. 48
Annex 4: Application of the HACCP system to u /i ....................................................... 49
Annex 5: Application of the HACCP system to iogwa ...............................................55
Annex 6: Application of the HACCP system to gari ...................................................62
Annex 7: Summary of’selected published data demonstrating
pathogen inhibition by lactic acid bacteria .................................................. 68

(ii)
 1

1. INTRODUCTION

Fermentation is one ofthe oldest technologies used for food preservation. Over the
centuries, it has evolved and has been refined and diversified. Today a large variety o f foods
are derived from this technology which is used in households, small-scale food industries and
large commercial enterprises. Foods so produced form a major part o f the human diet all
over the world, and in some regions, mainly in African countries, the technology is also used
to prepare foods for infants and young children.

In the past, traditional fermentation technologies were based on experiences

accumulated by consecutive generations of food producers, as a result of trial and error. Only
recently has science and technology started to contribute to a better understanding o fthe
underlying principles of fermentation processes and of the requirements for quality and
safety. However, in many instances, food fermentation practices, especially at the household
level, do not benefit yet from advances in science and technology. Since the days of
Louis Pasteur who pointed out the importance of hygiene in relation to fermentation, it is
known that this technology is readily influenced by various factors during processing, and
that if it is not applied correctly the safety and/or quality of the final product may be
jeopardized. Because ofthe ineffective foodborne disease surveillance programmes in roost
countries, in particular developing countries, many cases of foodborne diseases do not come
to the notice of public health authorities. Nevertheless, it has been possible to trace some
foodborne disease outbreaks to fermented foods and to the inappropriate application of this
technology.

On the other hand, fermentation is o f economic importance as a method o f food

preservation in areas where preservation techniques such as cold storage (refrigeration) or
hot-holding cannot be used due to lack o f facilities and resources. For such situations,
fermentation has been considered as an affordable technology for the safe preservation of
foods, in particular weaning foods. In developing countries, as a result of poor hygienic
handling and inadequate preservation, weaning foods are often contaminated and are a major
cause of diarrhoea and associated malnutrition.

With these considerations in mind, the Food and Agriculture Organization o fthe
United Nations and the World Health Organization organized a Workshop to assess
fermentation as a household technology for improving food safety. The Workshop was held
in Pretoria from 11-15 December 1995 in collaboration with the Department o f Health o f the
Republic of South Africa (RSA). The aims of the Workshop were: (i) to assess the risk and
benefits associated with current household fermentation practices, with specific emphasis on
the food safety aspects; (ii) to outline improvements which can be achieved by process
development and education of food handlers; and (iii) to identify gaps in the existing
knowledge and priorities for research.
 2

The Workshop was opened by Dr Jocelyn Webster from the Division of’Food
Technology of the Council for Scientific and Industrial Research (CSIR), Republic o f South
Africa, who welcomed the participants to Pretoria, Dr Webster emphasized the need for
collaboration between international organizations and South African research organizations,
universities and government departments to ensure information, research and technology
transfer which address key health, nutritional and food security issues in South Africa,
Dr Theo van de Venter, Director of Food and Chemicals, Department of Health, RSA then
gave a brief overview of the country’s Programme for Reconstruction and Development
which places specific emphasis on the underdeveloped and underprivileged communities.
The objective of the Workshop, therefore, met one o f the current concerns in the RSA, that is,
to meet the basic needs of the population.

Dr D.L, Tern ho, the WHO Liaison Officer ad interim in the RSA, welcomed the
participants to the Workshop on behalf of the Directors-Generai of the Food and Agriculture
Organization of the United Nations (I’’AO) and the World Health Organization (WHO).
Dr Tcmbo stated that FAO and WHO were particularly pleased to organize the Workshop in
Africa. He pointed out that the International Conference on. Nutrition (Rome, December 1992)
had expressly recommended that high priority be given to problems encountered in the African
continent, and it had recommended that action should be taken to promote sound weaning
practices by encouraging the use of nutritionally adequate, safe and appropriately processed,
locally-available foods. He added that fermentation is a common practice in the preparation of
weaning foods in. many African countries, and said that the problem o f diarrhoea! diseases in
infants and young children is also a dominant problem and one o f massive proportions.

Dr Tcmbo thanked the participants and representatives of international organizations

for having accepted the invitation of FAO and WHO to participate in the Workshop and
gratefully acknowledged the contribution of the International Foundation for Science which
supported several participants. Special recognition was also given to the Department o f
Health of the RSA and the CS1R for hosting the Workshop,

Dr Olusola Oyewole was elected Chairman of the Workshop, Dr Fernando Quevedo

as Vice-Chairman and Dr Robert Nout as Rapporteur. The deliberations o f the Workshop
were based on a number of background papers (listed in Annex 1) and the work carried out by
Working Groups, under the leadership of Drs Richard Fuchs, Alex von Holy and
Wilhelm Ilolzapfel. The full list of participants is given in Annex 2.

In closing, Dr G. Kouthon of F AO, on behal f o f WHO and FAO, thanked all

participants, the Chairman, the Chairmen o f the Working Groups and the Rapporteur for their
thorough work during the Workshop.
 3

2, BACKGROUND

Poodbornc diseases are a major health and economic problem in both industrialized
and developing countries. The incidence of foodborne diseases in the industrialized countries
has been estimated to be as high as 10% of the population. In some countries the trend is on
the increase. 'The developing countries bear the biggest burden o f foodborne diseases in the
world ('fable 1). Although reliable statistics on the incidence o f diarrhoea! diseases arc not
available due to lack of, or poor reporting systems in most countries, the high prevalence of
diarrhoea! diseases in these countries, particularly in infants and children, is evidence o f tins
tremendous problem. Annually, some 1500 million episodes o f diarrhoea occur in children
under the age of five, and over 3 million children die as a direct result. Indirectly, diarrhoeal
diseases kill many more children, as they are one o f the major underlying factors of
malnutrition. It is estimated that annually some 13 million children under the age of five die
from the associated effects of malnutrition and infections.
Table 1. Examples of pathogenic organisms of public health importance
which may be transmitted through food

Bacteria Protozoa

Bacillus cereus Cryptosporidium spp.

Brucella spp. Entamoeba histolytica
Campylobacter jejuni Giardia lambda
Clostridium boiulinum Toxoplasma gondii
Clostridium perfringens
Escherichia cpli spp, Trematodes
(pathogenic strains)
Listeria monocytogenes Clonorch is s mensis
Mycobacterium bo vis Fasciola hepatica
Salmonella typhi and paratyphi Fasciolopsis buski
Salmonella (non-typhi) spp. Opisthorch is fel incus
Shigella spp, Opisthorchis viverrini
Staphylo cocc us aure us Paragonimus westermani
Vibrio cholerae
Vibrio parahaemolyticus Cestodes
Vibrio vulnificus
Yers inia entero colit ica Diphyllobothrium latum
Echinococcus spp.
Taenia solium/ T. saginata
Viruses
Nematodes
Hepatitis A virus
Hepatitis E virus Anisakis spp
Norwalk agents A.scar is lumbri coides
Poliovirus Trichinella spiralis
Rotavirus Trichuris trichiura
 4

Pathogens identified as the cause of diarrhoea! diseases include bacteria such as

Escherichia coli, Shigella spp., Salmonella spp., Vibrio cholerae O! and Campylobacter
jejuni.; protozoa such as Giardia lamblia. Entamoeba histolytica, Cryptosporidium, spp.; and
enteric viruses, such as rotavirus. Infections due to pathogenic strains of/T coll are probably
the most common cause of diarrhoea, in developing countries. They constitute up to 25% of
diarrhoea! diseases in infants and children and have been associated, among others, with
weaning foods. The distribution of other pathogens, as observed among cases o f diarrhoeal
diseases seen at treatment centres in developing countries, is shown in Table 2.

Contaminatcd food is a major cause

'Fable 2, Some of the major pathogens
of diarrhoeal diseases; it is estimated that up
frequently identified in children
to 70% of all cases are of foodborne origin.
with acute diarrhoea seen at
The sources of contamination are numerous treatment centres in developing
and include nightsoil, polluted water, dies,
countries
pests, domestic animals, dirty utensils and
pots, food handlers (e.g. soiled hands), dust RajJifwwn Percentage
and dirt. Raw foods themselves are
frequently the source of contamination, as Rotavirus 15-25
some may naturally harbour pathogens, or Escherichia coli.
come from infected animals. Moreover, j - enterotoxigenic 10-20
during food preparation and storage there is i - cntcropathogenic 1-5
an added risk of cross-contamination. Shigella spp 5-15
However, one of the major factors leading to Campylobacter j ejuni 10-15
ftjod coiitarnination is time-ternp erature Vibrio cholerae 01 5-10
abuse during preparation, with the resultant Salmonella (non typin') spp 1-5
survival and/or growth of pathogens or . Cryptosporidium spp 5-15
production of toxin (Figure I ).

Applying basic rules for safe food preparation (Annex 3) will help to prevent, the
contamination, growth and survival of pathogens in foods and will reduce the incidence of
diarrhoeal diseases. However, application of these rules can be sometimes hampered by
socioeconomic constraints, such as an inadequate supply of sale water, Jack of facilities for
safe preparation and storage of food (e.g. refrigerators, fuel for hot-holding or thorough
reheating), and lack of time to prepare food properly prior to each meal. As a result, poor
householders are simply not able to apply certain essential food safety principles, such as
feeding infants with freshly prepared food, refrigeration (below 1()"C), hot storage (above
60°C), or reheating of stored food (Annex 3).

In some countries, fermentation (lactic acid fermentation in particular) is traditionally

used as a household technology for preservation of foods. For example, in some African
countries it is customary to give infants fermented cereal or root crop products such as ogi
( Nigeria) or uji (United Republic of Tanzania, Uganda, Kenya). In addition to nutritional
benefits, such fermented foods offer a good keeping quality as a result o f acidity produced by
lactic acid bacteria (pH <4.5). Therefore, lactic acid fermentation has been considered as an
alternative to what are presently regarded as conventional methods o f food preservation (he.
cold storage, dehydration or canning). It is also a belief that, fermented products can
 5

Food handier (e,g

contammaited bauds)

rt
o

£
ou
Sources of

ITIME-TEMPEEATUME
' ABUSE

T
CONTAM INATED FOOD

Figure 1. Sources of food contamination

 6

he consumed without, further reheating, and using this technology therefore overcomes fuel
problems. In addition, some nutritional benefits have been attributed to fermented foods.
However, four important questions arise when considering the safety implications o f the
application of fermentation at household level. Firstly, what kind of hazards can be
controlled by the application of such a technology? Secondly, what kind of risks are
associated with the actual application of the technology due to food handlers' lack o f
knowledge, or poor hygienic conditions during food preparation? Experience has shown that
when this technology has been applied improperly, fermented products were the source of
food borne illness. Thirdly, what kind of considerations of a sociocultural nature should be
taken into account in order to successfully apply or transfer fermentation technology to
another region? And finally, considering the risks and benefits, should such a technology be
promoted at all?

Figure 2. Interrelation of care, foodbornc infections and nutrient intake on the health and
nutritional status of infants and children
(source: Svanberg, U. and Lorri, W. Fermentation and Nutrient Availability. Back}.'run rid paper
presented at the. Workshop)
 7

3. DEFINITION OF FERMENTATION

Fermentation is defined as a desirable process o f biochemical modification of primary

food products brought about by microorganisms and their enzymes. Fermentation is
purposely carried out to enhance properties such as taste, aroma, shelf-life, texture and
nutritional value. Fermentation is often part o f a sequence o f food processing operations,
including cleaning, grinding, soaking, salting, cooking, packaging and distribution.
Therefore, the potential of fermentation to enhance food safety or nutritional value should be
assessed in the light of the total manufacturing sequence.

From a microbiological point of view, it is tempting to distinguish food fermentations

according to the organisms responsible for the desired modification, Le. filamentous fungi,
yeasts and bacteria.

However, for the purpose of this commodity-oriented Workshop it appeared more

appropriate to distinguish several characteristic groups of fermented products, as follows1

• Textured vegetable protein meat substitutes made from legumes and/or cereals using
mixed starter cultures of filamentous fungi, bacteria and yeasts; the fungal mycelium
keeps the food particles together in a sliccablc cake, whereas various enzymatic
degradations contribute to enhanced flavour and digestibility.

• food-flavouring sauces and pastes (protein hydrolysates) with high salt content made
from proteinaceous seeds, fish or fishery by-products, using combinations of
filamentous fungi, yeasts, bacteria, as well as fish intestinal proteolytic enzymes; the
resulting peptides and amino acids have a flavour enhancing effect.

• Lactic acid fermented preserved foods, characterized by a significant acidity caused

by the production of lactic acid by lactic acid bacteria. Foods of plant origin
(vegetables, cereals, roots, legumes) as well as animal-derived foods (milk, meat, fish)
are transformed into relatively shelf-stable, refreshing and nutritious, sour-tasting
products worldwide.

• Alcoholic beverages, including beers, wines and spirits made from starchy or sugary
substrates using yeasts and occasionally bacteria for alcohol formation. In several
alcoholic beverages a sour taste is produced by simultaneous activity of lactic acid
bacteria,

• Vinegars characterized by a significant acetic acid content, made from various

alcoholic products using acetic acid bacteria. Vinegar is not a food of major
importance to the diet, but plays an important role as a highly effective food
preservative and flavouring agent o f biological origin.

1 Steinkraus, K.H, Classification of Fermented Foods. Background paper presented at tine Workshop
(see Annex I).
 8

• Alkaline food condiments made from proteinaceous seeds. As a result of bacteria)

proteolytic action on the seed protein, nitrogenous degradation products are released
resulting in a strong ammoniacal flavour and an alkaline reaction.

* Breads made from cereal meal or flour, leavened by the action of yeasts or yeast-lactic
acid bacteria mixed populations. The fermentation o f bread dough contributes to the
texture, taste and shelf-life of baked bread.

4. SCOPE AND OBJECTIVES

It is essentia! that public health and food authorities concerned with nutrition, food
safety and prevention of diarrhoea consider the advantages and disadvantages with regard to
the application and promotion of fermentation at household level. These considerations
should also be included in programmes for the education o f consumers, food handlers and
manufacturers.

After reviewing some traditional fermented foods (particularly those consumed in

Africa, Asia and Latin America), the effects o f fermentation on different foodborne hazards
and nutritional quality, and the potential use of starter cultures on a household scale, the
Workshop decided to locus the scope o f its discussions on :

food safety problems as related to feeding o f infants and children under the age of
live, as the occurrence of under-live diarrhoea poses a serious public health
problem;

fermented foods worldwide, with particular reference to African fermented

weaning foods;

food commodities such as cereals, dried legumes, root and tuber crops, fruits and
vegetables, and milk;

lactic acid fermentation; and

production at household level, which will also be o f relevance to cottage

industries.

The following three objectives were adopted:

a) to review the current "state of the art" with respect to the benefits and the risks
of fermentation;

b) to develop practical interventions for improving the safely and nutritional

quality of fermented foods; and

c) to identify gaps in knowledge and establish where additional research is

needed.
 9

5. FERMENTATION: CURRENT HOUSEHOLD PRACTICES

Fermentation is a common traditional household technology in many parts o f the

world. Regional differences occur in manufacturing practices, consumption habits, quality,
and level of acceptability of fermented foods for weaning purposes. These will depend on
such factors as the availability of raw materials, the laborious processes involved, and
changing patterns in society. Fermented foods intended lor infants and young children consist
mainly of lactic acid fermented cereals (e.g. maize, sorghum, millet), root crops (c.g.
cassava), milk, and to a lesser extent fish, meat and vegetables.

Lactic acid fermentation at the household level is a natural process brought about by
the lactic acid bacteria present in the raw food, or those derived from a starter culture. The
following representative examples of fermentation practices serve to illustrate the variety of
techniques employed in Africa.

Cereal grains are dry, and can be fermented only after the addition of water. Thus in
most cases, after manual cleaning, grains are soaked in water. During soaking for a period of
a few days, a succession of naturally occurring microorganisms will result in a population
dominated by lactic acid bacteria. It is also possible to first grind the grains to a meal and
then moisten to obtain a dough. If the dough, is kept for a few days, a similar succession will
take place.

fermentation may be "fuelled" by the endogenous grain amylases which generate

maltose (fermentable sugar) from starch, a type of fermentation which is very common; it
can be accelerated by adding a simple starter culture containing a large number o f active
lactic acid bacteria. This can be some of the previous batch of fermented dough (a practice
referred to as "back-slopping"), or a carrier material to which lactic acid bacteria attach (such
as the porous wall of a gourd or vessel, or the "inoculation belt" used in Ghana), The
resulting fermented dough can be cooked with water to make a beverage, such as Kenyan uji,
or a product such as Ghanaian kenkey.

Sometimes a mixture of cereal meal and water is cooked first and fermented
afterwards. The endogenous amylases have then been inactivated, and less fermentable sugar
will be available for lactic acid bacteria. Household experience has LaughL that the addition of
an enzyme rich material is required Lo bring about the fermentation. For this purpose the use
of germinated grain (such as malted sorghum) is common, although some people use plant
juices or saliva. The germinated grain will act as a source of maltose-generating enzymes,
and also as a starter culture, although of a less homogeneous type than the back-slopping
starter culture mentioned above. In the fermentation which follows, lactic acid bacteria
should quickly colonize the substrate by rapid acidification. Often, some yeasts will also
develop. The latter are not dangerous, but in weaning foods their activity must remain
limited because of undesirable gassiness and alcohol production. This type of fermented
beverage is exemplified by Tanzanian togwa.
 10

Cassava is a staple food for about 500 million people in developing countries, and
bitter varieties are potentially toxic because of their cyanide content. However, fermented
cassava products are generally introduced to children after one year of age, and soon form a
major part of their daily diet. The addition of water is not usually necessary when processing
cassava because of its high moisture content. However, the peeled roots, either whole or cut
Into pieces, are often fermented submerged in water. This soaking process is also called
"retting'1and is common in Africa and Latin America in the household production o f sour
cassava starch products such as lafun and far inha da mandioaa. Under water, the facultative
anaerobic lactic acid bacteria will dominate within a day and acidify the product. After
several days of retting, the pieces of tuber are removed from the water and sun-dried. After
grinding, the Hour is used for porridge preparation. Usually a starter culture is used by way
of adding some water from a previous batch, or from, the wall of the vessel. Another way of
cassava fermentation is by grating the peeled and washed roots into pulp, and pressing the
pulp in jute or polypropylene bags. The pressure ensures drainage o f excess fluid, and in a
few days a thorough acidification is the result of lactic acid fermentation. The starter culture
is usually present on the grater and in the previously-used bags. The fermented pulp is
crumbled and roasted in a hot cast-iron pan to a pregelatinized and shell-stable product called
gari. It can also be steamed after sun-drying for about one day to a more perishable product
called aliiake. A third option for cassava fermentation is to stack the peeled and washed
whole or cut roots under a plastic sheet to avoid dehydration. After a few days "sweating",
moulds will grow. Research has shown that the desirable moulds are Mucor, Rhizopus and
Neurospora spp., and that during the "solid substrate fermentation" moulds overgrow the
bacterial species, causing flavour production and root softening. After the “sweating" stage,
the plastic sheet is removed and the roots are gradually dried in the sun. The dried material is
ground to a meal, which is used for porridge preparation, dins practice is common in
Mozambique and Uganda.

Lactic acid fermentation of milk usually takes place with raw (unpasteurized) milk, by
keeping it in a gourd which is always used for that purpose. The lactic acid bacteria present
in the cavities of the gourd's wall act as a starter culture. Fermentation is usually rapid, and
adequate acidification should be obtained within a few hours. The fermented product usually
has a semi-liquid consistency due to the coagulation o f casein. Often, bigger coagulated
casein lumps are strained off prior to consumption or sale, as these can be used as starter
cultures for succeeding batches.

The common, denominator of" lactic acid fermentations of fish, meat and vegetables is
that in most cases, salt (kitchen salt, or rock salt) is added in varying quantities (1-25% w/w).
Many lactic acid bacteria have a better tolerance to salt than most pathogenic bacteria. Salt is
also effective in protecting the product against some spoilage bacteria, and in the ease of
vegetable fermentation, it makes fermentable plant sugars available by osmotic extraction of
juices. Lactic acid fermented foods with a high salt eontent are not normally given to
children.
6* FERMENTATION: ASSESSMENT OF BENEFITS AND RISKS

Food can act as a vehicle for illness in a number of ways. Figure 1 illustrates the
various potential sources of contamination. Contamination o f food with enteropathogenic
microorganisms may result in foodborne infections, whereas growth o f toxigenic micro­
organisms may give rise to toxin accumulation in the food and, consequently, foodborne
intoxications. The single most effective way o f controlling most of these microbial hazards is
to cook foods thoroughly. The effect of lactic acid fermentation on some food hazards has
been studied, and its potential for improving safety noted. Microbial fermentation is often
just one step in a food preparation process. Usually, other operations, such as size reduction
(grating, cutting, grinding), salting and heating, are also involved. Where the reduction o f a
hazard has been observed, this may be the result of other unit operations or their combination
with fermentation rather than the fermentation step alone.

6.1 Benefits

6-1..1 Biological

There is considerable evidence showing that lactic acid fermentation inhibits growth
and survival of and toxin production by a number of pathogenic bacteria. In the latter case,
rapid growth of lactic acid bacteria and decrease in pH inhibits growth of the toxin-producing
organisms, or inhibits toxin production by competition. A summary of recent published data
for the principal foodborne bacterial pathogens is presented in Annex 7.

A number of antimicrobial factors associated with lactic acid fermentation have been
identified, but the most important is the production of lactic acid itself The extent to which
bacteria are inhibited will depend on the organism concerned, the temperature, the amount of
acid produced and the properties of the food, i.e. its buffering capacity. In cereal and
vegetable products which are weakly buffered, an efficient lactic acid fermentation will
produce a pH of 4.0 or less, at which the growth o f bacterial pathogens is inhibited, and many
bacteria will die at a rate which increases with increased ambient temperature.

The potential of lactic acid fermentation for controlling food contamination will
depend, on factors that are difficult to quantify, such as initial level of contamination, which in
turn will depend on local conditions, levels o f hygiene and sanitation, and the degree of
acidification achieved. Therefore, it should be noted that fermentation cannot replace the
need for observing rules of hygiene. There is, though, recent evidence to suggest that
prevalence of diarrhoea in young children is reduced by consuming lactic acid fermented
cereal gruels.2

7 Svanberg, U. and Lorri, W. Fermentation and nutrient availability. Background paper presented during
the Workshop (Annex 1).
 12

6.1.2 Chemical

Lactic acid fermentation has been associated with the reduction o f certain naturally-
occurring toxins in plant foods. For example, levels o f cyanide from cassava, which has been
implicated in a number of health problems, are reduced in several traditional fermented
products. Although cassava can be fermented in different ways, experimental evidence
shows that in at least one of these, acid fermented grated roots (e.g. gari)^ cyanide removal is
a consequence of the activity o f naturally-occurring plant enzymes rather than microbial
activity. In other cassava products, microorganisms play an essential role in softening the
plant tissues thus facilitating the reduction in cyanogen content. Microbial fermentation also
contributes to the keeping quality and desirable sensory properties.

6 .1.3 Nutritional

Change in nutrient composition. Carbohydrates, particularly starch and soluble

sugars, are the principal energy source o f fermenting microorganisms. T’he level o f these
compounds as well as non-digestible oligosaccharides decrease during the microbial
fermentation. Certain amino acids may be synthesized during fermentation. Lactic acid
fermentation of cereals and cereal-legume blends improve the availability o f certain B-group
vitamins, although variation has been observed. The major organic acids produced arc lactic
a d d and acetic acid; these and other metabolites contribute to the rich variety o f taste and
aroma of the fermented products.

* Carbohydrate digestibility. There is an enhanced nutritional quality through better

digestibility by reduction of certain oligosaccharides particularly prevalent in
legumes. This reduces side effects, such as abdominal distention and flatulence,
which customarily occur among people eating a diet which is high in
oligosaccharides, such as raffinose, stachyose and verbascose.

* Nutrient density - dietary bulk. Fermentation techniques which involve a combination

of amylase rich flour (ARF or power flour) and a small amount of a lactic starter
culture provide a considerable opportunity for increase o f the nutrient density. The
decrease in viscosity enables the addition of more dry matter while maintaining a
semi-liquid consistency. The ARF must be added after cooking the gruel; the Hour
concentration can be increased by more than 100% while still maintaining a semi­
liquid consistency regarded as preferable for feeding young children. This thinning
effect is partly due to the low pH o f the fermented gruels but is mainly due to the
effect of the amylase activity o f the germinated cereals.

Effect on anti-nutritional factors. Some cereal-based diets have restricted

bioavailability of nutrients as a result of the presence o f anti-nutritional factors such as
phytates and polyphenols (tannins).*

* Phytate (or inositol hexaphosphale) is an abundant plant constituent and accounts for
60-90% of the total phosphorus content o f the product. This is necessary for the
energy metabolism of the plant itself. Phytate content in fruits and vegetables is
 13

generally lower than in cereals and is decreased by enzymes (phytases) and high-
temperature processing. Phytate is normally found in the form of complexes with
polyvalent cations, e.g. iron, zinc, calcium and magnesium, and proteins. The
inhibition of non-haem iron absorption by phytates is dose dependent and even low
levels (less than 90% of whole wheat flour phytate content) are inhibitory, Phytases
are present in most cereals and active at a pH of around 5,0, The ideal fermentation
process provides optimum pH conditions for degradation o f phytate. This is obtained
by initial soaking of the flour in water for about 12-24 hours. Such a reduction in
phytate increases the amount of soluble iron several-fold. There arc similar benefits
for zinc and calcium. Thus, lactic acid fermentation o f maize or sorghum changes a
diet of "low iron bioavailability" into a diet o f "intermediate to high iron
bioavailability".

* Tannins (or polyphenols) are plant components which contribute to protection against
plant disease and predators. They also inhibit dietary mineral absorption and protein
digestibility. The galloyl groups of polyphenols are mainly responsible for the
inhibiting effect on iron absorption. The tannin content of cereals is reduced by lactic
acid fermentation. In some high-tannin cereals, however, there seems to be little or no
improvement in iron availability after lactic acid fermentation. This is presumably
due to production of metabolites o f tannins which are inhibitory to iron absorption.
Microbial fermentation improves protein digestibility of high-tannin cereal varieties.
The greatest increase in digestibility is observed in high-tannin sorghum gruels
fermented with a natural starter culture. Tannins have also an inhibiting effect on the
growth of lactic acid bacteria, thereby slowing the process of microbial fermentation.

Presence o f promoters. Vegetables generally contain low but sufficient amounts of

phytate to have an inhibitory effect on iron absorption. During lactic acid fermentation,
e.g. in "sauerkraut", phytate may be completely degraded. The amount o f iron absorbed is
increased when fermented vegetables arc added to a phytate-rich diet. This indicates the
presence of iron-promoting factors in lactic acid fermented vegetables. Vitamin C is such an
iron-promoter; it is well-known that it is preserved in lactic acid fermented vegetables
because of the prevailing reducing conditions.

6.2 Risks

The aspects listed below are generally supported by published experimental evidence.
However, in some cases the evidence is fragmentary and rather reflects a lack o f clearly
established scientific evidence.

6.2.1 Biological

A certain number of agents appear not to be affected by lactic acid fermentation.

However, they may be adequately destroyed by other processing operations involved in the
preparation of the food, such as cooking.
 14

• There arc emerging patterns o f acid resistance in some enteropatbogens such as

E. call. 0 1 57:ii7, where for example, fermented meats and yoghourt have been
vehicles of infection and this should be monitored closely.

• Foodborne viruses arc recognized as a significant cause of gastroenteritis, and

rotavirus has been identified as one o f the most common causes of diarrhoea in
childhood. Enteric viruses are necessarily relatively acid stable to survive passage
through the stomach's acidity, and unlike bacteria do not have greater sensitivity to
weak organic acids, such as lactic acid. Simian rotavirus has been shown to survive at
high levels of acidity during 24 hours storage in a model fermented weaning food.
They did, however, show increased heal sensitivity at low pH,

• The diseases produced by parasites such as Cryptosporidium, Giardia lambliu, and

trematodes transmitted by foods arc varied and widely distributed in all parts o f the
world. There is little information on the effects of fermentation on these parasites.
The cysts of these organisms often show resistance to adverse conditions although
they arc generally killed by adequate cooking. For example, there are indications that
cysts of many foodborne trematodes may survive 70°C and further studies are
required to deline the precise thne/temperature combinations to assure safety from
these organisms, and to assess whether the fermentation step will have an effect, on
their infectivity.

6.2.2 Chemical

Certain algae, bacteria and moulds can produce toxins that may be transmitted by
foods. Many of these are beat resistant and will survive normal cooking temperatures.
Generally, lactic acid fermentation will not eliminate the risk posed by these preformed
toxins.*

* Mycotoxins arc toxic secondary metabolites that are produced during the growth of
certain moulds on foods. They may be present in the food material as a result of
mould contamination in the held or during storage in uncontrolled, hot and humid
conditions. The risk of contamination by mycotoxins of raw materials used in
fermented foods is a serious food safety hazard. Some studies have reported no
reduction in the level of mycotoxins by fermentation while others have reported
appreciable decreases (Annex 7). Other processing steps, such as cleaning, milling,
dehulling and cooking will contribute to the reduction in my cotoxin levels. However,
the precise role of microbial fermentation in reducing the concentration ol mycotoxins
in foods is not well established. From these data, it is clear that fermentation cannot
be relied upon as a means of detoxifying mycotoxin-contaminatcd foods.
 15

• Bacteria can cause foodborne illness cither as a result of ingestion of preformed

bacterial toxins with a food (intoxication) or the ingestion of live organisms
(infection). There is no evidence to suggest that microbial fermentation alone will
eliminate risk by removing preformed bacterial toxins from food. A final cooking
stage will eliminate heat labile toxins, such as those produced by Clostridium
botulinum, but cannot be relied upon to destroy the heat stable toxins produced by
other bacteria such as Staphylococcus aureus and Bacillus cereus,

6.2.3 Physical

There is no evidence to suggest that lactic acid fermentation reduces the level of
contamination with extraneous matter. On the other hand, in certain cases fermentation
follows a steeping step which might contribute to the removal o f dirt.

6.2.4 Nutritional

Microbial fermentation has a minimal effect compared with cooking in reducing the
anti-nutritional effects of protease inhibitors, and the toxic effects of lectins on the intestinal
epithelium.

Microbially-produced lactic acid is usually a mixture of the optical isomers L-(+) and
D“( - ) lactic acid. D -(-) lactic acid cannot be metabolized by humans. Excessive intake of
D“(--) lactic acid may resulL in acidosis, a disturbance o f the acid-alkali balance in the blood.
Little is known about, the "toxicity" of D -(-) lactic acid for malnourished or sick children. In
addition, relatively little data is available about the D -(-) lactic acid content of fermented
foods prepared at the household level.

7. PRACTICAL INTERVENTIONS FOR IMPROVING THE

SAFETY AND NUTRITIONAL QUALITY OF FERMENTED
FOODS AND TECHNOLOGY TRANSFER

7.1 Weaknesses in present practices of fermentation, and considerations for

improvement

The constraints and shortcomings related to traditional fermented weaning foods can
be threefold: technical and safety, nutritional, and social. The complexity o f the problems
necessitates a multidisciplinary approach to improve fermentation practices.

7.1.1 Food safety constraints

The time necessary for food processing in the traditional household fermentation
process is a constraint on the hours available to women who, as mothers and food processors,
are also engaged in child care and other household activities. Lack of time may have
 16

.significant implications regarding safety and nutritional quality o f fermented foods because
any time saved by cutting down on fermentation periods may jeopardize the effectiveness of
acidification by lactic acid bacteria, or the degradation o f plant toxins and anti-nutritional
factors by the relevant enzymes.

Reduction of time expenditure may be achieved by accelerating the process, or by a

different distribution oflabour. In the latter case, foods might be produced by entrepreneurs,
Care should be taken that no unjustified shortcuts are employed in the process which might
jeopardize the safety and nutritional value o f the product.

Other food safety problems arise from shortcomings in handling/processing o f foods,

resulting in different types of hazards (e.g. phytotoxins or anti-nutritional factors in the raw
materials, survival and/or growth of pathogenic organisms, contamination from the
environment). Improvement of product quality and safety could be achieved by Good
Manufacturing Practice (GMP) and Good Hygienic Practice (GIIP), and by using the Hazard
Analysis Critical Control Point (HACCP) system. The latter is aimed at identification,
assessment and control of hazards throughout the process from raw material to packaging
and consumption.

7.1.2 Nutritional constraints

The limitations related to many currently-used weaning foods include:

a) low content and limited quality o f protein in raw materials, mainly

cereals and root crops;
b) low nutrient density o f the prepared foods; and,
c) poor or low bioavailability o f proteins and minerals in the finished
product.

The following measures for improvements may be considered:

Macronutrients'. The viscosity of starchy and bulky products could be reduced in order to
enable an increased nutrient density while maintaining an acceptable viscosity. In addition,
the protein quantity and quality could be improved by protein supplementation, e.g. by
adding legumes,

Micronulrients: Micronutrient forti fication could improve the nutritional quality o f the
product, provided that their bioavailability is ensured. At the household level, however,
fortification seems of lesser relevance as it might not be affordable or practicable. At all
levels of production, the bioavailability o f macro- and micronutrients could be improved by
strategic use of germination and fermentation techniques.
 17

7.1.3 Sociocultural constraints

The major social constraint related to fermented foods for weaning is one o f poor
image when compared to industrial preparations which are considered superior and associated
with progressive ness in some countries. Fermented foods arc often poorly perceived and
poorly accepted by mothers whose responsibility it is to prepare and feed them to the
children. Another constraint here is that o f a socioeconomic nature where sophisticated
processing equipment is not affordable at the household level. In other words, the
sophistication level of the fermentation method must fit the socioeconomic framework.

The Workshop identified several areas requiring attention:

* The public image of some traditional fermented foods is poor, and should be
improved.

* An important aspect is to educate the mother or child carer, as well as the food
manufacturer, about the optimum conditions for the preparation of specific
fermented foods.

* The involvement of food manufacturers in terms of training and experimenting

with new or upgraded techniques is important. Participatory research has
benefits for the manufacturer as well as the researcher,

* The present exchange of information between mothers, manufacturers,

scientists, government and non-governmental organizations needs to be
improved.

7*2 Mode! approaches for improvement of fermentation

Interventions for improving the safety and nutritional adequacy of traditional

fermented food should take into account:

traditional, technical and socioeconomic aspects; and

the needs and realistic prospects to achieve this aim.

In assessing the safety and nutritional value of weaning foods produced by a

fermentation process, either at household or cottage level, the Workshop considered that the
assessment of socioeconomic and cultural aspects is essential to enable the optimum
utilization of this technology for the preparation o f these weaning foods. The
socioeconomical and cultural considerations should be integrated with key concepts o f food
safety, nutrition, household food security, and prevention and control o f infection, if an
improvement is to be achieved in the nutritional status o f infants and young children.
 18

Therefore, where fermented foods already form part o f the diet o f infants and young
children, it is important to examine the existing socioeconomic and cultural relations and
patterns, and identify the type of support which is needed to improve the safety and
nutritional value of the fermented foods.

7.2.1 Technical and safety aspects

Reduction, in the processing time can be attempted using fermentation starter cultures.
In principle, starter cultures contains a. high concentration, of live microorganisms which arc
added to raw materials with the aim o f achieving the desired fermentation as rapidly as
possible. At the household level several starter cultures are practicable. These include using
batches of previously fermented products (also referred to as back-slopping), or specially
prepared dry starter cultures such as the Ghanaian inoculation belt or the Indonesian ragi and
mar .

The Hazard Analysis Critical Control Point (HACCP) system could be used in order
to identify and evaluate hazards and control measures.-’’34 The application o f the HACCP
concept to a few selected but representative processes of African fermented foods, c.g. gari
(Nigeria), togwa (Tanzania) and uji (Kenya) is illustrated in Annexes 4-6.5 'I’he schematic
presentation of the production processes for these products are shown in Figures 3-5.

Some important safety considerations which derive from the application o f HACCP to
cassava and cereal for production of gari> togwa and uji are:

• Rapid and adequate acidification (a combination o f low pH and sufficient titratablc

acidity to result In an inhibitory level o f undissociatcd weak organic acid (mainly
lactic and some acid acetic).

* Sufficient cooking for rendering food safe, particularly in terms o f parasites and.
viruses. If starchy meals are cooked for palatable purposes, the importance of
adequate thermal processing for elimination or reduction o f hazards should
nevertheless not be overlooked.

3 WHO. Hazard Analysis Critical Control Point system: Concept and Application, Report of a WHO
Consultation with the participation of FAO, Geneva 29-31 May 1995 (Unpublished WHO document
WHO/FNU/FOS/95.7).

4 Bryan, I\ Hazard Analysis Critical Control Point Evaluations, A guide to identifying hazards and
assessing risks associated with food preparation and storage. World Health Organization, Geneva, 1992.

5A prerequisite for the application of the HACCP system in food processing/preparation is that the
principles of Good Hygienic Practice (GHP) or Good Manufacturing Practice (OMP) are adhered to. In principle,
Critical Control Points (CCPs) should be restricted to steps in a food operation which, if not controlled properly,
may lead to significant food safety problems. In a newly-developed I (ACCP plan, more CCPs may be included than
are perhaps necessary. Based on a review of the monitoring and verilication results, CCPs may be deleted lrorn the
11A.CCP plan, if they turn out to be sufficiently covered by GHP/GMP. The HACCP studies presented in Annexes
4-6 are models for the application of the HACCP system to fermented foods, based on a worst case scenario, thus
many steps have been identified as CCPs. Depending on the situation, some of these steps may not need to be
considered as CCPs. It should also be noted that model HACCP plans arc not appropriate for use until validated
for a specific food and food process.
 19

* Sufficient size reduction in cassava to enable enzymatic degradation o f toxic

cyanogenic glycosides.

* Avoidance of mouldy raw materials in view of possible mycotoxin contamination.

* Using safe water.

Togwa preparation is associated with a higher food safety risk than fermented uju as the first
involves the addition of power flour (or ARP) and togwa after the food has been cooked (see
Annexes 4 and 5)* There is thus a risk o f post-cooking contamination, particularly with
acid-resistant pathogens. For example by the addition of power flour and if the lactic acid
fermentation fails, the proliferation of bacterial pathogens may occur. Possible options to
minimize the saf ety risks of togwa preparation include quick (accelerated) fermentation by
back-slopping or use of other starter cultures; using ARF o f high (hygienic) quality; and
avoiding post-cooking contamination.
 20

Maize
(Sorghum, millet)

Figure 3. Application o f the HACCP system to preparation o f u ji in households.

The numbers refer to the steps described in Annex 4.
 21

Figure 4* Application of the HACCP system to preparation o f t o g w a in households.

The numbers refer to the steps described in Annex 5.
 22

1
Cassava

\ _____________________ 4

Peeling |

Water
1

Washing CCP

G rating

CCF

Fermentation
(in bags under weight)
CCP

F igure 5* Application of the HACCP system to preparation o f g a r i in households.

The numbers refer to the steps described in Annex 6,
 23

7.2.2 Nutrition

At the household level, it is technically feasible to increase the nutrient density of

foods while maintaining a semi-liquid consistency. It is possible to prepare porridges
containing 20-25% (w/w) dry matter (about 1 kcal or 4 kJ per gram o f porridge) which can
still be swallowed easily by a small child, using 1-5% (w/w) ARF after having cooked the
starchy cereal or root crop based food.

Likewise, it is technically feasible to enrich the protein content o f such porridges

using legumes such as soya beans or cowpeas. As a rule of thumb, a 70:30 weight ratio of
starchy staple versus protein-rich legume will be adequate.

7.3 Alternative options in household food technologies

As a single unit operation, lactic acid fermentation provides acidity and flavour and
contributes to the nutritional value. The acidity provides a significant microbiological
stability enabling storage at ambient temperature for a day without risking associated
microbiological hazards. If combined with an appropriate heat treatment, a fermentation-
based process will also minimize hazards (e.g. viruses, parasites or some anti-nutritional
factors) which cannot be reduced by the fermentation process alone.

Alternative options to fermentation-based food processing in households in

developing countries include:

1) Consumption of fresh food raw materials without fermentation or cooking. This is the
cheapest way. The risk of foodbornc infections may be high, particularly for foods of
animal origin or made with crops grown in contaminated environments. In some
foodstuffs, natural toxins may pose a severe threat to human health. The
characteristic fermentation flavour will be absent.

2) Cooking of fresh (non-fermented) food. More energy is required to cook fresh rather
than fermented food to achieve the required palatability/digestibility. Some of the
natural toxins and anti-nutritional factors cannot be adequately removed by cooking
alone. The biological safety of cooked fresh food is adequate, provided that it is
consumed immediately after cooking, and post-contamination is avoided. Left-overs
need to be refrigerated (<10°C) or kept hot (>60°C) as the neutral pH allows
proliferation of surviving or post-cooking contaminating microorganisms. Re-heating
prior to consumption is highly recommended. The characteristic fermentation flavour
will be absent.

3) The use of non-fermented (ready-to-consumc) food, preserved by canning. Generally,

the safety of canned food is high, if the product is consumed immediately after
opening the can and, in principle, no thermal energy is required at the household level.
Left-overs require refrigeration and re-heating, as in option 2 above.
 24

4) Dehydration (e.g. using solar energy) o f non-fermentcd fresh produce, followed by

reconstitution and cooking. This option provides a relatively cheap way to preserve
perishable raw food materials such as roots and vegetables. Adequate solar
dehydration requires appropriate climatic conditions and hygienic practices to avoid
contamination via soil, insects, rodents, other animals and humans. The resulting
dehydrated food would require processing as in option 2 to render it palatable and
sale.

However, if fermentation is culturally acceptable and desirable, it provides a valuable and

relatively cheap option, even when combined with a cooking step, as cooking a fermented
product requires less energy-

7.4 Technology Transfer

7.4.1 Target groups

Where fermentation is not commonly practised and its introduction is being

considered (or being revi ved), the study o f the socioeconomic and cultural factors is
important in order to assess the feasibility of application o f the technology. In this case, the
need to educate those who will apply the technology should be particularly emphasized with
respect to the factors determining the safety and nutritional adequacy o f the food.

Social and cultural patterns vary tremendously from one place to another and are
subject to change over time. The impact of these patterns on food safety and nutrition as well
as solutions to the problems encountered arc therefore location and time-specific. Perhaps the
only common thread is that, in all cultures and at all times, women have played and will
continue to play a prominent role in infant and young child care. Women are the key players,
cither as mothers preparing food, or as decision-makers in selecting infant food. The children
play a role as consumers, but not as decision makers. Therefore, gender relations have to be
addressed in attempts to improve food safety and nutrition.

Issues to be considered when recommending the use o f fermented foods arc:

• Know-how, education and practices o f food handlers / households in the

preparation of fermented foods;

• f acilities for hygienic preparation o f fermented foods (e.g. starter cultures,

materials, fuel);

• Environmental conditions, such as the quanti ty and quality o f water and the
sanitary conditions;•

• Environmental pollution, detrimental ecological conditions and biological

changes in the environment, e.g, the emergence o f resistance o f pathogens;
 25

• Agronomic, food storage, food processing, and food marketing practices;

• Consumers’ purchasing power, and their access to markets;

• Family and social structures;

• Caring capacity for the infant, e.g, time available to mothers;

• Food choice and acceptability of fermented foods; and

• The level of education in general, and as related to food safety and nutrition in
particular.

7.4.2 Policies

The introduction of food and nutrition know-how should be seen in the light o f a
country’s overall development. Important issues at stake arc access to shelter, safe drinking-
water, wholesome food and education. Appropriate policies should be developed, supported and
implemented by relevant government agencies. Specific technologies should be tested in multi-
facetted pilot projects, during which implementation is closely monitored with a continued feed­
back from the community.

Transfer of know-how is a continuous process, and one in which the following parties
play an important role:

Government authorities especially those responsible for public health and food control:

to adopt and implement policies, where appropriate, regarding the improvement

of water quality, control of agricultural residues, promotion o f improved crop
cultivars (acceptable to subsistence agriculture) at the level o f the household; and

to develop and implement a two-way communication mechanism between the

central government offices and the household to facilitate education.

International agencies: to participate in the development and introduction o f policy and in the
implementation of projects.

Non-governmental organizations: to contribute to the process of policy making and

implementation of policies.

Public educators: including teachers and consumer groups engaged in food and nutrition and
health care education. This includes formal and non-formal education structures (community
forums, newspapers and media).

Scientisls/academia: to assist in research and education in food technologies, and fermentation

in particular.
 26

8. RESEARCH NEEDS

A comprehensive overview o f the research on fermented foods used throughout the

world was presented during the Workshop, The current status of research was assessed with
particular emphasis on understanding the potential and effects of using fermented foods as
weaning foods. The crucial questions addressed were:

• With our current knowledge of fermented foods, can the use o f these foods be
promoted as safe and nutritional foods, particularly for infants and young
children?

• Whether future research is required to improve the safety o f fermented foods

used at the household level?

• With the worldwide importance of small-scale food processing enterprises

(i.c. cottage industries), what arc the research priorities to ensure that
fermented foods are safe for the consumer?

• What arc the socioeconomic and cultural issues that need to be addressed to
ensure that fermentation is adopted both at the household and cottage levels?

Each identified research need was analysed to determine the relative research priority,
taking into account the state of the current knowledge and the severity o f the problem. It will
be essential in any o f these studies to take into account diff erences between rural and urban
dwellers.

Research issues In four areas were considered, namely: food safety, nutritional vaJue,
technology development, and technology transfer and related socioeconomic aspects.

8.1 Food Safety

8.1.1 Efficiency of fermentation in biological safety

A considerable amount of work has been done on the effectiveness o f lactic acid
bacterial fermentation for the inhibition of a wide range o f pathogenic bacteria. A meta­
analysis would enable a quantitative analysis of these data, for trends. Mathematical models
describing the survival of pathogens in lactic acid fermentation would have a useful
predictive value without recourse to challenge testing. A few research opportunities exist in
this area specifically related to the survival o f sub-lcthally injured organisms and certain acid-
tolerant pathogens such as Escherichia call 0.157:117.

Little information exists on the destruction o f parasites (such as trematodes) during

fermentation. Limited information is available on the fate of viruses during fermentation, but
there is still need for some further studies on their survival. Fart oi the reason for the lack of
information on viruses and parasites is associated with the problems of enumerating them.
 27

It is essential that a multidisciplinary approach to these problems is taken. It is very unlikely

that the growth of mycotoxigenic fungi represents a problem in anaerobic fermentations.

In studies on the efficiency of fermentation in the inhibition of pathogenic

microorganisms, it is important to distinguish between those present in raw materials and
those introduced into the product during and after processing (for example, after cooking).

Laboratory observations of the inhibition o f pathogenic organisms need to be verified

under household conditions.

Research is needed on the epidemiology of diarrhoea among infants and young

children who are receiving fermented or nomfermented foods. Such studies will require very
careful control of epidemiological design for the confounding variables and the differences
that might occur between experimental and control groups. U is recommended that a
carefully produced protocol is subjected to widespread critical peer review before the
implementation of the studies.

Research needs:

• To determine effects of lactic acid fermentation on parasites and undertake more

confirmatory studies on the effect o f the process on viruses. [High priority]

• To establish the effect of fermentation on su b- lethal Iy injured pathogenic bacteria

and certain pathogens such as Escherichia coli 0157:H7. [High priority]

• To determine the effect oiThe consumption o f fermented foods on the incidence of

diarrhoea by studying the epidemiology o f diarrhoea among infants and young
children receiving fermented or non-fermented foods. [High priority]

• To undertake a meta-analysis o f current literature on the inhibition of pathogenic

bacteria and the development of appropriate mathematical models for assessing
safety. ]Medium priority]

• To verify laboratory observations o f the inhibition of pathogenic organisms under

household conditions. [Medium priority]

Overall, research in this area is considered to have a high priority

 28

8,1.2 Effect of fermentation on biochemical/chemical toxicants in raw materials

Fermentation cannot be seen as a means o f cleaning up contaminated raw materials.

However, recognizing that contaminated raw materials are frequently used, further research
on a number o f issues is justified. The importance of water quality in the fermentation
processes must also be addressed.

Limited information is available on the effect o f fermentation on mycotoxins. Some

information exists with respect to aflatoxin. Very little is known about the effect on bacterial
toxins that might be present. 1'oxicity of mycotoxin breakdown products is largely not
understood. Further work is justified in these areas, but the long-term solution lies in
improving raw material quality.

Consideration needs to be given to the effect (including changes to bioavailability) o f

fermentation on environmentally-acquired (in food and soil) chemical contaminants, such as
heavy metals, trace elements, herbicides, and pesticides.

Research needs:

• Effect of fermentation on mycotoxins and on the toxicity o f breakdown products.

[High priority]

• Effect of fermentation on environmental contaminants. [Medium priority]

• Effect of fermentation on bacterial toxins. [Low priority, because o f focus on

dried grains]

Overall, research in this area is considered to have a medium priority

8.1.3 Additional considerations in the promotion of fermentation

The extent of knowledge on the potential problem of D-lactatc acidosis is limited.

Studies need to be undertaken to determine whether a problem with D -(-) lactate acidosis
exists or potentially exists when fermented foods are consumed. 'There is a need to
specifically consider the situation with regard to malnourished children who may have
impaired buffering capacity.

(■are should be exercised to ensure that the generation of biogenic amines or other
toxic materials such as ethyl carbamate does not occur. This could be done by the
optimization of the various processing steps involved in the preparation of fermented foods.
This is considered to have low to medium priority because of the reported lack o f a problem
with fermented cereal and legume foods.
 29

Research needs:

* Investigation into the significance oi D -(-) lactate acidosis associated with the
consumption of fermented foods. [High priority]

• Optimization of processing with respect to biogenic amines and ethyl carbamate

(ethylurcthane). [Low to medium priority]

Overall, research in this urea is considered to have a high priority

8.2 Nutritional value

A major objective is to provide infants and young children with products o f high
nutritional value. It is important to consider the whole process in relation to nutritional value
and not just the fermentation step.

The reduction in the levels of anti-nutritional factors is important, but it is important

to understand the mechanism by which changes occur. For the purpose o f this review of
research needs, cyanogenic glucosides are considered in this section.

Anti-nutritional Present status of Severity of Research need

factors knowledge problem

Phytate good (some gaps) high medium-high

Tannins moderate high high

Protein inhibitors moderate high medium

Others (lectins, poor high medium

saponins)

Oligosaccharides moderate high medium-high

Cyanogenic good medium relatively low

glucosides
 30

O f equal importance to reduction of anti-nutritional factors is the improvement o f the

bioavailability of micro-nutrients. It is important to compare the micro-nutrient status and
growth of infants and young children fed fermented and non-fermented cereals.

There is a need to investigate the mechanisms in the fermentation process that

influence the bioavailability of nutrients, especially iron, zinc, calcium and protein.

Research needs:

* Reduction in levels of anti-nutritional factors focusing specifically on the

mechanisms of change during the whole process. | Medium to high priority]

* Investigation of the mechanisms in the fermentation process that inlluen.ee the

bioavailability of nutrients, especially iron, zinc, calcium and protein. [Medium to
high priority]

* Comparison of the mieronutrient status and growth of children under live fed
fermented and non-fermented cereals. [Medium priority]

Overall, research in this area is considered to have a medium-high priority

8.3 Technology development

8.3.1 Characterization of fermentations

There has been a large amount of work on the microbiological characterization ol

fermented foods. Justi fication for future work is relatively low with the exception o f the need
to understand the dynamics of natural, fermentations. Those fermentations that have not been
studied should be considered.

Extensive documentation exists on the methods of'processing fermented foods. There

arc some gaps in the literature and there is a need to verily the existing data. The
dissemination of currently available information has a high priority.*•

Research need:

• Characterization of previously uninvest!gated fermentations, especially where they

are used or could be used for feeding infants and children. ]Higb priority]
 31

8.3.2 Dcvclopment/improvement of fermentation systems

It is recommended that research on starter cultures adopt the following approaches:

a) Determination of the need for and feasibility of using starter cultures. Specific
attention should be given to cost:bcnefit analyses and processor/consumer requirements. The
level of knowledge in this area is low and hence the priority for research is high,

b) Establishment o f the appropriate level o f technology. This might range from the use
of back-slopping to the use of defined starter cultures with specific biochemical properties.
The approach taken is dictated by the needs o f the target groups (a) and an understanding of
the scale and nature of operation. There is a reasonable level of knowledge on some aspects
of this subject and hence research is given medium priority.

c) Development o f appropriate starter culture delivery mechanisms. Mechanisms for the

distribution and maintenance of starter cultures must be developed with a good understanding
of the conditions under which they will be used and their cost. Little work has been done in
this area and the need for research is high, provided that the selected level of technology
demands it.

d) Selection o f microorganisms with desirable properties. Such properties might include

the possession of phytase active at low pH values and high levels of acid production.
Whereas there is a moderate amount of knowledge on this subject, further research should
receive high priority where issues a, b, and c above have been properly addressed.

Based on a sound understanding of the changes that occur during fermentation and
knowledge of consumers and/or processor requirements, there is the potential to optimize
fermentation conditions to provide a range of benefits. This provides an alternative to the
development of starter cultures.

Research needs:

• Development of appropriate starter cultures for lactic acid bacterial fermentations,

according to the sequence of activities mentioned above. [High priority]

• Optimization of fermentation conditions to achieve specific benefits. [High

priority]
 32

8.3.3 Probiotics

The consumption of live lactic acid bacteria (such as Lactobacillus acidophilus) is

thought to help prevent diarrhoeal disease. Such effects are desirable for weaning foods. The
feasibility of using microorganisms as probiotics should be assessed. It will be important to
take into account problems o f starter culture development (see above), acceptability to the
consumer, distribution and maintenance of starters, and the fact that many gruels are boiled
before consumption.

Research need:

• Determination of the feasibility o f the use of specific microorganisms with

probiotic activities. [High priority]

8.3.4 Effects o f each processing stage on food safety

It is important to understand the role that individual and combinations o f processing

stages play in the safety of the final product. Such processing operations include cooking,
washing, peeling, grinding, dehydration, packaging and fermentation. An example o f this is
the order of cooking and fermentation in the preparation of weaning gruels. Changing the
order of these stages has implications for food safety.

Research need:

• Investigation (HACCP studies) into the role o f individual processing steps and
combinations of steps in ensuring food safety. [High priority, but only where
there are specific gaps in knowledge]

8.3.5 Application of quality and safety systems (including HACCP)

Few studies have assessed fermentation as a household level technology in terms of

food quality and safety. The application o f the HACCP approach and the principles o f good
manufacturing practice offer great potential for focusing education and extension
programmes.
 33

Research needs:

• To assess the hazards and risks associated with the household preparation and
processing (biological, chemical, physical) of infant foods. [High priority]

• To determine the Critical Control Points in the processing and preparation of

fermented weaning foods at the household level with respect to food safety and
quality. [High priority]

• To determine the most appropriate means o f transferring knowledge o f improved

procedures in safety and quality. [High priority]

Overall, research in this area is considered to have a high priority

8.4 Technology transfer and related socioeconomic aspects

8.4.1 Consumer and producer perception and needs

Research is needed to understand consumer and producer (processor) perception of

food safety and specifically of fermentation. It is not known whether food safety is a
significant enough issue in iLs own right for these target groups to adopt fermentation or
change traditional practices. For example, if fermented food is being promoted as a means of
reducing the incidence of diarrhoeal diseases in children, the benefits to the household have
to be obvious if change is going to take place.

There are many reasons and advantages for using fermentation, including extending
shelf-stability, addition of variety to the diet, as an income generating activity, nutritional
benefits, and processing otherwise unusable raw materials. Even with these advantages, there
are some communities that have discontinued using fermentation processes.

The initial stage in safety improvement o f a fermentation process is understanding

why that process is used. This would be an important part of a needs assessment, which
should be carried out as an initial step in any research programme. The needs assessment
should also determine what the perceived issues and problems axe for both the processor and
the consumer.

It may be possible to make changes to existing fermentation systems or introduce a

fermentation process for food safety purposes if one can also demonstrate advantages such as
extended shelf-life, cost savings, reduction in processing time, and improvement in taste or in
nutritional quality. This requires an understanding of consumer and processor needs and
perceptions. If fermented products are to be promoted as safe weaning foods, it is particularly
important to evaluate the contribution that these foods make to the nutritional needs o f the
child.
 34

During the implementation of any research project, it is crucial to have continuing

interaction between scientists, processors and end-users to ensure that any changes to the
process or product arc acceptable, practical and cost-effective.

Re^earpJ^ne.eds:

* To gain a greater understanding o f consumer perceptions of food safety and the

significance of this with respect to modifying food processing practices. [High
priority]

* To gain an understanding of the needs and perception of processors in relation to

their use of fermentation and potential adoption o f the technology, [High priority]

* To evaluate the potential contribution o f fermented foods to the daily nutritional

requirements o f weaning infants and children, [High priority ]

* To determine why the use o f a particular food fermentation has been discontinued,
or continued in certain communities. [Medium priority]

Overall, research in this area is considered to have a high priority

8.4.2 Transfer of information and technology to meet the needs

of the target arouns in relation to food safety

The requirement for needs assessment studies was emphasized elsewhere in this
Report. It is essential that such studies form an integral part o f any project and arc carried out
not only at the beginning, hut also during and after project activities. It is important to
include target groups in the research exercise thereby considering them as partners rather than
observers. Monitoring and evaluation are essential parts o f the project cycle to determine
whether or not an approach is effective and allows for corrective measures.

Adaptive research (pilot studies) is required to develop and modify technologies in

partnership with target groups. Pilot studies can also be a useful tool in assessing the most
appropriate means of technology and in formation transfer. It is important to recognize that
different approaches will be required according to the scale o f operation, for example the
dissemination of fermentation and associated training may be appropriate at the household
level. There is a need to understand the most appropriate mechanisms o f education and
communication to facilitate rapid and sustainable technology adaptation. In the transfer of
technology/information on food fermentation, there might also be an opportunity to transfer
other information such as that related to health, hygiene, food sa fe ty and nutrition.
 35

Research needs:

* Adaptive research to develop and adapt processes. [High priority 1

• Determination of appropriate mechanisms o f education and communication.

['High priority]

8.4.3 Research issues relevant to the household

The driving force behind the adoption o f fermentation for domestic use, including
infant feeding, is food security. Safety issues are important, but probably have a lower profile
from the mother’s perspective than from the commercial perspective. Key issues will include
quality of raw materials, ease of processing, energy use, and the extension of shelf-life for use
within the home. The role of women is a specific issue that will determine the nature o f the
technology and how it is transferred. It will be important to make changes In small
incremental steps so that the development is sustainable. One suitable approach may be the
development and dissemination of fermentation kits,

8.4.4 Research priorities relevant to cottage industry

The adoption of fermentation at the commercial level is driven by the need to make a
profit. Food regulation is a significant consideration in some countries. The research
priorities of relevance are dictated by these issues. Starter cultures may be more relevant in
this case than for domestic use, and the appli cation o f the principles o f good manufacturing
practice and other quality /safety criteria should be appropriate. Safety will have a high
profile since it contributes to a commercial reputation. Product distribution issues are critical,
and this would be expected to be a driving force behind the need to extend shelf-life.
 36

9. CONCLUSIONS AND RECOMMENDATIONS

9.1 Conclusions

9.1.1 General

Lactic acid fermentation can contribute towards the safety, nutritional value, shelf-life
and acceptability of foods for infants and young children. It is an advantageous technology,
in the sense that extension of shelf-life, enhancement o f sensory properties, safety and
improved nutritional value are achieved by one technique which is affordable at the
household level.

On its own, fermentation cannot eliminate all food-related health risks, but its benefits
can be enhanced when combined with other unit process operations such as soaking, grinding
and particularly cooking. Though shortcomings in the use o f fermentation as a household
food technology exist, options and solutions have been identified and proposed. There is a
great need to ensure that existing knowledge o f the fermentation technology is used for the
maximum benefit of households and cottage industries.

The education o f food handlers and consumers about the proper application o f
fermentation as part of the total food preparation process is essential.

The assessment o f socioeconomic and cultural aspects is essential to enable the

optimum utilization of fermentation technology for the preparation o f weaning foods. The
socio econo mi cal and cultural considerations should be integrated with key concepts o f food
safety, nutrition and household food security, and prevention and control o f infection and
care, if improvement is to be achieved in the nutritional status of infants and young children.

9.1.2 Safety

Major benefits include the inhibition o f growth o f most pathogenic bacteria, the
inhibition o f formation o f bacterial toxins, and the degradation of some plant toxins
e.g. cyanogenic glycosides.

In combination with other regular food preparation operations such as cleaning,

cooking and appropriate hygiene, adequate protection is provided against most foodborne
diseases of microbial and chemical origin. An exception should be made for pesticide and
mycotoxi.n contamination occurring in the raw food materials. These are mostly not affected
by fermentation or other process operations usually accompanying the fermentation step.

The prevalence o f diarrhoea among infants and young children is influenced by the
interaction of organisms in the environment (water, food, soil), hygienic behaviour, the
virulence and number of organisms and prior health and nutritional status o f the host.
Despite the favourable effect o f fermentalion on contamination levels in food, it is not yet
known whether the use of fermented food will additionally protect against diarrhoea when all
the above variables are controlled.
 37

9.1.3 Nutritional value

Preparation of foods of plant origin by processes involving fermentation contributes to

the degradation of some anti-nutritional factors, e.g, phytate, thus increasing mineral
bioavailability, to the improvement of the protein digestibility o f tannin “rich cereals, and to
the improvement of carbohydrate tolerance by degradation o f flatulence causing oligo­
saccharides. When germinated cereal grains arc included as an ingredient in fermented
weaning foods, reduction of viscosity enables the preparation o f semi-liquid porridges with
increased nutrient density.

9.1.4 Shelf-life

In the absence of facilities for refrigeration and/or hot-holding, lactic acid

fermentation provides an affordable method to extend the shelf-life o f food. However, good
care should be taken to ensure that fermentation results in rapid and adequate acidification.

9.1.5 Acceptability

Lactic acid fermentation provides a variety o f tastes to otherwise bland foods.

9.1.6 Research needs

High priority research needs were formulated within the areas o f food safety,
nutritional value, technology development, and technology transfer and related socio­
economic aspects. Some major questions to be resolved include the effect o f lactic acid
fermentation on the fate of parasites, viruses and certain pathogenic bacteria; the effect of
fermentation on mycotoxins and the toxicity of breakdown products; the significance o f
D -(-) lactate acidosis associated with the consumption o f fermented foods; the effect of
fermentation on the anti-nutritional impact o f tannins on nutrient bioavailability;
characterization of hitherto uninvestigated fermentations; development o f appropriate starter
cultures; optimization of fermentation conditions to achieve specific benefits; feasibility of
the use of probiotic microorganisms; development and application o f quality and safety
systems (including IIACCP); assessments o f consumer and producer perception of
fermentation and needs; assessment of appropriate mechanisms o f communication and
education; and transfer of information and technology to households and cottage industries
through adaptive and participatory pilot projects.

9.2 Recommendations

9.2.1 Policy matters

The present exchange of information between mothers, manufacturers, scientists,

government and non-government organizations needs to be improved.
 38

It is recommended that medical, health, technological and sociological services arc

integrated to coordinate efforts against foodbome diseases, with food fermentation as an
integral part of this action.

Safety considerations should be integrated when fermentation is advocated and

promoted for nutritional purposes.

In communities where lactic acid fermentation is usually carried out, this practice
should be encouraged while educating the food handlers, in line with the HACCP approach,
about the critical points in the process for controlling the safety o f the products. Existing
socioeconomic and cultural relations and patterns should be examined, and the type of
support which is needed to improve the safety and nutritional value o f fermented foods
should be identified. Appropriate communication strategics and means should be developed
and applied, to inform households about the appropriate food processing techniques with
respect to fermentation.

If lactic acid fermentation is not known or used, a sociocultural assessment should be

made of the appropriateness and feasibility o f fermentation practice in that communi ty, and
its food safety and nutrition implications, prior to any attempt to formally introduce
fermentation technology.

Education or development o f communication strategies should be based on KAP

(a methodology for the assessment o f Knowledge, Attitudes, and Practices) and HACCP
studies, from which community needs will be derived. On the basis o f these identified needs,
information can be disseminated, preferably utilizing existing and already well-established
strategies.

9.2.2 Research

Research in the high priority areas as mentioned above and listed in more detail in
section 8 should be promoted and supported. The execution should preferably have a
collaborative and multidisciplinary character.

A follow-up to this Workshop, e.g. in the form of a “forum”, touching on all the
matters referred to in these recommendations should be planned in the near future.

A network of scientists should be established to facilitate exchange o f information,

coordination o f research efforts, and dissemination o f results. Such a "food fermentation
network" should be adequately affiliated with international professional organizations,
governments andN G O ’s.
 39

GLOSSARY

Acidosis
A pathologic condition resulting from accumulation o f acid or loss of base in the body, and
characterized by increase in hydrogen ion concentration (decrease in pH),

ARP
Amylase Rich Flour. See also: Power Flour.

Back-slopping
The practice of employing material from previous successful batches as a fermentation starter
culture. In fermentation of cereals, root crops and leguminous seeds (beans, pulses), back­
stopping usually results in a gradual dominance oflactic acid bacteria.

Contaminant
Any biological or chemical agent, foreign matter or other substance present in the food - not
intentionally added - which may compromise food safety or suitability.

Control (verb)
To take all necessary actions to ensure and maintain compliance with established criteria.

Control (noun)
The state wherein correct procedures arc being followed and criteria are being met.

Control measure
An action or activity that can be used to prevent or eliminate a food safety hazard or reduce it
to an acceptable level.

Corrective action
A type of action to be taken when the results o f monitoring the CCP indicate a toss o f control.

Critical Control Point (CCP)

A step at which control is essential to prevent or eliminate a food safety hazard or reduce it to
an acceptable level.

Critical limit
A value which separates acceptability from unacceptableness.

ERF
Hnzyme Rich Flour. See also: Power Flour.
 40

Fermentation
A desirable process of biochemical modification o f primary food products brought about by
microorganisms and their enzymes. Fermentation is purposely carried out to enhance taste,
aroma, shelf-life, texture, nutritional value and other attractive properties o f food.
Fermentation is often part of a sequence o f process operations incl uding one or more o f the
following: cleaning, grinding, soaking, salting, cooking, packaging, and distribution.

Fermentation (characterization of):

The investigation and description o f microbiological, chemical and other relevant changes
taking place during a fermentation. Characterization of fermentations is required to
understand the factors and substances affecting food quality and safety.

Foodhorne disease
A disease, usually either infectious or toxic in nature, caused by agents that enter the body
through the ingestion o f food. The term 'food' includes drinking-water, or water used in food
preparation.

Food safety (state)

Assurance that food will not cause harm to the consumer when it is prepared and/or eaten
according to its intended use.

Food safety (measure)

All conditions and measures that are necessary to ensure the safety and suitability ol food for
human consumption at all stages of the food chain.

Food hygiene, Food sanitation

For the purpose of this Report, these terms are considered as synonymous to food safety
(measure).

Good Manufacturing Practice

Practices employed by food manufacturing enterprises that are necessary to produce quality
food products conforming to food laws and regulations.

Good Hygienic Practice

Practices during food handling that are necessary to conform with basic food hygiene rules.

HACCP system
A scientific and systematic way of enhancing the safety of foods from primary production to
final consumption, through the identification, evaluation and control o f hazards which are
significant for food safety.

Hazard
A biological, chemical or physical agent in, or condition of, food with the potential to cause
an adverse health effect.
 41

Ha usehold tecbiology
The combination of methods, utensils and manual labour, as are available in the average
home. It may happen that certain steps in food preparation, e.g. grinding, need to be
performed for a lee, using equipment and know-how from outside the household. Household
technology is primarily used to feed the household, i.e. a family group eating from the same
pot. In this case, a direct link exists between the person preparing the food and the family
consuming it. The risk of adulteration is low, and usually the products are not subject to
official food inspection.

When food is prepared on a large scale for commercial purposes, the term ' enterprise'
is used. This may mean a single entrepreneur, small cottage- or village-based enterprises, or
even semi-industrial ones, ail depending on the scale of production, the number o f employees
and the level of capital investment. Even in an industrial setting much of the technology
employed could still be regarded as "household technology", as described above in terms of
methods, equipment and low degree of technical sophistication. However, commercial
production activities may involve more complicated channels leading from producer to
consumer. This increases the risk of adulteration; thus such products arc, or should be,
subject to official food inspection,

inoculation belt (as used in Ghana)

Belt of woven plant fibre used as a fermentation starter culture, e.g. in the traditional brewing
process of "p ito \ a maize-sorghum beer. The belt is held suspended in the vessel during
fermentation and serves as an attachment site for the predominant microorganisms, in this
case lactic acid bacteria and yeasts. Towards the end of the fermentation, the belt is removed,
gently dried and kept until required for the next fermentation.

L-(+) and D-(-) Lactic acid

Lactic acid is optically active as it contains an. asymmetric carbon atom. The two mirror-
image optical isomers L-(+) and D -(-) lactic acid are rotating the axis of polarized light to the
right and left, respectively. L-(+) lactic acid can be metabolized by man, whereas D -(-) lactic
acid is absorbed by the human body but not metabolized. Consequently, if consumed in large
quantities it may result in acidosis. Lactic acid bacteria produce a mixture of the two optical
isomers in a ratio characteristic for their species.

Monitor
The act of conducting a planned sequence of observations or measurements of control
parameters to assess whether a CCP is under control.

Power flour
Germinated cereal grain (mostly sorghum or millet), either dried in the sun or artificially at
temperatures not exceeding 50°C, and ground to flour. This material, also referred to as malt,
contains active starch degrading enzymes which enable the liquefaction o f a stiff gelatinized
gel of cooked starch (such as cooked cereal or root crop-based food). The sudden change in
viscosity explains the name of the product.
 42

Ragi (as used in Indonesia)

A common name for a dried and shelf-stable rice floor-based fermentation starter culture, fo r
example, ragi tape is used as a starter culture to ferment glutinous rice to tape ketan\ this
particular ragi contains a mixed starter culture o f an amylolytic mould (Amylomyces rouxii), a
yeast (llyphopichia burtonii) and some lactic acid bacteria. The starter culture is prepared in
the household or in cottage industry, in the shape of coin-si zed tablets, which can be crushed
and sprinkled on the material to be fermented.

Starter culture
A. starter culture is defined as material containing a high concentration o f live microorganisms
which is added to raw food materials with the intent of speeding up the process of
fermentation. Lactic acid fermentation is often promoted by adding large numbers o f active
lactic acid bacteria. Most simply this could be done by back-siopping.

Step*
A point, procedure, operation or stage in the food chain, including raw materials, from
primary production to final consumption.

Usar (as used in Indonesia)

A dried and shelf-stable starter culture used to ferment soya beans to tempe kedele, a mould-
fermented soya bean cake. Plant leaves (such as Hibiscus tiliaceus) which have a rough
surface, to which the fermentation microorganism (moulds such as Rhizopus oligosporus in
this ease) arc able to atLach are used. After growing the mould sandwiched between leaves,
the latter are sun-dried. The material to be fermented (cooked soya beans) is rubbed between
some leaves of usar in order to transfer the mould spores from the starter culture to the beans.
The used usar leaves are then discarded.6

6 In relation to the HACX'P system

 43
ANNEX 1
LIST OF BACKGROUND PAPERS
The following is a list of papers presented by the some of the participants at the Workshop,
Copies can be obtained by writing to the authors. The address given here is that o f the first
author.
Title
Review of the sensitivity of different
foodborne pathogens to fermentation
Use of Starter Cultures in Fermentation
on a Household Scale
Household Food Safety in Developing
Countries with regard to Fermented Foods
Lactic fermented foods and their benefits
in Asia
Fermentation - The key to food safety assurance
in Africa?
Contaminated weaning food: a major risk
factor for diarrhoea and associated
malnutrition
Author
M.R. Adams and L. Nicolaides, School
o f Biological Sciences, University of
Surrey, Guildford, Surrey GU2 5XH, UK
W. Flolzapfel, Institute o f Hygiene and
Toxicology, Federal Research Centre for
Nutrition, Engesserstrasse 20, D-7613I
Karlsruhe, Germany
Z. Merican, Senior Research
Officer, Food Technology Research
Centre, Malaysian Agricultural Research
and Development Institute (MARDl),
P.O. Box 12031, G.P.O., 50774 Kuala
Lumpur, Malaysia
C.-H, Lee, Department of Food
Technology, College of Natural
Resources, Korea University, 1 Anam-
dong, Sungbuk-ku, Seoul, 136-701
Korea
P. Mensah, Noguchi Memorial Institute
for Medical Research, P.O. Box 25,
Legon, Ghana
Y. Motarjcmi, F, Kafcrstein, G, Moy and
F. Quevcdo. Food Safety Unit,
World Health Organization, 20, Avenue
Appia, CH-121 ] Geneva 27,
Switzerland.
 44

Title A uthor

Technological aspects of preparing M J.R , Nout and P.O. Ngoddy

affordable fermented weaning foods Department of Food Science,
Agricultural University, Bomcnweg 2,
6703 D Wageningen,
The Netherlands

Lactic fermented foods in Africa O.B. Oyewole, Department o f hood

and their benefits Science and Technology, University of
Agriculture, P.M,B. 2240, Abcokuta,
Ogun State, Nigeria

Food Safety and Fermented Foods in F. Quevcdo, Food Quality and Safety
in Latin America Assurance International, Las Petunias,
140, Dpto 201, Lima 12, Peru

Socio-economic pitfalls of enhancing T. van de Sande, Socrlaan 17,

indigenous capabilities in household 1185 JG Amstelvccn, The Netherlands
fermentation

Classification o f fermented foods: K.H. Sieinkraus, Cornell University,

Worldwide review o f household 15 Cornell Street, Ithaca, New York 14850
fermentation techniques USA

Fermentation and nutrient availability U. Svanberg and W. Lorri,

Chalmers University of
Technology, c/o SIK; Box 5401,
40 229 Gotcborg, Sweden

Review of the effect of fermentation A, Westby, A. Reilly and Z, Bainbridge

on naturally occurring toxins Natural Resources Institute, Overseas
Development Administration, Central
Avenue, Chatham Maritime, Kent ME4
4TB, UK
 45

ANNEX 2

LIST OF PARTICIPANTS

Prof. John W. Hastings, Department o f Genetics, University o f Natal, Pietermaritzburg, Republic

of South Africa

Prof Alex von Holy, Department of Microbiology, University of the Witwatcrsrand,

Johannesburg, Republic of South Africa

Dr Cherl-Ho Lee, Professor of Food Engineering, Department o f Food Technology, College of

Natural Resources, Seoul, Korea

Dr Wilbald Lorri, Managing Director, Tanzania Food and Nutrition Centre, Dar es Salaam,
Tanzania

Prof S.K. Mbugua, Department of Food Technology and Nutrition, College o f Agriculture and
Veterinary Sciences, University of Nairobi, Kabete, Kenya

Dr Patience Mcnsah, Head Bacteriology Unit, Noguchi Memorial Institute for Medical Research,
University of Ghana, Legon, Ghana

Dr M.J. Robert Nout, Department of Food Science, Agricultural University, Wageningen,

The Netherlands (Rapporteur)

Dr Olusola R. Oyewole, Department of Food Science and Technology, College o f Agricultural

Management, Rural Development and Consumer Studies, University o f Agriculture, Abeokuta,
Ogun State, Nigeria (Chairman)

Prof Fernando Quevcdo, Executive Director, Food Quality & Safety Assurance International,
Lima, Peru ( Vice-Chairman)

Dr Theo van de Sande, Vrije Universiteit, Amsterdam, The Netherlands

Dr Morenike 0 . Sanni, Department of Human Nutrition, College o f Medicine, University of

Ibadan, Ibadan, Nigeria

Prof. Keith H. Steinkraus, Professor Microbiology emeritus, Cornell University, Ithaca, New
York, USA

Dr U lf Svanberg, Department of Food Science, Chalmers University of Technology,

Gbteborg, Sweden

Prof. Andrew Tomkins, Director, Centre for International Child Health, Institute of Child Health,
University of London, London, UK

Dr Jocelyn Webster, Division of Food Science and Technology, Council for Scientific and
Industrial Research, Pretoria, Republic o f South Africa
 46

Representatives o f Other Organizations

Association of African Universities (AAU): Prof. 0 . Onayemi, African Universities House,

Accra-North, Ghana
]unable to attend]

European Union (HU), Brussels, Belgium

j unable to attendJ

Industry Council for Development (ICD): Ms Zahara Mcrican, Malaysian Agricultural Research
and Development Institute, Kuala Lumpur, Malaysia

International Commission on Food, Microbiology and Hygiene (ICFMB):

Dr Wilhcm I-I. Ilolzapfcl, Institute of Hygiene and Toxicology, Federal Research Centre for
Nutrition, Karlsruhe, Germany

International Commission, on Microbiological Specifications for Foods (ICMSF):

Ms Zahara Merioan, Malaysian Agricultural Research and Development Institute, Kuala
Lumpur, Malaysia

International Foundation for Science (IFS): Dr Richard Fuchs, Scientific Secretary, Stockholm,
Sweden

International Life Sciences Institute (ILSI), Washington, USA

[unable to attend]

International Union of Food Science and Technology (lUFoST): Dr Lilian Marovatsanga,

Institute o f Food, Nutrition and F’amily Sciences, Harare, Zimbabwe

International Union of Nutritional Sciences (IUNS): Dr M J. Robert Nout, Department of’Food

Science, Agricultural University, Wageningen, The Netherlands

Overseas Development Administration (ODA): Dr Andrew Wcstby, Natural Resources Institute,

Kent, UK

South African Association for Food Science and Technology (SAFST): Prof. Alex von Holy,
Department of Microbiology, University of the Witwatersrand, Johannesburg, Republic o f South
Africa

United Nations Children's Fund (UNICFiF): Dr Joan Matji, Nutrition Consultant, Pretoria
Office, Republic of South Africa

United Nations Industrial Development Organization (UNIDO): Vienna, Austria

[unable to attend 1
Observer

Mrs Ina Willken, Consumer Council, Pretoria, Republic o f South Africa

Secretarial

Dr Gabriel Kouthon, Senior Officer (Food Industries), Food and Agricultural Industries
Service, Agricultural Support Systems Division, FAO, Rome, Italy ( Co-Secretary)

Dr Yasmine Motarjemi, Food Safety Unit, WFIO, Geneva, Switzerland (Co -Secretary)

Mr Alan Reilly, Food Safety Unit, WHO, Geneva, Switzerland

Dr Martin Adams, School of Biological Sciences, University of Surrey, Guildford, UK

(Temporary Adviser)

Local Organizers

Ms Leoni Bosman, Division of Food Science and Technology, Council lor Scientific and
Industrial. Research, Pretoria, Republic o f South Africa

Mr Dave Harcourt, Division of Food Science and Technology, Council for Scientific and
Industrial Research, Pretoria, Republic of South Africa

Ms Brenda Liebenberg, Dietitian, Directorate Nutrition, Department of Health, Pretoria,

Republic of South Africa

Ms Ilze Meyer, Di vision of Food Science and Technology, Council for Scientific and
Industrial Research, Pretoria, Republic of South Africa

Ms F W J van Rijssen, Deputy Director, Food and Chemicals, Department of’Health,

Pretoria, Republic of South Africa

Dr Thco van de Venter, Director of Food and Chemicals, Department of Health, Pretoria,
Republic of South Africa

Dr Jocelyn Webster, Division of Food Science and Technology, Council for Scientific and
Industrial Research, Pretoria, Republic of South Africa

Mr Johan dc Wet, Division of Food Science and Technology, Council for Scientific and
Industrial Research, Pretoria, Republic of South Africa
 48
ANNEX 3
BASIC PRINCIPLES FOR THE
PREPARATION OF SAFE FOOD FOR INFANTS AND YOUNG CHILDREN
• Cook food thoroughly
Many raw foods, notably poultry, raw milk and
vegetables, arc very often contaminated with disease-
causing organisms. Thorough cooking will kill these
organisms. For this purpose, all parts of the food must
become steaming hot, which means they must reach a
minimum temperature of 70 °C.
• Avoid storing cooked food
Prepare food for infants and young children freshly, and
give it to them immediately after preparation when it is
cool enough to eat. Foods prepared for infants and
young children should preferably not be stored at all. If
this is impossible, food could be stored only for the next
meal, but kept cool (at temperatures below 10*C) or hot
(at temperatures near or above 60°C). Stored food
should be reheated thoroughly. A gain, this means that
all parts of the food must reach at least TO^C,
• Avoid contact betw een raw foodstuffs
an d cooked foods
Cooked food can become contaminated through even the
slightest contact with raw food. This cross­
contamination can be direct, as, for example, when raw
food comes into contact with cooked food. It can also be
indirect and subtle: for example, through hands, flics,
utensils or unclean surfaces. Thus, hands should be
washed after handling high-risk foods, c.g. poultry.
Similarly, utensils used for raw foods should be
carefully washed before they arc used again for cooked
food. The addition of any new ingredients to cooked
food may again introduce pathogenic organisms. In this
ease, food needs to be thoroughly cooked again,
• W ash fru its an d vegetables
Fruits and vegetables, particularly if they are given to
infants in raw form, must be washed carefully with safe
water. If possible, vegetables and fruits should be
peeled. In situations when these foods arc likely to be
heavily contaminated, for example when untreated waste
water is used for irrigation or untreated night-soil is used
for soil fertilisation, fruits and vegetables which cannot
he peeled should be thoroughly cooked before they are
given to infants.
Adapted from Golden Rulesfor Safe Food Preparation of Heahh surveillance and management proceduresforfood-
handling personnel: report o f a WHO consultation. Geneva, World Health Organization, 1989 (WHO Technical Report
Series, No. 785),
• Use safe w ater
Safe water is just as important in preparing food for infanta
and young children as it is for drinking. Water used in
preparing food should be boiled, unltsa the food to which
the water is added has subsequently to be cooked (c.g,, rice,
potatoes). Remember that ice made of unsafe water will also
be unsafe.
• W ash h an d s repeatedly
Wash hands thoroughly before you start preparing or
serving food and after every interruption - especially if you
have changed the baby, used the toilet, nr been in contact
with animals. It should be remembered that household
animals often harbour germs that can pass from bands to
food.
• Avoid feeding infants with a bottle
Use a spoon and cup to give drinks and liquid foods to
infants and young children. It is usually difficult to get
bottles and teats completely clean. Spoons, cups, dishes and
utensils used for preparing and feeding infants should be
washed right after use. This wilt facilitate their thorough
cleaning. If bottles and teals must be user!, they should be
thoroughly washed and boiled after every use,
• P ro tect foods from insects, ro d en ts and
o th er anim als
Animals frequently carry pathogenic organisms and are
potential sources of contamination of food.
• Store non -p erish ab le foodstuffs in a safe
place
Keep pesticides, disinfecting agents or other toxic chemicals
in labelled containers and separate from foodstuffs. To
protect against rodents and insects, non-perishable foodstuffs
should be stored in closed containers. Containers which
have previously held toxic chemicals should not be used for
storing foodstuffs.
• K eep ali food p re p a ra tio n prem ises
m eticulously clean
Surfaces used for food preparation must be kept absolutely
clean in order to avoid food contamination. Scraps of food
and crumbs arc potential reservoirs of germs and can attract
insects and animals. Garbage should he kept in safe,
covered places and be disposed of quickly.
 ANNEX 4

APPLICATION OF THE HACCP SYSTEM TO U J I ' 2 3

a. Product description

Preparation of uji varies depending on the region. The following description is one
example of uji preparation as practised in Kenya,

The basic cereal in uji production is maize, but at times a mixture o f maize, sorghum
and millet is used. The raw cereal is finely ground and mixed with water in a concentration
of about 30% solids. The dough, without inoculation, is fermented for 2-5 days at ambient
temperature, and it is then diluted to about 4-5% solids in boiling water, and sweetened with
crystalline sugar.

b. Intended use

Uji is consumed by adults as well as children. For the purpose of this Report, its use
as a weaning food is considered,

c. Flow diagram

Figure 3 shows the flow diagram of uji.

d. Hazards of concern

Hazards considered in this context include biological (e.g. bacteria, viruses, parasites),
chemical (e.g. contaminants, mycotoxins) and physical agents.

e. Identification o f hazards, control measures and Critical Control Points

Table 3 shows hazards associated with each step in the preparation o f uji, and some
possible measures for their control.

1) Raw m aterial: Major hazards in maize, millet and sorghum are toxins, e.g. aflatoxin
produced by moulds, and agrochemicals. For prevention of toxigenic moulds during storage,
the raw material should, as far as possible, be stored under appropriate ambient conditions.
When the ambient temperature and humidity are high, storage time should be limited. In so

1 This study has been carried out by the Joint FAO/WHO Workshop Secretariat,

2 Application of the HACCP system has been simplified and adapted to household conditions. Although
the same approach can be used for production on a cottage and industrial scale, the requirements in terms of Critical
Control Points, critical limits, and monitoring procedures may be different and more severe.

3 Model HACCP plans are not appropriate for use until validated for a specific food and food process.
 50

far as agrochemicals are concerned, households cannot do much except to get assurance from
suppliers about the safety of the products. The possibility o f accidental contamination of
grains during storage with agro-chemicals should be prevented. The grains may also contain
foreign matter such as stones and insect fragments. These will not be eliminated or controlled
at a later step, so it is important that households thoroughly clean the raw material.

Cereals may also be contaminated with pathogens. These will be eliminated at

subsequent steps of preparation, i.e. fermentation and boiling.

Water may be contaminated with pathogens. As part o f a good hygienic practice, sale
water should be used, particularly for washing hands and utensils. As the fermented dough is
subsequently boiled, the quality of water used for its preparation is not considered as a
Critical Control Point with regard to pathogens. However, wi th respect to chemical
contaminants, the quality of water is a Critical Control Point as chemical contaminants will
not be removed, during later stages of preparation.

Crystalline sugar may contain foreign matter. Some foreign matter, e.g. glass,
constitutes a health risk. Care should be taken to see that sugar does not contain any foreign
matter.

2) G rinding: This Step may introduce dirt and foreign matter. As part o f a good
hygienic practice this should be avoided as far as possible by using clean and properly
maintained equipment. However, it is unlikely that this step will introduce any major health
hazard.

3) Dough p rep aratio n : Except for the quality o f water (see step 1), this step does not
present a specific hazard. As a part o f a good hygienic practice, households should use safe
water, as far as possible.

4) Ferm entation: This step is important for preventing the growth of undesirable
bacteria and moulds. However, microorganisms (vegetative form) surviving this step will be
eliminated during the subsequent boiling step. The major hazards associated with this step
are microorganisms producing thermostable toxins, e.g. Staphylococcus aureus, or moulds, as
the toxins will not be destroyed later by boiling. Fermentation is therefore a Critical Control
Point for these hazards. To prevent these hazards, the fermentation process should be rapid,
i.e. characteristic odours and smell of fermentation should appear within 24 hours.

5) Boiling w ater: All pathogens (vegetative form) arc killed during this step.

6) D ilution in continuously boiling w ater: 'Phis step is a critical point for ensuring the
biological safety of uji, as pathogens existing in the raw material or introduced during
previous steps will be killed at this step. It should, however, be noted that spores o f bacteria,
e.g. Bacillus cereus, may survive.
 ..
..

51

7) Sweetening: Provided that sugar or utensils used for sweetening are clean, no major
hazard is associated with this step.

8) Serving: Care should be taken to ensure that pathogens are not re-introduced into the
prepared uji by dirty hands or utensils. Therefore;, these have to be washed carefully with
safe water. This is particularly important with regard to pathogens o f a low-infective dose,
e.g. Shigella, The prepared uji should be consumed as soon as possible. Although the acidity
of the product discourages spore germination, a significant delay in serving may give an
opportunity for the growth of bacterial spores which have survived previous steps
(e.g. spores of Bacillus cer&us) or microorganisms which may have been introduced by dirty
hands or utensils.
 52

Table 3 Application o f the HACCP system to preparation o f g,?7 in households

Step Hazards Control Measures : CCPs Critical Lim it . Monitori n g Proce du re ; Corrective Actions

1. Raw m aterial a. My cotoxins a. a. Yes a. a. a.

i) Maize i) Obtain assurance i) No mouldiness. i) Observation, i) Discard the raw material
Sorghum from supplier of good smell smelling and change supplier
Millet adequate
preharvest and
post-harvest
handling of the
grains

ii) Store grains in dry ii) Adequate time. ii) Time keeping ii) Utilize the raw material
(and if possible temperature, (measurement of as quickly as possible,
cool) area, limit humidity of temperature or when temperature and
storage time storage area humidity if humidity are not
possible) appropriate for storage
b. Agrocliemicals b. Obtain assurance b. No
from supplier of
adequate pre-
harvest and post-
harvest handling of
grains

c. Pathogens: c. Heat treatment, c. Ho

Bacillus cereus, correct
SaimoueUa, E.coli fermentation

d- Physical: d. Manual cleaning d. Yes d. No visible insect d Observation d. Re-clean

insects and stones fragments or stones
Table 3 Application o f the HACCP system to preparation o f uji in households

Step Hazards Control Measures CCPs Critical Limit Monitoring Procedure Corrective Actions

I. Raw m aterial a. Chemical a. Obtain assurance a. Yes a. Clear, free of a. Observation, a. Use another source of
ii) Water contaminants, about the source of odour and off-taste smelling water
depending on the water, use only and tasting
source safe water

b. Pathogens, e.g. b. Use safe water b. No

E.coli, (i.e. filtered and
Campylobacter, disinfected} or boil
K cholerae, the water
Salmonella,
Cryptosporidium,
Giardia lambda,
Entamoeba
histolytica, Rotavirus

1. Raw m aterial Filth, dirt, insect, glass Use clean sugar Yes No visible foreign Observation Clean the sugar (e.g. sieve)
iii) Crystalline matter and if cleaning is not
sugar possible, discard the sugar

2. Grinding Introduction of filth, Use clean and No

dirt, and foreign matter properly maintained
equipment

3. Dough Contamination with Use safe water No

preparation water

4 Ferm entation a. Growth and a. Rapid fermentation a. Yes a. Acid taste and a. Observation a. Discard the material
formation of toxin by characteristic
Staphylococcus odour within 24
aureus hours

L Growth of toxigenic b. Remove surface b. Yes b. No visible moulds b. Observation b. Remove more o f the top
moulds mould growths layer

5. Boiling water Survival of pathogens Thorough boiling Yes Bubbles Observation Continue boiling
 54

Table 3 Application of the HA (HOP system to preparation o f uji in households

Step:, Hazards ( Control Measures CCPs. Critical Limit Monitoring Procedure Correct ive. Actions..

6, Dilution Survival o f non-spore Continuous bolting Yes Gelatmizatiom Observation Keep boiling
(to 4-5% solids forming pathogens W'-ell cooled
in
continuously
boiling water)

7. Sweetening Mo hazard
(in hot ujt) (for hazards associated
with sugar see step l(iii)

8. Serving a. Re-contamination by a. Wash bands and a. Yes a. Washing w-ith soap a. Observation Thorough reheating
hands, utensils, use clean utensils and thorough (steam, bubbles)
environment rinsing with clean
^vater

b. Growth of pathogens b. Consumption b. Yes b. Use within four b. Time keepitrg

and spores of w ithout delay hours
Bacillus cereus, if
consumption delayed
for more than four
hours
 55

ANNEX 5

APPLICATION OF THE HACCP SYSTEM TO T O G W A 121

a. Product description

Togwa is prepared by many tribes in Tanzania, and there arc many variations in its
production. The preparation involves mixing cooked cereals (e.g. maize, sorghum) with
germinated cereals, e.g. finger or bulrush millet or sorghum. Fermentation takes about
9-12 hours, depending on whether or not an old batch is used as a starter culture. If an old
batch or power flour is used, the fermentation is completed in about 6-9 hours.

b. Intended use

Most fermented gruels in Tanzania remain edible for 1-2 days. Beyond this period, the
product is too sour, or gives off an unpleasant odour. Fermented gruels are traditionally
given to children under five years of age.

c. Flow diagram

Figure 4 shows the How diagram oi togwa,

d. Hazards o f concern

Hazards considered in this context include biological (e.g. bacteria, viruses, parasites),
chemical (e.g. contaminants, mycotoxins) and physical agents,

e. Identification o f hazards, control measures and Critical Control Points

Table 4 shows hazards associated with each step in the preparation of togwa and of
power flour which is an essential ingredient in this gruel.

1) Raw m aterial: Major hazards in maize, millet and sorghum are toxins, e.g. allatoxin
produced by moulds, and agrochemicals. For prevention of toxigenic moulds during
storage, the raw material should, as far as possible, be stored under appropriate ambient
conditions. When the ambient temperature and humidity are high, storage time should be
limited. In so far as agrochemicals are concerned, households cannot do much except to get

1 This study bus been curried out by the Joint FAO/WHC) Workshop Secretariat.

2 Application of the HACCP system has been simplified and adapted to household conditions. Although
the same approach can be used for production on a cottage and industrial scale, the requirements in terms of Critical
Control Points, critical limits, and monitoring procedures may be different and more severe.

3 Model HACCP plans are not appropriate for use until validated for a specific food and food process.
 56

assurance from suppliers about the safety o f the products. The possibility o f accidental
contamination of grains during storage with agro-chemicals should be prevented.

The grains may also contain foreign matter such as stones and insect fragments.
These will not be eliminated at a later step, so it is important that households thoroughly
clean the raw material.

Water used in the preparation o f slurry may be contaminated. Boiling the slurry (see
step 9) will eliminate eventual pathogens. Therefore, water used for the preparation o f slurry
is not a Critical Control Point, although as part o f a good hygienic practice, safe water should
be used as far as possible in the preparation of togwa and for washing hands and utensils. On
the other hand, the safety of’water used in the preparation o f power flour is essential, as the
production of power flour does not include a step which would ensure the elimination of
pathogens introduced through the raw material, i.e, water, sorghum or millet. In addition,
pathogens introduced through the raw material may proliferate during the soaking and
germination periods and also survive the sun-drying stage. Therefore, the safety o f water
used for the preparation of power flour is critical for minimizing the contamination of power
flour. The hygienic quality of the power flour is particularly important for the safety o f the
final product, as once the power flour has been added there is no step which would ensure the
killing of acid resistant pathogens.

2) Soaking: During the soaking period, bacterial growth will occur. Use o f safe water
may minimize final bacterial load. If at all possible, soaking should take place at low
temperatures to minimize the growth o f microorganisms.

3) Germination: This usually takes place in layers a few centimetres thick, spread on
mats or leaves, and covered with leaves, mats or gunny sacks to avoid excessive dehydration.
From time to time, the material must be aired and mixed while checking and adjusting the
degree of grain humidity. Further contamination by mats and microbial growth can occur at
this stage. Microbial growth, particularly with respect to toxigenic moulds, can also occur.
As far as possible, germination should be carried out in cool conditions to minimize microbial
growth.

4) Sun-drying: The cover is removed, the sprouted grains arc spread on mats or
bamboo trays to dry in the sun. This may take a few days. All kind o f contaminants and
foreign matter can fall into the sprouted grains, if not well protected. Insufficient drying may
lead to a mi.crobi.ally unstable product during subsequent storage. Thorough drying is critical
for the stability of the product.

5) Storage of sun-dried germ inated grains: Hazards associated with this step are
contamination, for example by rodents and other animals during storage, and microbial
growth, particularly toxigenic moulds, if the germinated grains are not properly dried or are
kept in humid conditions.
 57

6) Grinding to power flour: This step may introduce dirt and foreign matter. As
part of a good hygienic practice this should be avoided as far as possible by using clean and
properly maintained equipment. However, it is unlikely that this step will introduce any
major health hazard.

7) Grinding: Same as step 6

S) Preparation of slurry: Except for the safety of water and cleanliness o f utensils, no
other major hazard is associated with this step. As the subsequent boiling step will kill the
pathogens which may have been introduced at this step, it is not considered a Critical Control
Point. Nevertheless, as a part of a good hygienic practice, households should use clean
utensils and safe water as far as is possible.

9) Boiling: Boiling should be thorough to fully gelatinize all starch. This step is also
essential to kill all pathogens (bacterial spores may nevertheless survive).

10) Cooling: The pot should be covered to protect against dirt or other foreign matter
falling in. It is important that cooling is carried out as fast as possible. Prolonged cooling
may give an opportunity for bacterial spores to grow. When large quantities o f togwa are
prepared, the cooling time can be reduced by dividing the togwa into small recipients.

11) Addition of power flour and to g w a : Two ingredients may be added here to initiate
the fermentation, i.e. power flour and previously fermented togwa. The contamination
brought about by power flour is diverse and difficult to control. Viruses and other acid-
tolerant agents are of particular concern here. The togwa starter culture is quite acid, and will
thus contain only those contaminants which are acid-tolerant in nature.

During the fermentation which follows, acid-sensitive pathogens may be killed.

However, acid tolerant pathogens may survive in togwa. A power flower, prepared under
hygienic conditions may minimize the contamination of togw>a. However, in the absence of
a final killing step, e.g. thorough reheating, the presence of acid tolerant pathogens in
the final product may not be excluded.

12) Ferm entation: During fermentation a rapid dominance o f lactic acid bacteria may
be expected. This is supported by the short fermentation time to reach acidity. A rapid
fermentation is critical lor killing acid-sensitive pathogens and tor the prevention o f bacterial
growth and production of toxin. Addition of togwa enhances fermentation and may be
beneficial provided that it does not introduce acid-resistant pathogens.

13) Serving: It is important to ensure that pathogens are not re-introduced into togwa by
dirty hands and utensils. Therefore, these have to be washed carefully with, safe water.
Depending on the hygienic measures taken to prepare togwa, the final product could be more
or less contaminated, as there is no final Critical Control Point which would ensure the killing
of acid-resistant pathogens. Thorough reheating greatly contributes to the safety o f the final
product. However, implications in terms of textural and other changes should be considered,
as the final product may become unacceptable to the consumer.
 58

Table 4 Application of the HACCP system to preparation o f fogu-a in households

Step Hazards .. Control Measures CCPs Critical Limit Monitoring. Corrective Actions :
Procedure

l.Raiv a. Mycotoxins a. a. Yes a. a. a.

i) Obtain assurance i) No mouldiness. i) Observation, i) Discard the raw material and
material
from supplier of good smell smelling change supplier
i) Maize
adequate pre-
Sorghum
harvest and post­
Millet
harvest handling of
grains

ii) Store grains in dry ii) Adequate time, ii) Time ii) Utilize the raw material as
(and if possible temperature, keeping quickly as possible
cool) area, lint it humidity of storage (measure­
storage time area ment of
temperature
or humidity
if possible)
b. Agro-chemicals b. Obtain assurance b. No
from supplier of
adequate pre-
harvest and post­
harvest handling of
grains

c. Pathogens: c. Heat treatment, c. No

B a c illu s cereiiSj fermentation
S a ltu o a e ifo , E.coU

d. Physical: d. Manria] cleaning d. Yes d. No visible insect d. Observation d. Re-dean

insects and stones fragments or stones
 59

Table 4 Application of the HACCP system to preparation o f togwa in households

Step : Hazards Control Measures CCPs Critical Limit Monitoring Corrective Actions
Procedure

1. Raw material a. Chemical a. Obtain assurance a. Yes a. Clear, free of odour a. Observation, a. Use another source of
ii) Water contaminants, about the source of and off-taste smelling and water
depending on the water; use only tasting
source safe water

b. Pathogens, e.g. b. If safe water b. Yes for b. Bubbles b. Observation b. Re-boil

E.coli, (i.e. filtered and step 2
Campylobacter, disinfected) is not
V. choleras, available, boil the No for
Salmonella, water step 8
Cryptosporidium,
Giardia lamblia,
Entamoeba
histolytica, Rotavirus

2. Soaking Growth of As far as possible at Yes Water should remain Observation, Refresh water
microorganisms low temperatures free from odour or smelling
foam

3. Germ ination Growth of As far as possible at Yes Grains should remain Observation Remove mouldy grains
m icroorganisms: low temperature free of mouldiness
e.g. toxigenic moulds

4. Sun-drying a. Contamination a. Protect the sprouts Yes a. No foreign matter a. Observation a. Clean if possible. If not. discard

b. Inadequate drying b. Ensure thorough b. Sufficient time, b. Time b. As long as there is no

may lead to growth and fast drying adequate exposure keeping, mould growth, re-dry
of microorganisms to sun, dry ambient observation under proper conditions,
during storage conditions, adequate otherwise discard
air circulation,
no mould
 60

: Table 4 Application of the HACCP svste na to.pre pa rat ion of rogyva in households

Step ;Hazards; Control Mea iures CCPs Critical Limit : Monitoring Corrective Actions
Procedure

5. Storage of a. Contamination a. Protect the grains Yes a. No foreign matter Observation a. Clean if possible. Ifnot,
sun-dried discard
germinated b. Growth of toxigenic b. Keep dry b. Dry conditions of b. Discard
grains moulds, ifthe storage, no mould
moisture content is
high

6. G rinding to Introduction o f filth, dirt Use clean and No

power flour and foreign matter properly maintained
equipment

7. Grinding same as step 6

S. Slurry Contamination through Use clean utensils and No

preparation utensils and/or water safe water

9. Boiling Survival of pathogens Thorough boiling Yes Bubbles Observation Re-boil

10. Cooling a. Growth of bacterial a. Ensure rapid Yes a. Short time, room a. Time a. Re-boil
spores cooling temperature within keeping
four hours

b. Contamination b. Protect the b. No foreign matter b. Observation b. Depending on the nature of

porridge during the contamination, either clean, re­
cooling process boil or discard

11. Addition of: a. Contamination by a. Ensure hygienic Yes a. Power flour and a. & b. a.& b. Use another power flour
a. Power flour power flour quality of power togw aoi high Observation and togyva
flour hygienic quality

b. Togwa b. Contamination with b. Ensure the safety b. Absence o f disease

acid-resistant of previously upon consumption
pathogens by togwa prepared togyra o f fOg-U'tf
 Table 4 Application o f the HACCP system to preparation o f togwa in households

Step Hazards Control Measures CCPs Critical Limit Monitoring Corrective Actions
Procedure-

12. Ferm entation a. Growth and a. Rapid fermentation a. Yes a. Acid taste and a. Observation a. Discard the material
formation of toxin by characteristic odour
Staphylococcus within 24 hours
aureus

b- Survival of acid - b. Minimize contami­ b. No

tolerant pathogens nation with acid-
tolerant pathogens
(see step 11)L

13. Serving Recontamination by Wash hands and use Yes Washing with soap and Observation Thorough reheating
bands, utensils, clean utensils thorough rinsing with
environment clean water

1 As there is no Critical Control Point in the subsequent steps which would ensure the killing o f acid-tolerant pathogens surviving the fermentation step, the present process
of togwa preparation may lead to a high risk product.
 62

ANNEX 6

A PPLIC A TIO N OF TH E HACCP SYSTEM TO GARI

a. Product description

Gari is a granular starchy food made from cassava roots. The processing starts with
peeling, washing and grating the tubers. The grated pulp is then, put into bags (often jute, or
woven polypropylene bags) and left to ferment for several days under weight (pressure),
during which time water is also removed. Fermentation is followed by fragmentation, drying
and roasting. During the roasting stage, the core temperature reaches 80-85°C, and the starch
is gelatinized. Palm oil is sometimes added during roasting. After the roasting process, the
gari, as it is now called, is cooled and stored. The final moisture content will determine its
shelf-life. When a final moisture content of below 10% is reached, gari may be stored for
several months. At higher moisture contents, the shelf -life of gari is reduced to a few weeks,
because of potential mould growth.

b. Intended use

Gari is an important part of the staple diet in Nigeria and many other African countries.
It is also given to children over one year. Gari can be prepared in. many different ways. In
the following example, soaking in cold water is used.

c. Flo w diagram

The flow diagram of gari is presented in Figure 5.

d. Hazards o f concern

Hazards considered in this context include biological (e.g. bacteria, viruses, parasites),
chemical (e.g. contaminants, mycotoxins) and physical agents.

1 This study lias been carried out by the Joint. FAO/WHO Workshop Secretarial.

2 Application of the HACCP system has been simplified and adapted lo household conditions. Although
the same approach can be used for production on a cottage and industrial scale, the requirements in terms of Critical
Control Points, critical limits, and monitoring procedures may be different and more severe.

3 Mode) IIACCP plans are not appropriate for use until validated for a specific food and food process.
 63

e. Identification o f hazards, control measures and Critical Control Points

Table 5 shows hazards associated with each step in the preparation of gari, and some
possible measures for their control.

1) Raw m aterial: Major hazards of cassava arc cyanogenie glucosides (linamarin and
lotaustralin), and contamination by agro-chemicals. Cyanogenie glucosides will be
hydrolized and removed during later stages in the processing and preparation of gari,
i.e. grating, fermenting and roasting. However, in regard to chemical contaminants and
agrochemicals, households should obtain assurance from the suppliers about the safety o f raw
products.

Depending on its source, water may be contaminated. While the microbiological safety
of water is of lesser importance when washing cassava, as it will be fermented and heat
treated, it is critical that safe water is used in the final preparatory stages before consumption.

2) Peeling: Some foreign matter and pathogens may be introduced at this step. However,
as the cassava will be washed and heat treated, the control of hazards, other than peeling in
hygienic conditions, is not critical at this stage.

3) W ashing: Microbiological hazards may be introduced if the water is not clean.

Therefore, as part of a good hygienic practice, safe water should be used. Hazards introduced
at this step can nevertheless be controlled during subsequent steps of gari production.
Washing can, though, decrease the amount of foreign matter.

4) G rating: This is the most important step with regard to detoxification when the
cellular disruption results in release of linamarase enzymes, and greater contact o f the
enzymes with its substrate linamarin. Therefore, grating must be thorough to ensure a fast
degradation of linamarin.

Foreign matter and pathogens may also be introduced at this stage. While pathogens
can be killed at the roasting step, prevention and elimination of any foreign matter at this step
is essential.

5) Bagging: Unclean bags may further contaminate the raw material. Chemical
contamination is of particular concern, at this step. The bags should not have been previously
used for purposes which could jeopardize the safety of gari, e.g. for storage of pesticides.

6) Ferm entation: Rapid fermentation is important to prevent growth of undesirable

microorganisms and production of toxins. Fermentation is therefore a Critical Control Point
for control of pathogens.
 64

Fermentation also provides the opportunity (contact time) necessary for the action of
linamarasc on its substrate. During later stages, however, fermentation may have an
antagonistic effect on detoxification, as the decrease in pH resulting from fermentation may
lead to the stability of cyanohydrins. An optimisation o f the fermentation process with
respect to hydrolysis of linamarin and control of microbial growth is therefore important for
ensuring the chemical and microbiological safety o f gari,

7) Roasting; Further detoxification of cassava occurs during roasting. The hydrogen

cyanide is evaporated. Thorough drying at this step is also important for the stability of gttri
and prevention o f mould growth during storage. It is important to prevent formation o f lumps
as these may limit drying and evaporation o f hydrogen cyanide,

8) Cooling; Cooling should take place under hygienic conditions.

9) Storing; To prevent mould growth, gari should be kept under dry conditions, and
protected from animals and rodents.

10) Serving: Water used for soaking gari, as well as hands and utensils, may re-introduce
pathogens. It is critical that the water used at this step is safe, and that utensils and hands are
thoroughly washed.
 65 1

Table 5 Application o f the HACCP system to preparation o f gari in households

Step Hazards Control Measures CCPs Critical Limit Monitoring Procedure Corrective Actions

1. Raw material: a. Agro-chemicals a. Obtain assurance a. No

i) Cassava from supplier of
adequate pre­
harvest and post­
harvest handling of
grains

It b. Cyanogenic b. Grating, b. No
glucosides fermentation and
roasting

c. Pathogens c. Heat treatment c. No

1. Raw m aterial a. Chemical a. Obtain assurance a. Yes a. Clear, free of a. Observation, smelling and a. Use another source of water
ii) Water contaminants, of the source of odour and off- tasting
depending on the water; use only taste
source safe water

b. Pathogens, e.g. R b. Yes for b. b. b.

E.coli, i) Use safe water step 10 i) Indication of i) Inquiry from health e) Boil the water
Campylobacter, (i.e. filtered and contamination authorities
V cholerae, disinfected)
Salmonella,
Qyptosporidiumr or
Giardia lamblia.
Entamoeba ii) Boil the water ii) Bubbles ii) Observation ii) Re-boil
histolytica,
Rotavirus

2. Peeling a. Foreign matter a. Washing a. No

b. Pathogens b. Heat treatment b. No

..........
^SBSsm m A
 66

Table 5 Application of the IIACCP system to preparation of gar i in households

Step Hazards - - Control Measures CCP.s Critical Limit ?Monitoring Procedure Corrective* Actions

3. Washing a. Introduction of a. Use safe water a. No

pathogens through
water

b. Residual foreign b. Thorough washing b. Yes b. As clean as b. Observation b. Re-clean

matter possible

4. Grating a. Residual cyanide a. Complete grating a. Yes a. Absence of coarse a. Observation a. Re-grate
particles
b. Pathogens b. Cleaning the b. No
equipEtient

c. Foreign matter c. Use well- c. Yes c. Free o f visible c. Observation c. Remove foreign material
maintained foreign matter
equipment

5. Bagging Chemical Use clean bags. Yes Absence of chemical Monitor the source and other Use other bags
contamination Obtain assurance from contaminants uses of bags
supplier about no
prey Iotas and
hazardous use of the
bags

6. Fermentation Growth o f pathogen s Rapid fermentation Yes Acid taste and Observation ssnelling and Discard
under weight and production of characteristic odours tasting
toxin, e.g. within 24 hours
Staphy?ococcus aureus
 67
1
Table 5 Application o f tb e HACCP system to preparation o f gari in households

Step Hazards Control Measures CCPs Critical Limit Monitoring Procedure Corrective Actions

7. Roasting a. Residual cyanide a. a. Yes a. a. a.

i) Thorough roasting i) Sufficient time for i) Tlme keeping i) Continue roasting
roasting
ii) Breaking up lumps ii) small size ii) Observation ii) Breaking up lumps
particles

b. Mould growth b. Same as above b. Yes b. Same as above b. Same as above b. Same as above
during storage, if
high moisture
content

8. Cooling Contamination through Cool under hygienic No

environment conditions e.g. putin
clean container and
j clean environment

9. Storing Mould growth during Thorough roasting No,

storage, if high (see step 7: roasting); see step 7
moisture and keep in dry
content conditions

10. Soaking and a. Recontamination a. Use safe water a. Yes a. See step 1 (water) a. See step 1 (water) a. See step 1(water)
serving with water see step 1

b. Recontamination by b. Wash hands and b. Yes b. Washing with b, Observation b. Thorough heating
dirty hands, utensils, use clean utensils soap and thorough
environment rinsing writh clean
water

c. Growth of c. Consumption c. Yes c. Use within four c. Time keeping c. Thorough heating
pathogens and without delay hours
spores of Bacillus
ceveus. if
consumption
delayed for more
■j-_ . y j l .- ytl _v.-j than four hours

::

- SI
I x ix l
 68

ANNEX 7

SUMMARY OF SELECTED PUBLISHED DATA DEMONSTRATING

PATHOGEN INHIBITION BY LACTIC ACID BACTERIA

Hxcerpt from background paper:

Adams, M.R, and Nicolai ties, L. R eview o f s e n s i t iv i ty o f d i ff e r e n t f o o d b o r n e p a t h o g e n s to fe rm e n ta tio n

Species Level of Inhibition Lactic Acid Bacteria Concentration Reference

LAB of Lactic Acid
SALMONELLA.spp.
Fish Sausage .
-V. typhimurium Limited growth during initial Padiococcus Aryanta, R,W,,
12 hours, present in end- acidilactici, isolated Fleet, G,H, and
product. from "Lactacel plus" Buckle, K.A., 1991
( l p 13IS4) High initial
S. sofia j No growth observed. inoculum, >107cfu/g
Fish/Cassava
S, typhimurium Rapidly disappeared during LAB - Lactostart Twiddy, D.R,
ATCC 1311 fermentation at 30 "C. (Chr, Hansen Cross, S.J, and
Laboratory, Denmark) Cooke, R.D., 1987
Cereal Gruels
S. typhimurium Not detected after 48 It in LAB Kingamkono, R, at
No 18375 gruel with added starter at., 1994
| culture.
S. typhimurium Not detected in traditional Lactobacillus Olukoya, D.K. ct
ogi after 6 h, prepared with acidophilus (DK 77) a l, 1994
added starter culture
(DogiK). Lactobacillus pentasus
(DK 99)
■S. typhimurium. The higher the proportion of LAB Nout, M J,R,,
fermented ingredient base Rombouts, F.M,
(supporting a high level of and Havelaar, A,,
LAB), the lower the pH of 1989
the porridge was after
preparation. At pH 14,16 a
reduction in the level of the
pathogen was observed.
Rice-based Weaning Food
S. typhimurium Inhibition occurred only Lactococcus lactis Titratable acidity Yusof, R,M, ,
USCC18375 when initial level of LAB NCIB 497 of pre-fermented Morgan, J,B. and
were present in comparison weaning food Adams, M,R,, )993
with a low contamination Lactobacillus 0.23 - 0.26 %
level of the pathogen. plantarum (96% lactic acid)
The pathogen was unable to
grow when added to the pre- Microbiology Dept,
fermented weaning food Culture Collection,
(24 h). University of Surrey
 69

Species Level of Inhibition Lactic Acid Bacteria Concentration Reference

LAB of Lactic Acid |
Dairy
S. typhimurium Not detected after 30 days in Cheddar cheese starter Abdalla, O.M.,
NRRL-B4420 cheese curd nor, at any time, culture LAB Davidson, P.M. and
in the corresponding brine in (Chr. Hansen Christen, G.L.,
the presence of starter Laboratory, Denmark.) 1993
culture.

S, enteritidis Growth of LAB in souring Titratable acidity Ashenaff M,, 1993

$. typhimurium milk retarded both strains of at 48-60 h = 0,7%
the pathogen between 48-60h
of fermentation. Ergo is
traditionally consumed 24
hours after preparation,
however Salmonella spp.
were present. The 3 day sour
milk was identified as a safer
product.

Meat
S. diihlin Readily destroyed during LAB Smith, J.L. et al,.
S. typhimurium fermentation in Lebanon 1975
bologna prepared with starter
culture.
Salmonella spp. Levels of the pathogen LAB Alford, J.A. and
remained constant or Palumbo, S.A.,
increased by 1 log cycle in 1969
fermented sausage
production.
Laboratory medium
S. typhimurium Not detected in a mixed Lactobacillus Cieplinska, T, and
S. enteritidis culture at pH 3.8. acidophilus Zychowicz, C,,
1974
. 7 CAMPYLOBACTER spp
Cereal gruels
C, jejuni Inhibited after 28 h in LAB Kingamkono, R.
fermenting gruels. etal., 1994
C. jejuni Not detected in traditional Lactobacillus Olukoya, D.K.
ogi after 6 h, prepared with acidophilus (DK 77) e ta l, 1994
added starter culture Lactobacillus pent os us
(DogiK). (DR 99)

} 1
if

■!'i......
i 111'!'1
 70

Species Level of Inhibition Lactic Acid Bacteria Concentration Reference

LAB of Lactic Ac-id
YERSLWA E.NTEROCOUTICA. ■■
Y mterocolUica Not detected in traditional Lactobacillus Olukoya, D.K.
ngi after 6 h, prepared with acidophilus (DK 77) o.Vah, 1994
added starter culture.
Lactobacillus pentosus
(DK 99)
Y. cmcrocnlitica, Antagonistic effect was .Leucnnostac spp. (V 6) Jeppesen, V.i\ and
serotype 0:3 obtained with both strains of Huss, H.H., 1993
LAB. The pathogen was not Lactobacillus
detected after day 4 in extract plantarum (LKE 5)
inoculated with LKE 5 or at
day 6 in extract inoculated
with V 6.
ESCHERICHIA. COLI ■'
Fish Sausage
E. coli (strain 1) Limited growth during initial Ecdiococcus Aryanta, R.W.,
12 hours, present in end- acidilactici, isolated Fleet, G,H. and
product. from "Lactocel plus" Buckle, K.A., 1991
(LPI3I84). High
E, coli (strain 2) No growth observed. initial inoculum,
> J 07cfu/g
Pish/Cassava
E, coli Rapidly disappears during LAB - Lacto start Twiddy, D.R.,
A'l’CC 11775 fermentation at 3010C, (Chr, Hansen Cross, S.J. and
Laboratory, Denmark) Cooke, R.D., 1987
Cereal Gruels
Enterotoxigenic Reduced to undetectable LAB Kinamkono, R. el
E. coli limits after 32 h of at., 1994
ETEC No 2K662 fermentation in the gruel
containing starter cultures.
Enteropathogenic Not detected in traditional Lactobacillus Olukoya, D.K, et
E. coli Ogi after 6 h , prepared with acidophilus (DK 77) aL, .1994
Enterotoxigenic added starter culture
E, coli. (DogiK). Lactobacillus pentosus
(DK 99)
Ricc-based Weaning Food
E. coli Inhibition occurred only Lactococcus lactis Titratable acidity Yusof, R. M.,
ATCC 25922 when a high initial level of NCIB 497 of pre-fermented Morgan, .I.B. and
LAB were present in weaning food Adams, M.R., 1993
comparison with a low level Lactobacillus = 0.23 - 0.26 %
of Lhc pathogen. plantarum (96% lactic acid)
The pathogen was unable to
grow when added to the pre­ Microbiology Dept
fermented weaning food Culture Collection,
(24h). University of Surrey
 71

S p ecies L ev e l o f In h ib itio n L a c tic A cid B a c te ria C o n c e n tr a tio n R e fe r e n c e

LAB o f L a c tic A cid
M ilk
E. coli Growth inhibited by the Lactococcus lact is spp. Isono,Y,, Shingu, I.
OFC 491 presence of LAB. lac Us MOS-11 and Shimizu, S,,
1994
Lactobacillus confusus
NGB- 82
E\ COLI 0157:117
M eat
A five strain mix: No growth of tiie pathogens Lactacel 115 Glass, K.A, et at.,
E. coli Q157:H7 was observed during the (Pediococcus 1992
(932), manufacture of fermented acidilactici). Added as
£ coli 0157:117 dried sausage, initial level of recommended at levels
(CIS), 104cfu/g. As bacteriocins of ca. 107 efu/g.
E. coli 933,EC 204P offer little or no protection
and EC 505 B against Gram negative
bacteria inactivation of
£ co/r0157:H7 in this
product would be due
principally to acidity and
drying.
SHIGELLA spp.
C e re a l G ru e ls
S. sonnei Not detected in traditional Lactobacillus Olukoya, D.K. <st
S, flexneri ogi alter 6 h prepared with acidophilus (DK 77) at., 1994
added starter culture
(DogiK). Lactobacillus pentosus
(DK 99)
S. flexneri Not detected after 48 h in the LAB Kingamkono, R. et
fermenting gruel in the a t 1994
presence of starter culture.
F e r m e n te d M a iz e D o u g h
S. flexneri (20 strains) 14 strains showed complete LAB Mcnsah, P. et aL,
inhibition, whilst 6 showed 1991
partial inhibition in
fermented dough.
R ic e -b a se d W e a n in g F o o d
S. sonnei Inhibition occurred only LaclOcoccuS Iactis Titratable acidity Yusof, R.M.,
USCC 2006 when a high initial level of NCIB 497 of pre-fennented Morgan, IB . and
LAB were present in weaning food Adams, M.R., 1993
comparison with a low Lactobacillus = 0.23 - 0.27%
contamination level of the plantarum (96% lactic acid)
pathogen.
The pathogen was unable to Microbiology Dept.
grow when added to the pro- Culture Collection,
fermented weaning food University of Surrey
(24 h).
 72

Species Level of Inhibition Lactic Acid Bacteria Concentration Reference

LAB of Lactic Acid
Laboratory medium
S. sormei Not detected in laboratory Lactobacillus Cieplinska, 1’. and
medium in a mixed culture at acidophilus Z y ch o w ic C .,
| pH 3.8. 1974
■ VIBRIO sppr ..........
Fish Sausage
V. cholerae Not detected in traditional Lactobacillus Olukoya, D. K, ct
ogi after 6 h, prepared with acidophilus (DK 77) at., 1994
added starter culture.
Lactobacillus pentnsus
(DK 99)
V. par abac m o lytic us No growth observed. Pediococcus Aryartla, R.W.,
acidilactici. High initial Fleet, G.M. and
inoculum, > 107cfu/g Buckle, K.A, 1991
■ STAPHYLOCOCCUS A UREUS ......
Fish Sausage
S. w m s Limited growth during initial Pediococcus Aryanta, R.W.,
12 hours* present in end- acidilactici, isolated Fleet, G.H. and
product. from "Lactocel plus" Buckle, K.A.,
(UM3I84). High J99)
initial inoculum >10'
efu/g.
Fish/Cassava
S, aureus Rapidly disappeared during LAB - Lacto start Twiddy, D.R.,
ATCC 9144 fermentation at 30l"C. (Chr. Hansen Cross, S J. and
Laboratory, Denmark) Cooke, R.D., 1987
Cereal Gruels
S. aureus The higher the proportion of LAB Nout, M,J.R.,
fermented ingredient base Rombouts, F.M.
(supporting a high level of and Havclaar, A,,
LAB) the lower the pH of the 1989
porridge was after
preparation. A t p H s 4 TI6 a
reduction in the level of the
pathogen was observed.
Rice-based Weaning Food
S. aureus Inhibition occurred only Ladococcus lactis Titratable acidity Yusof, R. M.,
ATCC 25923 when a high initial level of NCIB 497 of pre-fermented Morgan, J.B. and
LAB were present in weaning food Adams, M.R., 1993
comparison with a low level Lactobacillus 0.23 - 0.27%
of the pathogen. plantarum (96% lactic acid)
The pathogen was unable to
grow when added to the pre­ Microbiology Dept.
fermented weaning food Culture Collection,
(24h) University of Surrey
 73

Species Level of Inhibition Lactic Acid Bacteria Concentration Reference

LAB of Lactic Acid
Cabbage salad
S. aureus 3-4 generations of growth, Lactobacillus 1.75 g/kg salad Bonestroo,M.H-
followed by a gradual decline plantarum Nos 9 and Sc 2.2 g/kg salad etal., 1993
after 7 hours (change of 20. produced after 7
incubation temperature from h, 3.0 g/kg salad
42 °C to 7°C) After 2 h at T C Sc 3.5 g/kg salad
a rapid decline observed. after 1.5 h at 7°C.

An increase > 1 log cycle Lactobacillus 1,5 g/kg salad

before decline observed after plantarum No P4 produced after 7
100 h. h, 2.7 g/kg salad
Similar decline (>0.5 log after 1.5 h at T'C
cycle when incubation
temperatures changed from
42°C to 76C).

Dairy
S. aureus The growth of the pathogen Lactococcus lactis ssp. 0.9% (w/v) Isono, Y., Shingu, I.
ATCC 25923 was inhibited by the LAB. lactis MOS-11 and Shimizu, S.,
1994
Lactobacillus confusus
NGB-S2
S. aureus Not detected after 30 days in Cheddar cheese LAB Abdalla, O.M.,
NRRL B-4420 curd and 20 days in brine starter culture Davidson, P.M, and
solution of corresponding (Chr. Hansen Christen, G.L., 1993
cheese, in the presence of Laboratory, Denmark)
starter culture.
Meat
S. aureus Growth and subsequent toxin Lactococcus lactis was Haines, W.C. and
production by S, aureus is more inhibitory to Harmon, L.G., 1973
greater at 25°C than at 30°C. S. aureus than
Pediococcus cerevisiae
S. aureus The presence of LAB, LAB Barber, L.E. and
reduced pH level and Deibel, RH., 1972
anaerobic conditions
inhibited the production of
entcrotoxin.
S. aureus The presence of LAB, LAB Peterson, A.C.
reduced pH level and el al. 1964;
anaerobic conditions Daly, C. etal., 1973
inhibited the growth of the
pathogen.
 74

Species Level of Inhibition Lactic Acid Bacteria Concentration Reference

LAB of Lactic Acid
S. aureus Growth is more effectively Lactocnccus lactis Peterson, A.Cl., at
inhibited when the al., 1962; T roller,
proportion of LAB is greater Pcdiococcus ccrcvis iac J.A.& Frazier,W,C.,
than the level of the 1963; Haines, W.C.
pathogen. & Harmon, L.G.
1973; Niskanen, A.
Sl Nurmi, E. 1976;
DiGiacinto, J.V. &
Frazier, W,C„1966

USTE1UA MONOCYTOGENES
Seafood
L. monocytogenes Leuconostoc spp., off- .leppeseri, V.F.,
odours were produced 1993
(diacetyl).

Growth reduced in brined Lactobacillus

shrimp by 3 !og cycles (10fi plantarum
to 1Q1efu/g) after 2.5 hours
incubation at 5nC. The enterococci
isolated from “sous-
vide” cod fillets
L monocytogenes, LAB had a significant Leuconostoc spp., (V6) Jeppesen, V.F. and
Scott A antagonistic effect On the lluss, H.H., 1993
growth of the pathogens. Lactobacillus
planiarum (LKE 5)
Salads - Fermented Sauce
L. monocytogenes, Following inoculation, 2-3 Lactobacillus Spp. Bonestroo, M.I-f
Scott A generations of growth el. at., 1993
occurred during fermentation
followed by a rapid decline
to undetectable levels.
L. monocytogenes, For all test strains the level of LAB Asenati, M., 1994
strains WS2300, pathogen increased by 1.0-
WS230I and WS 1,7 log units during the initial
2302 12 h souring of Ergo. The
counts of the pathogen then
decreased to undetectable
levels after 48 or 60 h in
unsmoked containers.
Smoking of the container
increased the rate of inactiva­
tion when the pathogen was
not detected after 36 h.
L. monocytogenes Not detected by direct plating Cheddar cheese LAB Abdalla, O.M.,
Scott A in cheese with added Starter starter culture (Chr. Davidson, JAM. and
culture 1fansen Laboratory, Christen, G.L.,
Denmark) 1993
 75

Species Level oflnbibition Lactic Acid Bacteria Concentration Reference

LAB of Lactic Acid
L monocytogenes^ Growth inhibited but not Lactococcus lactic Spp. EI-Gazzar, F.A.,
V.7 significantly reduced in cremoris Bohner H.F. and
Tyndallized skim milk and Marth, L.H., 1993
Tyndallized twofold retenate;
level of contamination
reduced by 2 log cycles in
permeate from UK skim milk
L monocytogenes Eventual decrease in levels LAB starter culture Abdalla, O.M.,
Scott A of pathogen in presence of Davidson, P.M. and
starter cultures. Christen, G.L.,
1993

Meat
L. monocylogenes The addition of starter Lactobacillus Campanini, M. et
SSICA 38 and SSICA culture prevented growth of plantarum MCS aL,1993
150, both serotype 1. the pathogen, although low (bacteriocin positive
levels were present during strain)
fermentation and the
subsequent ripening stage. Lactobacillus
L. monocytogenes was not plantarum
isolated from the end- MCS1 (bacteriocin
product prepared with the negative strain)
bactcrocin positive strain
(MCS).
L. monocytogenes Inhibition of the pathogen Lactobacillus Giraffa, G. et al
was demonstrated. plantarum 1994

Lactobacillus curvatus

Leuconostoc spp.
L monocytogenes Will survive the fermentation LAB Buncic, S.
and ripening stages during Paunovic, L. and
the manufacture of fermented Radisic, D., 1991
sausage.
L. monocytogenes Greater than 4 log cycles of LAB Glass, K.A, and
the pathogen were killed Doyle, M.P., 1989
during fermentation and
drying (within 5 days after
the start of the drying cycle).
BACILLUS CEREUS
Fish
B. cereus No viable cells were detected LAB Kingamkono, R. et
No W781 after 24 h in the gruels al„ 1994
containing starter cultures.
B. cereus Not detected after inoculation Lactobacillus Spp, Bonestroo, M.H. et
into salad before al., 1993
fermentation with selected
starter cultures.
 76

Species Level of Inhibition Lactic Acid Bacteria Concentration Reference

La b of Lactic Acid
B . C fire u s Not detected after 24 hours. Pcdiococcus Aryanta, R,W,,
acidilactici, isolated Fleet, G.H. and
from "Lactocel plus" Buckle, K.A.,1991
(LP13184), High
initial inoculum, >107
efu/g.

CLOSTRIDIUM spp.
Fish
C. perfringens No growth observed Pp.dlQCQCCUS Aryanta, R,W,,
acidilactici, isolated Fleet, G .H , and
from "Lactocel plus" Buckle, K.A., 1991
(LP13184). High
initial inoculum, >107
efu/g.
C. perfringenj Inhibition in sous-vide The enterococci Jeppesen, V. F.,
C. botulinum seafood - more detailed work isolated from sous-vide 1993
in progress cod fillets
C sporogenes Rapidly disappear during LAB - Lactostart Twiddy, D, R.,
ATCC 7955 fermentation at 30°C (Chr. Hansen Cross, S. J. and
Laboratory, Denmark) Cooke, R .D , 19R7
 77

References to Review o f sensitivity o f different foodborne pathogens to fermentation

Abdalla, O.M., Davidson, P.M. and Christen, G.L. (1993) Survival o f selected pathogenic
bacteria in white pickled cheese made with Lactic Acid Bacteria o f Antimicrobials. Journal
o f Food Protection 56 (11) 972-976,

Alford, J.A. and Palumbo, S.A., (1969). Interaction o f salt, pH and temperature on the
growth and survival of salmonellae in ground pork. Applied Microbiology 17 528-532.

Aryanta, R.W., Fleet, G.H. and Buckle, K.A. (1991) The occurence and growth of
microorganisms during the fermentation o f fish sausage. International Journal o f Food
Microbiology 13 143-156.

Ashenafi, M. (1993) Fate of Salmonella enteritidis and Salmonella typhimurium during

fermentation of Ergo, a traditional Ethiopian sour milk. Ethiopian Medical Journal 31 91-98.

Ashenafi, M. (1994) Fate of Listeria monocytogenes during the souring o f Ergo, a

traditional Ethiopian fermented milk. Journal o f Dairy Science 77 696-702.

Barber, L.E. and Deibel, R.H. (1972). Effect o f pH and oxygen tension on staphylococcal
growth and enterotxin formation in fermented sausages. Applied Microbiology, 24 : 891-898.

Bonestroo, M.H., Kusters, B.M J., de Wit, J.C. and Rombouts, F,M, (1993) The fate of
spoilage and pathogenic bacteria in fermented sauce-based salads. Food Microbiology 10
101 111
- .

Buncic, S,, Paunovic, L. and Radisic, D, (1991) The fate of Listeria monocytogenes in
fermented sausages and vacuum packaged frankfurters. Journal o f Food Protection 54 (6)
413-417.

Campanini, M., Pedrazzoni, I., Barbuti, S. and Baldini, P. (1993) Behaviour o f Listeria
monocytogenes during the maturation of naturally and artificially contaminated $alami:effect
of lactic-acid bacteria starter cultures. International Journal o f Food Microbiology 20 169-
175.

Cieplinska, T. and Zychowicz, C. (1974) Effect o f Lactobacillus acidophilus on Salmonella

and Shigella organisms under laboratory conditions. Pediatrica Polonica 49 991-996.

Daly, C., Lachance, M., Sandine, W.E. and Elliker. P.R. (1973) Control of Staphylococcus
aureus in sausage by starter cultures and chemical acidulation. Journal o f Food Science 38
426-430.

DiGiancinto, J,V, and Frazier, W,C. (1966) Effect of coliform and proteus bacteria ion growth
o f Staphylococcus aureus. Applied Microbiology 14 124-129.
 78

El-Gazzar, 17A,, Bohncr, H.F. and Marth, E.H. (1993) Antagonism between Listeria
monocytogenes and Lactococci during fermentation o f products from Ultrafiltered skim Milk.
Journal o f Dairy Science 75 43-50.

Giraffe, G., Gatti, M. and Beltrame, A. (1994) Antimicrobial activity o f Lactic Acid Bacteria
isolated from fermented meat products. Ann. o f Microbiol Enzimol. 44 29-34.

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