1 s2.0 S0304401711004869 Main

Veterinary Parasitology 182 (2011) 7995
Contents lists available at ScienceDirect
Veterinary Parasitology
journal homepage: www.elsevier.com/locate/vetpar
The socioeconomic burden of parasitic zoonoses: Global trends

Paul R. Torgerson a, , Calum N.L. Macpherson b
a
b
Division of Epidemiology, Vetsuisse Faculty, University of Zurich, Zurich, Switzerland

St Georges University, St George, Grenada, West Indies
a r t i c l e
i n f o
Keywords:
Disease burden, Parasitic zoonoses,
Economics, DALY, Emerging diseases
a b s t r a c t
Diseases resulting from zoonotic transmission of parasites are common. Humans become
infected through food, water, soil and close contact with animals. Most parasitic zoonoses
are neglected diseases despite causing a considerable global burden of ill health in humans
and having a substantial nancial burden on livestock industries. This review aims to bring
together the current data available on global burden estimates of parasitic zoonoses and
indicate any changes in the trends of these diseases. There is a clear need of such information as interventions to control zoonoses are often in their animal hosts. The costs of
such interventions together with animal health issues will drive the cost effectiveness of
intervention strategies. What is apparent is that collectively, parasitic zoonoses probably
have a similar human disease burden to any one of the big three human infectious diseases:
malaria, tuberculosis or HIV in addition to animal health burden. Although the global burden for most parasitic zoonoses is not yet known, the major contributors to the global
burden of parasitic zoonoses are toxoplasmosis, food borne trematode infections, cysticercosis, echinococcosis, leishmaniosis and zoonotic schistosomosis. In addition, diarrhoea
resulting from zoonotic protozoa may have a signicant impact.
2011 Elsevier B.V. All rights reserved.
1. Introduction
Of the nearly 1500 agents known to be infectious to
humans, 66 are protozoa and 287 are helminths infectious
agents, 66 are protozoa and 287 are helminths (Chomel,
2008; Taylor et al., 2001). The majority (60.3%) of emerging infectious diseases are zoonoses (Jones et al., 2008).
Zoonoses represent a large burden of disease and there
are changing patterns of disease burdens with disease
emergence. Human population growth and socioeconomic
changes result in the migration of populations into new
ecological regions and changes in animal husbandry practices which can impact on disease emergence and disease
burden (Macpherson, 2005). In addition improved diagnostics are demonstrating that many zoonoses have a higher
burden then previously recognised. Some new syndromes
Corresponding author. Tel.: +41 44 635 90 41.

E-mail address: paul.torgerson@access.uzh.ch (P.R. Torgerson).
0304-4017/$ see front matter 2011 Elsevier B.V. All rights reserved.
doi:10.1016/j.vetpar.2011.07.017
are also being attributed to parasitic zoonoses and hence

add to the disease burden. Global warming may change the
transmission dynamics of parasitic zoonoses in endemic
areas and enable some parasites to transmit in regions
where they were previously absent.
2. Disease burden and its calculation
Disease burden is the impact of a disease on society
measured by nancial cost, mortality, morbidity, or other
indicators. Calculating the total burden in monetary terms
has the advantage that, with zoonoses, there may be substantial animal health losses and hence both the human
and animal health losses can be calculated in one gure.
For several diseases monetary costs have been dened and
these are given where available. Monetary costs include
loss of productivity in animals and treatment costs and
loss of income in individuals affected by the disease. However, the absolute cost of treatment and convalescence of
human patients is higher in high income countries than
80
P.R. Torgerson, C.N.L. Macpherson / Veterinary Parasitology 182 (2011) 7995
in low income countries due to variations in medical and

wage costs. Thus a disease in a wealthy country may have
a higher nancial burden than the same disease in a low
income country even if it has a much higher incidence
in the latter. These issues are discussed in greater detail
in Carabin et al. (2005). Consequently, the World Health
Organisations preferred measure is the Disability Adjusted
Life Year (DALY) and this was used to calculate the Global
Burden of Disease (GBD) estimates (Lopez et al., 2006). This
non-monetary measure avoids valuing human health differently in low and high income countries. It is a composite
measure which takes into account the number of life years
lost due to premature death (Years of Life Lost or YLLs) and
the number of healthy life years lost due to living with
a disability (Years Lived with Disability of YLDs). DALYs
are calculated by summing the YLLs and YLDs. Diseases
that result in a high mortality rate and/or high numbers of
chronically disabled individuals will result in greater numbers of DALYs than acute diseases from which the patient
generally makes a complete or almost complete recovery.
Therefore human disease burden using this metric depends
on both severity of the disease syndrome and the incidence. GBD has been reporting health information since
1990 (Stein et al., 2007). The GBD 1990 series (Murray and
Lopez, 1996) constructed an internally consistent global
overview of morbidity, disability, and mortality burden for
some 130 diseases and conditions. This has been updated
for 2001 (Lopez et al., 2006) and estimates are also available
for 2004 with projections for 2008, 2015 and 2030 (WHO,
2008). However in GBD most zoonotic parasitic diseases
were neither specically included in the initial estimate nor
in the updated series. The only parasitic diseases that have
signicant zoonotic transmission included were Leishmaniosis, Schistosomosis and Trypanosomosis (Chagas disease
and African Trypanosomosis). Other parasitic zoonoses disappear as distinct entities, but the burden is included in
other categories. For example, diarrhoeal diseases were calculated as a general category and some protozoan zoonoses
will make a substantial contribution to the global burden of
diarrhoeal disease. Since these publications of GBD, there
have been estimates of the global or regional burden of
some additional parasitic zoonoses. In addition a number of
parasitic zoonoses are emergent or re-emergent and they
present a substantial burden to the human population.
It has also been suggested that DALY calculations may
be inappropriate for calculating the burden of parasitic diseases (Payne et al., 2009) due to, inter alia, inappropriate or
single disability weights for parasitic diseases when a variety of syndromes are present, problems of poly-parasitism
or problems with missing data. Such issues are being or
have been addressed using a variety of techniques including varying the disability weights and adopting stochastic
techniques (see for example Budke et al., 2004; Fevre et al.,
2008).
Often the burden has been calculated in monetary terms
rather than using the GBD approach and such data is available when DALYs may not be. In addition many parasitic
zoonoses are neglected zoonoses so have not yet been considered by GBD. The problem of calculating human costs
in DALYs and animal health costs in monetary losses is a
signicant one with zoonoses that affect both human and
animal health. Monetarizing human health losses is one

possible solution. A DALY is considered the equivalent of a
loss of one year of healthy life and so the mean annual GDP
per head in the country where the DALY was calculated
may have some nancial equivalence. But as previously
discussed this would move away from one of the central
ideas of the DALY which is to value human life equally and
hence is unlikely to be accepted. Cost sharing between animal and human health sectors is an approach that has been
proposed (Zinnstag et al., 2007) but still required monetary calculation of human health costs. This review will
summarize the major trends in disease burden of parasitic zoonoses in both terms of monetary losses and DALYs
where available.
3. Trends in the burden of cestode zoonoses
3.1. Larval cestode zoonoses
3.1.1. Cystic echinococcosis
Cystic echinococcosis (CE) in humans is caused by the
larval stage of a number of taxonomically related species
of Echinococcus: E. granulosus, E. ortleppi, E. intermedius and
E. canadensis. These were, until recently, all considered to
be strains of one species (E. granulosus), but following a
taxonomic revision a number of species are now proposed
(Thompson, 2008). All of these Echinococcus genotypes
utilise canid, usually domestic dogs, as denitive hosts and
a variety of ungulates, particularly farm animals as intermediate hosts. Man is generally an aberrant intermediate
host in which the hydatid cyst develops, usually in the liver
or lungs as a space occupying lesion, which can result in
considerable morbidity (Eckert and Deplazes, 2004). As a
result of a number of studies undertaken in recent years the
societal burden of this disease is better known than many
other parasitic zoonoses and updates are being undertaken
in the GBD study.
A preliminary estimate of the annual global burden of
CE has suggested approximately 1 million DALYs are lost
due to this disease (Budke et al., 2006). This is likely to be
a substantial underestimate (Craig et al., 2007) (Table 1)
with perhaps 1 million or more individuals currently suffering from CE globally. The global burden of CE, in terms
of DALYs lost, suggests that CE may cause disability on at
least a similar level to numerous better-known Neglected
Tropical Diseases (NTD), including Chagas disease, dengue,
onchocercosis, and African trypanosomosis. In addition the
nancial burden of CE on the global livestock industry is
considerable with up to $2 billion lost annually.
In Iceland, New Zealand, southern Cyprus and Tasmania
the burden of CE is close to zero as a result of successful control or elimination programmes or due to high standards of
veterinary public health that limit transmission to humans.
These are islands which has facilitated elimination of the
parasite.
Some progress has also been made in Latin America to
reduce human incidence of CE (Craig and Larrieu, 2006).
Despite success in reducing this burden in some countries,
much of Latin America remains highly endemic with particular problems in, for example parts of Peru (Gavidia et al.,
2008). An economic assessment of the disease was under-
81
Table 1
Possible magnitude of the annual global burden of parasitic zoonoses with that of the global burden of malaria, tuberculosis and HIV for comparison.
Zoonosis
Important aetiologies
Possible Global
Burden (DALYs)*
Animal Health Costs
Trends
Zoonotic
Schistosomosis
Echinococcosis
Schistosoma japonicum
? 106 107
Unknown
Long term is decrease
Echinococcus
granulosus
E. multilocularis
Taenia solium
T. saginata
2-5 10
US$2 10
2-5 106
Very low
Toxoplasma gondii
2-8 106
Unknown
Substantial animal
health costs
Possibly substantial
Cysticercosis
Toxoplasmosis
Food borne trematodes Fasciola spp.

Opithorchis spp.
Clonorchis spp.
Paragonimus spp.
Giadia spp.
Zoonotic Intestinal
protozoa
Cryptosporidium spp.
Vector born zoonotic
Trypanosoma brucei
protozoa
rhodesiense T. cruzei
Leishmania spp.
Others
Toxocara spp. Other
nematodes
The big three global infectious diseases
Malaria
HIV
Tuberculosis
>0.5 106
Animal Fasciolosis is
very high
? 105 106
Unknown, but likely to

be high
>1 10
? 106
39 106
71 106
36 106
CE emergent in NIS, AE
emergent in Europe
New sequaelae are

being assigned to
toxoplasmosis
Increasing reports
Burden due to Chagas

disease is decreasing
Control programmes
for Trichinella are a
large nancial burden
Assumes new disability

weights
Assumes c 30% of epilepsy

in low income countries
due to neurocysticercosis
Congenital and non
congenital toxoplasmosis
see text
Estimated from GBD

gures (WHO, 2008)
Individually low human
disease burden but
collectively large
From the most current
GBDdata (WHO, 2008)
*
For most of these zoonoses, a global burden has yet to be published. The possible DALYs indicate a very crude estimate based on available data and serve
only to illustrate the likely magnitude of the disease burden.
taken in Uruguay (Torgerson et al., 2000) which suggested

annual losses, including both animal and human health
costs, of at least $2.9 million, and possibly as high as $22.1
million. However Uruguay is a country where control has
made some progress in reducing the burden of CE, so the
nancial burden is now likely to be reduced.
Generally in north America the human incidence is very
low and consequently so is the human disease burden
(Moro and Schantz, 2006). Sporadic cases of CE due to E.
canadensis are seen mainly in indigenous people in northern Canada or Alaska (Rausch, 2003).
Typically in central or Western Europe there is a tendency for decreasing numbers of autochthonous cases but
increasing numbers recorded in immigrants. This is typied by a recent report from Austria (Schneider et al.,
2010). There are important foci in southern Europe. In
Spain CE annual costs of approximately EURO 133 million
due human ill health and D 16 million to animal health
losses (Benner et al., 2010). In the Italian islands of Sicily
or Sardinia prevalences in sheep of 67% and 75% respectively and high human incidence rates of 2.3 and 6.6 per
100,000 per annum respectively have been recorded. On
the Italian mainland there are also focal hotspots of CE in
north, central and southern Italy (Garippa and Manfredi,
2009). In Greece a decline in the ultrasound prevalence
(the prevalence recorded by ultrasound scanning in a cross
sectional study of the population) in human patients now
being seen in some areas (Varbobitis et al., 2010), probably
attributable to a national control programme. In northern
Europe there is generally a low or negligible burden of
autochthonous CE.
The UK has an endemic focus, mainly in Wales and is

believed to result in economic losses of greater than $1 million per annum (Torgerson and Dowling, 2001). A control
campaign in Wales was abandoned in the 1990s and there
is some evidence that CE may be re-emerging in Wales
(Buishi et al., 2005).
In most countries of the former Soviet Union and Eastern
Europe there have been considerable increases in human
CE since the early 1990s with reported cases, and hence
burden, approximately four fold higher than during communist administration. This is due to the abandonment
of large collectivised farming systems and the neglect or
collapse of veterinary public health services (Todorov and
Boeva, 1999; Torgerson et al., 2006).
In many areas of the world there is a persistently high
burden of CE, which has become better documented in
recent years. In China CE affects large parts of the Tibetan
plateau and western regions of the country. In some districts of western Sichuan for example, perhaps 6% or more
of some rural populations have evidence of cysts through
ultrasound examination (Tiaoying et al., 2005). Similar proportions are also infected with alveolar echinococcosis (AE)
and over the population as a whole echinococcosis has a life
time burden of 0.81 DALYs per person (Budke et al., 2004)
making it amongst the leading causes of morbidity in these
regions. The other highly endemic region is Xingjiang and
there are also many cases reported from inner Mongolia
(Zhenghuan et al., 2008). It has been estimated that China
has approximately 40% of the global burden of CE (Budke
et al., 2006), with nearly 350,000 individuals living with the
disease (Craig et al., 2007).
82
Elsewhere in Asia there are large numbers of CE cases

in parts of Russia, most of central Asia, Iran and Turkey.
CE is also common in the Middle East and North Africa.
The annual incidences vary between 1 and 27 cases per
100,000 with most being in the 510 cases per 100,000
ranges. Estimates of close to half a million people across
this endemic area living with CE have been made (Craig
et al., 2007). Economic evaluations have been undertaken
in Tunisia (Majorowski et al., 2005) and Jordan (Torgerson
et al., 2001) which indicate that echinococcosis represents
a substantial economic effect in relation to the respective
countries GDP perhaps up to 0.5% of total economic activity for these countries. In Turkey production losses due
to CE in livestock have been estimated at $89 million per
annum (Sariozkan and Yalcin, 2009).
In sub-Saharan Africa a notable endemic area is the
Turkana region in northern Kenya. Here incidences are
amongst the highest in the world (Magambo et al., 2006).
In northern Ethiopia a recent study suggested that 22%
of cattle have hydatid cysts resulting in the equivalent of
US$1.56 loss per animal due to condemnation and production losses (Kebede et al., 2009b). A similar study suggested
that the prevalence in some regions approaches 50% with
the direct and indirect losses of $21 per infected animal
(Kebede et al., 2009a). Elsewhere in Ethiopia prevalences
in cattle and sheep of 47% and 29% respectively have been
reported (Getaw et al., 2010).
3.1.2. Alveolar echinococcosis
Human alveolar echinococcosis (AE) is caused by the
larval stage of the fox tapeworm Echinococcus multilocularis and is distributed through much of the northern
hemisphere. The global burden of AE has recently been estimated at over 600,000 DALYs per annum (Torgerson et al.,
2010). This is comparable to several of the diseases in the
neglected tropical disease cluster (trypanosomosis, Chagas
disease, schistosomosis, leishmaniosis, lymphatic lariasis, onchocercosis, intesinal nematode infections, Japanese
encephalitis, dengue, and leprosy) (Mathers et al., 2007)
Over 90% of the global burden of AE is in China on
the Tibetan Plateau. In certain communities there may
be as many as 510% of the population infected by AE
and the annual incidence of new cases possibly exceeded
16,000 in this region (Torgerson et al., 2010). Dogs have a
high prevalence of infection with E. multilocularis (Budke
et al., 2005) and are likely to be the important source of
infection for humans. Landscape change, often associated
with overgrazing, appears to have altered the small mammalian fauna on the Tibetan plateau and hence promoting
transmission in both the fox-small mammal cycle and the
anthropomorphic cycle involving dogs (Wang et al., 2004,
2006a).
Elsewhere in Asia there are important foci in Turkey
and sporadic cases in Iraq, Iran, Afghanistan and India
(Torgerson et al., 2010). On the Japanese island of Hokkaido
there are perhaps 10 or so human cases per year (Ito et al.,
2003).
In the former Soviet Union and Eastern European there
may be over 1000 cases per year (Torgerson et al., 2010).
In Kazakhstan and Kyrgyzstan there have been high prevalences of infection recorded in dogs (Stefanic et al., 2004;
Ziadinov et al., 2008) and a very high intensity of infection

in foxes (Ziadinov et al., 2010), but there has not yet been
a major epidemic in humans (Torgerson et al., 2009). However as there are clearly high levels of transmission of CE
resulting from dog contact in these countries, it is possible
that increased reports of AE may occur in the future
In Europe increasing fox populations have been associated with an increase in AE incidence in Switzerland
(Schweiger et al., 2007). However, the actual burden of
disease due to AE has almost certainly been reduced due
to better case management and hence improved prognosis
in recent years (Torgerson et al., 2008). The UK presently
appears to be free of E. multilocularis although there is
believed to be a high probability of introduction through
infected dogs if the requirement for praziquantel treatment
of dogs prior to UK importation is abandoned which may
occur as a consequence of EU regulations (Torgerson and
Craig, 2009). Introduction to new areas is always a major
concern and this is demonstrated by the recent detection of
two infected foxes in Sweden, a country previously thought
to free of E. multilocularis (Osterman et al., 2011)
In North America human AE is very rarely seen, despite
the parasite being endemic over large parts of the mid
western USA, Canada and Alaska. In some isolated Native
American communities in Alaska substantial numbers of
cases have been recorded in the past, possibly associated
with dog infections and an anthropomorphic cycle. These
outbreaks have now been controlled by successful intervention (Rausch et al., 1990; Schantz et al., 1991).
3.1.3. Other forms of echinococcosis
Echinococcus oligarthrus and E. vogeli are conned to
the New World. Either species is capable of causing
echinococcosis in humans (often referred to as neotropical echinococcosis). Disease due to E. vogeli is similar to
AE and is characterized by aggressive inltrative growth
and external budding, whereas infection with E. oligarthrus
has a more benign course. Compared to other Echinococcus
species, human echinococcosis caused by these two species
is relatively rare. Up to March 2007 a total of 172 cases of
human neotropical echinococcosis had been documented
(DAlessandro and Rausch, 2008). However there is some
evidence that this incidence may be increasing albeit from
a low base (Tappe et al., 2008).
3.1.4. Cysticercosis
Taenia solium has a global distribution but is rare or
absent in high income countries and in countries where
pork is not consumed. The main endemic regions include
Latin America, China, South East Asia and sub-Saharan
Africa. Presently the global burden of cysticercosis is
unknown, but some local studies have been completed.
In west Cameroon epilepsy associated with neurocysticercosis is believed to result in approximately 45,800 DALYs
or 9 per 1000 persons with a possible economic burden
amongst the same population of over D 16 million (Praet
et al., 2009). In the eastern cape of South Africa the annual
monetary burden of cysticercosis has been estimated at
between US$18.6 million and US $34.2 million (Carabin
et al., 2006). Perhaps a good indication that the global
burden of cysticercosis is likely to be considerable comes
from the results of a systematic review on the association of epilepsy and neurocysticercosis (Ndimubanzi et al.,
2010). This study suggests that in low or middle income
endemic countries approximately 30% of epilepsy may be
attributable to neurocysticercosis. The global burden of
epilepsy estimated is to be 7.8 million DALYS. Of these,
6.5 million DALYs occur in Sub Saharan Africa, Latin America, South Asia and the Western Pacic (including China):
regions where T. solium is highly endemic. It is also interesting to note that the proportion of the total burden of
disease caused by epilepsy in the Middle East and North
Africa, middle income countries where pork consumption
is very low, is 0.378%: comparable to that of high income
countries (0.314%) where T. solium has largely been eliminated. In Latin America, middle income countries but with
high pork consumption, the proportion of the total disease
burden attributable to epilepsy is 0.707% (calculations from
data in (Lopez et al., 2006). Thus an estimate of over 2 million DALYs per annum (Table 1) would not be unreasonable,
although the actual global burden is still unknown.
The future trends on the burden of T. solium cysticercosis will depend on patterns of pork consumption, the
success of veterinary public health interventions and economic growth. Pork consumption is increasing in countries
such as China (Ortega et al., 2009), but rapid economic
development should also promote veterinary public health
programmes to control this parasite. Human cysticercosis,
dracunculiasis and lymphatic lariasis are the only human
parasitic diseases that have the potential to be eradicated
globally (Molyneux et al., 2004). Therefore with effective
investment in veterinary public health it may be possible
to eventually reduce the global burden of cysticercosis to
zero, although in some regions (such as sub-Saharan Africa)
cysticercosis will remain problematic for the foreseeable
future.
3.1.5. Other larval cestodoses
Human coenurosis caused by the larvae of Taenia multiceps, T. serialis or T. brauni are sporadically recorded in
the literature. CNS infection can be devastating and hence
result in a high disability weight. As reports of such infections are rare, the global burden of human coenurosis is
likely to be very low.
83
as many parts of Africa, prevalences are typically greater

than 20% (Abunna et al., 2007; Opara et al., 2006).
3.2.2. Diphyllobothriosis
Diphyllobothrium latum has a circum polar distribution
in northern temperate and sub arctic countries. The parasite infects an estimated 9 to 20 million people (Lloyd,
2011). Infections have also been described in some South
American countries and sporadically elsewhere. Many
human infections are asymptomatic, but abdominal pain,
dizziness, fatigue, transient diarrhoea, dyspepsia, and vomiting may occur. Classically, pernicious anaemia may occur
due to uptake of vitamin B12 by D. latum and the dissociation of B12 and intrinsic factor. Improved sanitation and
treatment of efuents to remove eggs are being achieved at
many rivers and lakes and this may help to decrease prevalence. D. latum tapeworms also infect piscivorous domestic
(dog and cat) and wild life (bear, fox) reservoir hosts. The
increasing popularity of eating raw or undercooked sh
may lead to an increase in human dyphyllobothrioisis. The
burden of diphyllobothriosis is likely to be low despite
many human infections as the disability weight would generally be close to zero except in the small numbers of cases
that may suffer from anaemia.
3.2.3. Other adult cestodoses
Hymenolepis spp. are fairly commonly found in humans
with perhaps over 50 million global infections for H. nana.
H. nana can establish in humans without an intermediate host or can be transferred from rodents. For other
Hymenolepis spp. an intermediate host is obligatory. Generally human Hymenolepis infections are asymptomatic, but
heavy infections can result in abdominal pain, diarrhoea,
poor weight gain, eosinophilia, nausea, vomiting and uticaria. Other adult cestodes include Dypiledium caninum,
Bertiella spp., Mesocestoides spp. and Raillietina spp. have
been occasionally recorded in humans. As these infections
are rare and intestinal cestode infections are generally of
low pathogenicity, the socioeconomic burden is likely to
be very low
4. Trends in the burden of trematode zoonoses
4.1. Food-borne trematode zoonoses
3.2. Adult cestode zoonoses

3.2.1. Taeniosis
Human infection with adult Taenia occurs through
ingestion of undercooked pork or beef. When man is the
denitive host of these parasites, the clinical signs are moderate and hence the burden will be negligible in terms
of DALYs (although individuals infected with intestinal T.
solium are at high risk of being affected by cysticercosis
with the attendant health effects). There are considerable
economic effects as pork and beef containing cysticerci are
condemned to prevent human infection. Even when infections rates in animals are very low, the economic impact
can still be signicant. In Iran where about 0.02% of cattle
carcasses are condemned due to T. saginata cysticercosis,
the annual economic losses are in the order of $400,000
(Jahed Khaniki et al., 2010). In highly endemic areas, such
There are more than 80 species of food-borne trematodes of which Fasciola spp., Clonorchis sinensis, Opisthorchis
spp., Fasciolopsis buski, Paragonimus spp., and to a lesser
extent Heterophyes spp. and Metagonimus spp. are of public
health importance. Of the estimated one billion people at
risk of infection (Keiser and Utzinger, 2005) up to nine million may suffer from symptomatic sequelae and between
10,000 to 11,000 people die each year (WHO, 1998b). Thus
an annual global burden of over 500,000 DALYs would
not be an unreasonable expectation (Table 1) although
more precise estimates are presently unavailable The foodborne trematode zoonoses are transmitted by ingestion
of metacercariae and are perpetuated through inadequate
sanitation, cultural and evolving food habits, growth of
aquaculture and by a wide range of domestic and wild
denitive hosts. The DALYs contributed by the food-borne
84
trematodes have yet to be calculated but taken as a whole

are likely to be substantial and their importance is increasingly being recognized.
4.1.1. Fasciolosis
Fasciolosis is an important disease of livestock and
humans caused by species of the genus Fasciola. Fasciola hepatica is responsible for the disease in temperate
climates whereas F. gigantica is found in tropical areas. Fasciola spp. is a true zoonosis being predominantly a parasite
maintained by infected sheep and cattle that can be transmitted to humans. Humans may also maintain infection
as denitive hosts (Esteban et al., 1999). Other domestic animals, such as pigs, goats, dogs, alpacas, llamas and
also rats can serve as denitive hosts. The snail Galba truncatula (formerly Lymnaea truncatula) is a well recognized
intermediate host although other snail species may be
important locally. Transmission to the denitive host is by
the ingestion of metacercaria, either food-borne through
ingesting raw contaminated aquatic plants or water-borne
by drinking contaminated water (Esteban et al., 2002).
Risk factors associated with infection include age with
most infections in children. There is also a correlation
between human and animal prevalence in the same region
(Parkinson et al., 2007).
An estimated 2.4 million people in over 61 countries
are infected annually with Fasciola spp. with 180 million
at risk of infection (Haseeb et al., 2002; Mas-Coma et al.,
1998). Fasciola spp. endemicity is highest in Bolivia, Peru,
Cuba, Iran, and Egypt with signicant prevalence occurring
in Asia, Africa and a number of European countries. The true
extent of fasciolosis is unknown with large epidemiological
studies having only been carried out in Egypt (Curtale et al.,
2005) and Bolivia (Esteban et al., 2002; Parkinson et al.,
2007).
Fasciolosis is rarely fatal in humans and the major
pathology results from hemorrhaging and inammation of
the liver caused by trapped or migrating ukes (Aksoy et al.,
2005). The extent of this pathology is dependent upon the
number of ukes that invade the liver. Flukes that reach the
bile ducts cause signicant pathology through the thickening and dilation of the bile ducts and gallbladder. Blood
loss, particularly in the acute phase of infection, results in
anaemia. Similar clinical manifestations occur in animals.
Fasciolosis also impacts a major burden on the livestock
industries with substantial effects on productivity. Many
endemic countries have high livestock prevalences often
with more than 50% of animals infected (Torgerson and
Claxton, 1999). In Switzerland, which has a population of
1.6 million cattle the annual economic losses have been
estimated at D 52 million (Schweizer et al., 2005) based on
a mean prevalence of bovine fasciolosis of 10.9%.
4.1.2. Fish-borne trematodes
A large number of different trematode genera and
species result in millions of sh-borne human infections
annually (reviewed by Lloyd and Soulsby, 2011). Many
of these zoonotic trematode infections occur in Asia but
some are more widespread. Humans may be important or
occasional denitive host acquiring infection from eating
raw/undercooked sh. Adult sh-borne trematodes occur
in the biliary system or intestine: occasionally ectopic

sides are also reported. The global burden of sh borne
trematodes is presently being estimated and is likely to
be considerable due to high human incidences and severe
morbidity and high fatalities resulting from chronic sequelae.
Clonorchis sinensis, Opisthorchis viverrini and O. felineus
are parasites of sh-eating mammals, particularly in Asia
and Europe where more than 20 million people are
infected. In highly endemic areas, such as north-east
Thailand, the prevalence of O. viverrini may reach up to 90%
(Brockelman et al., 1987).
Clonorchis sinensis is prevalent in China, Taipei, Vietnam, Japan and Korea. The main animal hosts are cats, dogs,
pigs, camels and rats. Most light infections, including light
chronic infections (the ukes can live for up to 15 years), are
usually asymptomatic but moderately infected individuals
may experience fever, fatigue, rash and gastrointestinal complaints. These symptoms may be exacerbated in
patients with heavy (patients passing > 10,000 eggs per
gram of faeces) and long standing heavy infections. Such
patients can also experience cholestasis, recurrent pyogenic cholangitis, cholecystitis, biliary and liver abscess,
biliary and liver cirrhosis, pancreatitis, and hepatitis.
The most severe consequence is cholangiocarcinoma. The
mechanism of carcinogenesis remains arcane but irritation
caused by the uke plays a crucial role. The International
Agency for Research on Cancer upgraded C. sinensis from
a probable carcinogen (group 2A) to a denite carcinogen (group 1) (Bouvard et al., 2009). Patients developing
cholangiocarcinoma have a poor prognoses and most die
within a year of diagnosis even when sophisticated treatment is applied (Yalcin, 2004)
Opisthorchis felineus is prevalent in Poland, eastern
Germany and in parts of the former USSR. The adult ukes
live in the bile ducts and can occur in large numbers.
Infection occurs through eating sh and the metacercariae
reach the liver by direct migration up the bile duct. Clinical manifestations are rare, but infection increases the
risk of cholangiocarcinoma (Haswell-Elkins et al., 1994). O.
viverrini is categorized as a denite carcinogen (group 1)
whereas O. felineus is not (Bouvard et al., 2009).
Heterophyes heterophyes and Metagonimus yokogawai
are probably the two most important of numerous different species of small (usually <2.5 mm), zoonotic intestinal
ukes found in mammals and birds which ingest sh. These
ukes commonly occur in Japan, Laos, Thailand, the Republic of Korea, Hawaii, the Balkans, the Philippines, China,
Taipei, Turkey and Siberia. Clinical manifestations are rare
and, if present, are usually due to eggs trapped in various
tissues.
Echinostoma ilocanum, E. revolutum, E. malayanum, E.
echinatum and E. hortense are of minor zoonotic importance but a high prevalence has been reported in endemic
countries, such as the Republic of Korea, the Philippines,
Indonesia, Malaysia and Thailand. Heavy infections may
result in diarrhoea, anorexia and abdominal discomfort.
Control of all sh-borne trematode zoonoses is similar and
can be achieved through treatment with praziquantel, sanitation measures and education to discourage consumption
of raw sh.
Paragonimosis is an important food-borne trematode

zoonosis due infection by numerous species of lungdwelling ukes. Over 20 million people are infected
world-wide through eating raw or undercooked crabs,
craysh or shrimp. Infection may also occur when paratenic
hosts, such as wild boar are consumed. Paragonimus westermani, is the main species in the Far East, P. miyazakii,
P. skryjabini and P. heterotrema in Asia, P. africanus and P.
uterobilateralis in Africa and P. mexicanus and other species
occur in Latin America. Countries with signicant numbers of cases include China, Taipei China, Thailand, Japan,
Nigeria, Cameroon, Peru and Ecuador. Numerous species of
mammals may act as denitive hosts, including dogs, cats
and wild carnivores. Pulmonary infection is characterised
by a chronic productive cough and chest pain. Neurological
infections have been reported from the Far East, especially
the Republic of Korea. CT scans are useful for disclosing
brain lesions.
4.2. Schistosomosis
Of the 18 Schistosoma spp., ve infect humans and
three, S. japonicum, S. mansoni and S, mekongi are zoonotic.
The importance of the animal denitive hosts, baboons
(Legesse and Erko, 2004) and rodents (Duplantier and Sene,
2000) in Africa for S. mansoni and pigs in Laos and Cambodia
for S. mekongi (Strandgaard et al., 2001) is unclear. S. japonicum has a wide range of denitive hosts. Studies in the
marshlands and lake region of the Yanze river basin, where
the majority of human cases of S. japonicum in China occur,
demonstrated that water buffaloes and cattle contributed
signicantly more to human infection than other domestic
animals, such as dogs, cats, pigs, sheep and goats (Wang
et al., 2006b). In contrast rodents and dogs have been suggested as the most important reservoir hosts in some of
the hilly/mountainous regions of China, where bovines are
scarce and human infections are not as common (McManus
et al., 2010; Rudge et al., 2009). In the Philippines dogs
are thought to be important denitive hosts (Rudge et al.,
2008).
Worldwide an estimated 207 million people are
infected with schistosomosis (Steinmann et al., 2006). An
initial DALY estimate for schistosomosis of 1.74.5 million
has been recently reassessed. Most zoonotic cases of schistosomosis are due to S. japonicum. New disability weights
given to S. japonicum (Finkelstein et al., 2008) and update
information on global prevalence (van der Werf et al., 2003)
have been used. These studies indicate that the true burden of human schistosomosis is substantially higher and is
currently estimated to be approximately 70 million DALYs
annually (Hotez and Fenwick, 2009; King and DangereldCha, 2008). This burden estimate exceeds that for malaria
or TB and almost equates to the DALYs lost from HIV/AIDS.
The DALYs contributed by the zoonotic schistosomes will
be less. But even if only 14% of global schistosomosis is
zoonotic in origin, it would push the global burden of
zoonotic schistosomosis to over 10 million DALYs annually (Table 1). S. japonicum additionally debilitates infected
domestic livestock which are used for food and as work
animals. Economic losses for infections in livestock have
been seldom studied and hence are less dened but add
85
signicantly to the economic burden and suffering of communities. It is known that S. bovis (a non zoonotic species)
can result in substantial economic losses in livestock (Hunt
McCauley et al., 1984) and hence, by analogy, direct production losses due to S. japonicum are likely.
Schistosomosis is strongly linked with poverty, and
despite recent improvements in the rural Chinese economy, which have resulted in a better standard of living,
the prevalence of S. japonicum and its associated morbidity have continued to rise in some localities. The downturn
in the global economy in 2007 resulted in the closure of
businesses in urban areas, employment opportunities contracted and millions of city residents returned to their
former rural villages: some of which were located in S.
japonicum endemic areas (McManus et al., 2010).
S. japonicum currently is an important zoonosis in ve
provinces in China where more than 50 million people
are at risk and approximately one million people and several hundred thousand livestock are infected (McManus
et al., 2010). S. japonicum also occurs in 28 provinces in the
Philippines and in discrete foci in the province of central
Sulawesi in Indonesia (King, 2009).
Water resource development, including irrigation and
the construction of dams for water conservation, hydroelectric power generation etc. in schistosomosis endemic
areas, such as the Gezira-Managil dam in Sudan, the Aswan
dam in Egypt, the Melkasadi dam in Ethiopia, the Kariba
dam in Zimbabwe and the Danling and Huangshi dams
in China have resulted in an increase in prevalence or
reemergence of the disease in those countries (Gryseels
et al., 2006; Steinmann et al., 2006). The recently completed
Three Gorges dam in China which has endemic S. japonicum foci above and below the dam is anticipated to have
an impact on the parasite increasing its current distribution
and intensity (McManus et al., 2010). As with other water
development projects it is anticipated that this will occur
through habitat alteration favoring increased snail breeding sites, increased grazing areas for important reservoir
hosts, occupational factors and an increase in the susceptible human population attracted to migrate to the endemic
areas from non-endemic regions of the country. Availability and use of latrines inuences the importance of humans
in contaminating the environment and their importance
vis a vis domestic and wild denitive hosts in maintaining
transmission.
S. japonicum was successfully eliminated from Japan
through snail control and socioeconomic changes. The
national schistosomosis control program in China is recognized as one of the most successful globally: the
cornerstone of the programme being mass chemotherapy.
Spatial epidemiological methods using geographical information systems (GIS), remote sensing (RS), incorporated
with advanced Bayesian based spatial statistics have been
important tools for identifying high-risk areas for S. japonicum transmission for Chinas control programme (Yang
et al., 2005). However, recent control successes appear
to be stalling. Together with the potential for its reemergence S. japonicum is regarded by the Chinese authorities
as being on par with HIV/AIDS, TB and hepatitis B as a
public health problem (Wang et al., 2008). A recent trial
carried out in two villages where in one all humans and
86
water buffaloes were treated with praziquantel and the

other village where only humans were treated showed
that chemotherapy given to water buffalo reduced human
incidence. Mathematical models supported this conclusion and predicted that water buffaloes were responsible
for an aetiological fraction of 75% of human Schistosomosis in this setting (Williams et al., 2002). Thus an
integrated approach to control needs to be implemented,
supported strongly by mathematical models. It has been
proposed that such integrated control will incorporate the
use of human and bovine chemotherapy, anti-infection and
anti-fecundity DNA vaccine constructs for water buffaloes
(still under development), health education/promotion,
improved sanitation and focal use of molluskicides (Wang
et al., 2009). Control of zoonotic Schistosoma species provides a serious challenge but successes already achieved
show that it can be achieved.
5. Trends in the burden of nematode zoonoses
5.1. Ascaroses
5.1.1. Toxocarosis
Toxocarosis due to the zoonotic helminth, Toxocara
canis, can present as a number of syndromes including
covert toxocariasis, neurological toxocarosis, visceral lava
migrans (VLM) and ocular larva migrans (OLM). The parasite has a global distribution and human infection is
acquired by the ingestion of embryonated eggs of T. canis
passed by dogs (puppies in particular) and foxes and also
probably to a lesser extent by the ingestion of T. cati eggs
passed by cats. Other species potentially zoonotic include
Toxocara vitulorum and Toxocara pteropodis.
Humans are accidental or paratenic hosts, in which L2
larvae maturation is inhibited and clinical syndromes are
thought to be related to infection dose and frequency and
to the migratory habits of the L2 larvae. Most cases of Toxocara infection are asymptomatic but some result in a variety
of syndromes mediated mainly through a generalized antibody and inammatory response. VLM a syndrome which is
primarily diagnosed in young children, may last for weeks
or months and exhibits as inammation of internal organs
and sometimes the central nervous system. Patients can
present with fever, cough, asthma, abdominal pain, nausea,
fatigue, weight loss, anorexia, headache, rash, and vomiting. In rare cases, epilepsy, pleural effusion, respiratory
failure, and death have been reported. OLM is rare compared with VLM, is usually unilocular and is caused by
the migration of a single larva in the orbit. A gradual and
permanent visual impairment occurs over days or weeks
depending on the location of the larvae, the eosinophilic
and later the brotic granulomatous response: blindness
occurs in many cases. Covert toxocarosis is characterised
by chronic coughing, fever, abdominal pain, headaches
and changes in behavior. Covert toxocarosis, has also been
associated with asthma and may be linked to the rise in
asthma observed in inner city children in the US (Busse
and Mitchell, 2007), as well as impaired cognitive development (Stewart et al., 2005). Neurotoxocarosis is rare with
patients presenting with seizures, headaches and other
neurological symptoms.
Seroprevalence rates have been examined in a few

countries and vary from 2% to 14% in industrialised nations
with high risk groups having much higher prevalence, to
over 80% in the tropics (Smith and Noordin, 2006). Children
are most at risk in all parts of the world but increasingly adults are being diagnosed in greater number as a
result of meat-borne infection. In the US a recent national
seroprevalence and risk factor study involving more than
30,000 people demonstrated a prevalence of 13%. Infection was associated with the level of education of the head
of household, with poverty, ethnicity and dog ownership
(Won et al., 2008).
The costs associated with diagnosis, which is problematic, and treatment for this zoonosis are considerable. Given
the widespread distribution and high frequency of this
mainly childhood zoonosis, where in the US, for example,
between 1.3 and 2.8 million people are infected (Hotez,
2008) toxocarosis poses an important burden on society and at the individual level. Toxocarosis along with
other helminths, strongyloidiosis, ascariasis, and cysticercosis are regarded as one of the neglected diseases of
poverty in the US as the infection disproportionately affect
impoverished populations (Hotez, 2008). The DALY contribution is likely to be fairly high but the lack of data,
particularly source attribution data of the often vague
non specic symptoms makes the importance difcult to
quantify. The monetary and non-monetary methods by
which the burden of toxocarosis and hence the benets of control have been discussed (Torgerson and Budke,
2006).
5.1.2. Anisakiosis
Anisakiosis is a food-borne nematode zoonosis resulting
from ingesting the L3 larval stage of Anisakis simplex, A. physeteris and Pseudoteranova decipiens in marine sh, squid
or eels which serve as the second intermediate hosts. Clinical anisakiosis may be acute or chronic developing after
the penetration of the larvae into the mucosal wall of the
alimentary tract. The affected sites undergo erosion, ulceration, swelling, inammation, and granuloma formation
around the larvae. Patients present with acute abdominal pain, indigestion, nausea, vomiting, and occasionally
with allergic hypersensitive reactions. Such reactions vary
from isolated angioedema to urticaria and life threatening
anaphylactic shock. Generalized symptoms can be divided
into gastric anisakiosis, which may resemble peptic ulcer or
gastric cancer, or intestinal anisakiosis resembling appendicitis or peritonitis.
Anisakiosis, rst described in the 1960s has become
more frequently reported especially in eastern Asia (mostly
Japan) and Western Europe where large quantities of raw
marine sh are consumed (Chai et al., 2005). Improved
diagnostic tests increasingly demonstrate that this is a
worldwide zoonosis and today approximately 2000 new
cases are reported annually (Chai et al., 2005). Because of
the sometimes severe symptoms, chronic nature of some
infections and potential fatal cases, the disease burden
could be signicant. However, the difculties of making a
diagnosis make it a challenge to accurately assess this burden as the non specic clinical signs could be attributable
to other diseases.
5.1.3. Other ascarid species

Toxascaris (dogs, cats), Ascaris sum (pigs), Lagochilascaris
(opossums), Porrocaecum (birds of prey), Ophidascaris, Polydelphis, Travassoascaris (snakes), etc., can infect humans,
but any role is probably limited through short migratory
times or lack of human contact with eggs. Baylisascaris
procyonis (raccoons) L2 larvae migrate aggressively, pathology is severe and although rare this species is frequently
fatal increasing its zoonotic importance (Lloyd and Morgan,
2011). The incidence of this disease is extremely low, so
consequently the burden of disease will also be low.
5.2. Trichinellosis
Trichinellosis is a global helminth zoonosis, which
occurs when culturally distinct food habits include the
consumption of raw or improperly cooked meat or meat
products. Meat from pigs is the commonest source of
human infection; occasionally horses, fed pork products are
involved, and meat from a wide range of wildlife species.
Trichinella spp. consist of two clades: encapsulated and non
encapsulated (Pozio and Darwin Murrell, 2006). The encapsulated clade comprises ve species and four genotypes
whilst the non-encapsulated clade comprises one species
infecting mammals and birds, and two species infecting mammals and reptiles. T. spiralis is the only species
that normally occurs in domestic animals whilst all the
other species are primarily parasites of wildlife and. have
been reported from approximately 150 animal species.
Trichinella species can be transmitted either from the sylvatic environment to the domestic one or from domestic
animals to wildlife.
Human cases of trichinellosis have been documented
in 55 countries. The incidence of clinical trichinellosis is
unknown but it has been estimated that approximately
10,000 cases occur annually with 0.2% of these cases being
fatal (Pozio, 2011). The acute nature of the disease and
small numbers of fatalities will result in a low global burden of disease. The low incidence is due in part to good
pig farming practices legislatively enforced in most developed and some developing countries. The risk of outbreaks,
however, remains.
5.3. Strongyloidosis
Strongylodiosis, caused by Strongyloides stercoralis, is
a soil-transmitted helminth infection where humans, primates and dogs serve as denitive hosts. The parasite is
found in tropical and some temperate areas of the world
where poor sanitation and low socioeconomic conditions
prevail. S. stercoralis is unique amongst zoonotic nematodes, in that larvae passed in faeces can give rise to
free-living generations of adults and subsequently more
infective larvae. The parasite is also able to replicate within
the host (autoinfection) as the female is viviparous and thus
infections can persist for many decades. Human infection is
usually asymptomatic but clinical cases are associated with
chronic enteritis, eosinophilia, malabsorption syndrome
and impaired child development. Hyperinfection can occur
in some patients and an association with those who have
HTLV-1 infection or who are on corticosteroids has been
87
demonstrated giving rise to a syndrome, known as disseminated strongyloidosis. Such infections are nearly always
fatal.
The degree to which zoonotic transmission occurs is
uncertain though primate and dog- parasite clades have
been described (Hasegawa et al., 2010). Further studies are
required to elucidate the importance of dogs and humans
in perpetuating transmission.
Strongyloidosis occurs all over the tropics and subtropics and in found in varying prevalences in both
developed and industrialized countries. Difculties in diagnosis and the variability of prevalence within a country
coupled to the parasites longevity in infected hosts has
resulted in estimates on the numbers infected globally from
as low as 3 million to over 100 million (Nolan et al., 2011).
S. stercoralis is recognised as a neglected disease of poverty
in the US where 68,000 to 110,000 individuals are infected
(Hotez, 2008).
The burden from this parasitic disease is uncertain
but may be considerable, particularly since impaired child
development will result in considerable numbers of YLDs
associated with infection. The proportion of this burden
that is from animal sources is likewise uncertain.
5.4. Angiostrongylosis
Angiostrongylus cantonensis is an emerging zoonosis
with the rst human cases being reported in 1945 and
thereafter cases were only sporadically reported essentially until the 1990s. In the last few decades human cases
have been reported from endemic areas including a number of Pacic island nations and Asia (Thailand, Taiwan,
China, Vietnam, Malaysia, Cambodia) to more recently
described foci in the US, Caribbean, Japan, Indonesia, New
Zealand and Australia. Worldwide more than 2800 cases of
human angiostrongylosis have been reported from over 30
countries (Wang and Lun, 2011).
Human infection results from eating infected raw or
undercooked land or aquatic snails (the primary intermediate host species), slugs or paratenic hosts such as prawns
and land crabs, predacious land planarians, freshwater
sh, frogs, toads or monitor lizards and in endemic areas
from unwashed contaminated vegetables. The geographical expansion of the parasites range has been facilitated
by the unintended introduction of infected denitive hosts
such as numerous species of rats. Establishment of the parasite has also been facilitated by the intended or accidental
introduction of snail intermediate host species.
Clinically humans present with a range of symptoms
from mild to eosinophilic meningitis and in extreme cases
such infections have been fatal. The average patient is ill for
two weeks but the condition can last for months. Although
the DALYs for this zoonosis is currently low it is increasing
as the parasite spreads geographically.
5.5. Dirolariosis
A number of species of Dirolaria (including D. immitis,
D. repens, D. roemeri, D. tenuis, D. ursi, D. striata, D. subdermata, D. magnilarvatum and D. corynodes) have been known
to infect humans who do not serve as denitive hosts. The
88
lariae are transmitted by a range of mosquito (Culex, Aedes

and Anopheles spp) or Simulium spp. (in the case of D. ursi)
vectors. Human infection is rare and most infections are
asymptomatic. The majority of cases of human dirolariosis in the US and Japan involve the lungs, whereas in
Europe, the majority of cases are subcutaneous or ocular
in distribution (Simon et al., 2009). D. immitis worms cause
vasculitis and granuloma formation, coin like lesions,
in the lungs and most infections are diagnosed incidentally during examinations for other reasons. The burden
from dirolariosis is due to the costs of making a differential diagnosis, usually using imaging techniques but also
DNA techniques on biopsies. The parasites contribution to
DALYs is thought to be insignicant.
5.6. Hookworms
The zoonotic hookworms which are linked to human
disease are the common hookworm species of dogs, including Ancylostoma caninum, A. braziliense and A. ceylanicum
with the latter two species also commonly found in cats.
Geographically A. caninum is a common parasite found
throughout the tropics and sub-tropics, A. braziliense is
found on the eastern and Gulf coast of the US through the
Caribbean south to Brazil and also in Malaysia, Thailand
and Indonesia. A. ceylanicum is found in India and Southeast Asia. The importance of using morphological and
genetic markers in identifying hookworm species has been
stressed and such studies will further elucidate the global
distribution of the parasite species (Traub et al., 2007).
All zoonotic hookworms infect humans through skin
penetration and result in different clinical manifestations.
A. braziliense L3 are responsible for serpentine cutaneous
eruptions known as cutaneous larva migrans (CLM). A. ceylanicum is the only zoonotic hookworm where the adults
can reach maturity and patency in humans, albeit for short
periods of time (Bowman, 2011). Infection is transitory
and may manifest as abdominal pain. A. caninum infections have been reported to cause eosinophilic enteritis
in a number of patients in north-eastern Australia (Croese
et al., 1994). Diagnosis is difcult and is made from clinical symptoms, positive serology and indirectly through the
patients rapid recovery following treatment with mebendazole. Unlike their anthropomorphic cousins the zoonotic
hookworm species are of minor importance and contribute
insignicantly to DALYs due to parasitic zoonoses.
5.7. Capillariosis
Of the more than 200 species of Capillaria only three
are zoonotic, including C. philippinensis, C. hepatica and
C. aerophila. Only a few cases of the latter two species
have been reported in humans but C. philippinensis is a
fairly widespread zoonosis having been reported to result
in small epidemics in the Philippinnes and Thailand to
individual cases in a number of other countries including Taiwan, Indonesia, Japan, Iran and Egypt. Infection is
acquired through eating undercooked sh which serve
as intermediate hosts. The adults live in the upper small
intestine where autoinfection is responsible for maintaining infection over many years. A chronic malabsorption
syndrome can result which manifests as weight loss,

abdominal pain, muscle wasting, weakness, and oedema. A
study in the Philippinnes reported a fatality rate of around
5% (Cross, 1992) which is unusually high for nematode
infections in humans. Birds appear to be the usual denitive
hosts. Control is performed by treatment with mebendazole and through education. The parasite has been greatly
reduced in areas where the practice of consuming undercooked sh has been discontinued. The contribution to the
burden of parasitic zoonoses is low.
6. Trends in the burden of protozoan zoonoses
6.1. Diarrhoeal diseases
Approximately 4 billion diarrhoeal episodes occur
worldwide each year which account for 4% of all deaths and
5% of days lost to disability (Sazawal et al., 2006). Diarrhoeal
diseases result in 59 million DALYs per annum globally
(Lopez et al., 2006; WHO 2008). A signicant proportion
of this global burden is caused by zoonotic protozoan parasites including Cryptosporidium, Giardia and Blastocystis
spp.
6.1.1. Giardiosis
Giardia is the most common intestinal pathogen of
humans and domestic animals with a worldwide distribution including both temperate and tropical regions
(Thompson, 2011). Despite this the frequency of zoonotic
transmission is uncertain. Giardia spp. are widespread and
known to affect at least 40 species of vertebrates, including
humans. There is now strong evidence that some genetic
variants of G. duodenalis are host specic and the role of
this parasite as a zoonosis remains controversial. Only two
assemblages (i.e., A and B) seem to be zoonotic and recent
ndings suggest that zoonotic transmission occurs more
rarely than previously believed (Monis et al., 2009).
The clinical signs associated with Giardia infections
in humans vary greatly (reviewed by (Thompson, 2011).
There may be total latency, acute short-lasting diarrhoea or
chronic syndromes associated with nutritional disorders,
malabsorption, weight loss and failure to thrive. It is these
chronic syndromes that are likely to result in the highest
burdens of disease.
In low and middle income countries about 200 million
people have symptomatic giardiosis with some 500,000
new cases reported each year (Savioli et al., 2006). In the
USA the numbers of human cases between 1998 and 2007
remained fairly constant at around 20,000 per year (Hlavsa
et al., 2005; Yoder and Beach, 2007). Most authorities consider that direct person to person transmission is more
important than water-borne, food-borne or zoonotic transmission (Hunter and Thompson, 2005).
Livestock, such as cattle, are frequently infected but
molecular evidence suggests zoonotic transmission from
cattle is unusual. Molecular epidemiological studies in
localised endemic foci of transmission have provided evidence in support of the role of dogs in cycles of zoonotic
transmission (reviewed by Leonhard et al., 2007). There
appears to be scant evidence for transmission from wildlife
to humans and it may indeed be humans that transmit the

parasite to wildlife (Thompson, 2011).
6.1.2. Cryptosporidiosis
Cryptosporidium is a major cause of diarrhoeal disease
in humans worldwide. Water-borne, food-borne and contact with infected animals represent the major routes of
transmission to humans (Slifko et al., 2000; Smith et al.,
2007). Cryptosporidium infection can be a particular problem in immunosupressed and HIV positive individuals
resulting in severe, chronic disease and infection can be
fatal. In immune-competent patients, cryptosporidiosis is
usually a self-limiting disease of the intestinal tract. Sixteen
valid Cryptosporidium species and a further 33 genotypes
have been described, but only a few are zoonotic (Xiao
and Fayer, 2008). Cryptosporidium parvum is the major
zoonotic species with young cattle being an important
reservoir of infection. Water-borne outbreaks as well as
infections through handling animals, contact with children and through recreational waters have been reported.
Oocysts may also contaminate soft fruits and salad vegetables and cause infections in humans by these routes (Anh
et al., 2007). Oocysts have also been found in shellsh, such
as oysters and mussels that are often eaten raw (Schets
et al., 2007).
A systematic review of the global proportion of diarrhoeal cases in individuals of 5 years or greater suggested
that a median of 1.3% of inpatients and 6.9% of outpatient/community patients with diarrhoea had an aetiology
of cryptosporidiosis (Walker et al., 2010). The proportion
of these that were zoonotic is unknown.
In the UK, approximately 38.5% of human cryptosporidiosis is due to C. parvum which indicates substantial
proportions are zoonotic in origin. Of these, 25% are
attributable with direct contact with cattle (Chalmers et al.,
2011). In France between 2006 and 2009, 54% of conrmed cryptosporidiosis cases were due to C. parvum
(Derouin et al., 2010). Of these immunocompetent patients
accounted for 28% with HIV patients accounting for 39%.
In the US between 6479 and 11657 cases of Crytosporidium are reported annually (Yoder et al., 2010). However
differentiation at species level was not reported.
There appears to be different patterns of infection of
zoonotic Cryptosporidium spp. with high income countries
having a greater proportion of zoonotic cases compared to
low income countries. In low income countries, the majority of studies show a dominance of C. hominis in humans
representing 7090% of infections with the disease burden attributable to C. parvum much lower (Xiao and Feng,
2008). This trend is reversed in high income countries.
Children and HIV positive individuals have a higher prevalence of C. meleagridis, C. canis, C. felis, and C. muris. Most
human infections with C. canis have been reported from
low income countries. Furthermore, another interesting
features of C. parvum infection from low income countries
is that most human infections are due to the anthroponitc
IIc subtype of C. parvum. Thus, where C. parvum does occur
in such countries it is more likely to be of anthroponotic
rather than zoonotic in origin (Xiao and Feng, 2008).
The burden of disease in high income countries due
to zoonotic Cryptosporidium is low. Although there are a
89
small number of fatalities (Scallan et al., 2011), the disease generally has an acute non fatal outcome with few
long term sequaelae. In contrast there are reports from
lower income countries of signicant fatality rates in young
children and long term growth retardation (Chalmers and
Davies, 2010). These types of sequaelae will result in a considerable number of DALYs lost, but most of these DALYs
will be attributable to anthroponotic rather than zoonotic
transmission. In immunosupressed patients crytosporidiosis can be a major problem. In HIV patients infection can
be lifelong and result in premature mortality compared to
HIV patients without cryptosporidiosis. Thus it is possible
to attribute addition DALYs lost due to crytospridiosis in
HIV patients (Havelaar et al., 2000).
6.1.3. Blastocystosis
Blastocystis is now considered to be a zoonosis and it
is believed that animals such as pigs and chickens constitute large reservoirs for human infection via the faecal-oral
route (Tan, 2004). In addition high prevalence in domestic
dogs and cats suggest that these domestic animals could be
a source of human infection.
Blastocystis is reported to be one of the most common
protozoans found in faecal samples of both symptomatic
patients and asymptomatic individuals (Cirioni et al., 1999;
Taamasri et al., 2000; Windsor et al., 2002). Blastocystis
has a worldwide distribution and ndings of many surveys
reported it to be the most frequently isolated protozoan
parasite. Prevalence of Blastocystis infection is higher in low
income compared to high income countries with prevalences of up to 69% being reported from the former.
Despite the parasite being common and linked to
zoonotic transmission, the exact role of Blastocystis as a
cause of human disease is uncertain. A number of clinical and epidemiological studies implicate the parasite as a
potential pathogen whilst others exonerate it as an aetiology of intestinal disease. So whilst signicant progress
has been achieved on descriptions of the morphology and
genetic diversity of Blastocystis, most aspects of its life cycle,
molecular biology, and pathogenicity remain unresolved
(reviewed by Puthia and Tan, 2011; Stensvold et al., 2009)
Therefore until the clinical signicance of this parasite is
conrmed it is only possible to speculate on the likely
burden impact. Currently we have no indications that the
burden of blastocystosis is substantial
6.2. Microsporidiosis
Microsporidia were conrmed as a cause of encephalitis in 1959 (Matsubayashi et al., 1959). Subsequently
Microsporidia have been associated with intestinal disease
and other syndromes in HIV patients (Hennequin et al.,
1992). The number of articles describing human disease
has increased rapidly since 1990 and it is now known
that Microsporidia can infect virtually any organ system;
and patients with encephalitis, ocular infection, sinusitis,
myositis, and disseminated infection are well described in
the literature (Wieiss, 2011).
It now seems that Microsporidia are common enteric
pathogens causing self-limited infections in immune
competent hosts and have been reported globally. Serosur-
90
veys have demonstrated a high prevalence of antibodies

against Encephalitozoon spp. suggesting asymptomatic
infection could be common. It is likely that a number of
Microsporidia are zoonotic (Mathis et al., 2005). Acute self
limiting infections followed by recovery will result in a low
disease burden. Where Micropsoridia are likely to result
in a larger disease burden would be in syndromes where
there are chronic disabling sequaelae. This could include
syndromes such as encephalitis. Nearly all Microsporidia
infections are opportunistic in immunosupressed individuals, such as HIV patients and disease burden should be
assigned to the primary condition. Therefore Microsporidia
infections are likely to track those of the primary conditions
and hence the burden of primary microsporidiosis is very
low. In high income countries, where effective antiretrovial therapies are available, Microsporidia infections are
likely to become less frequent. In contrast in low income
countries where antiretroviral therapies are less available,
mircrosporidiosis is likely to remain a persistent problem
in HIV patients.
6.3. Trypanosomosis
6.3.1. African trypanosomosis
Human African trypanosomiosis (HAT) is caused by
infection with one of two parasites: Trypanosoma brucei
rhodesiense or Trypanosoma b. gambiense. Only the former
of these appears to be zoonotic with reservoirs in both
domestic and wild life species (Fevre et al., 2008). T. b.
rhodesiense occurs only in East Africa. The vast majority
of reported cases of HAT are due to T. b. gambiense with
between 11,000 and 24,000 cases reported annually. In
contrast only 400 to 800 annual cases of HAT due to the
zoonotic T. b. rhodesiense are reported (Simarro et al., 2008;
WHO, 2006). Estimates of the numbers of HAT including
unreported cases of both non zoonotic and zoonotic forms
have varied between 70,000 and 300,000 (WHO, 1998a,
2006). The rst global burden of disease study estimated
the burden of HAT as 1.78 million DALYs but did not differentiate between the two forms (World Bank, 1993).
Revised estimates have suggested 1.34 million DALYs lost
in 2000 and 1.54 million lost in 2002 (reviewed by Fevre
et al., 2008). These DALY calculations resulted from an
estimated 48,511 deaths and a disability weight on those
with HAT of 0.191. If the total burden for HAT is composed of a similar proportion of zoonotic to non zoonotic
HAT as the reported cases, then it can be estimated that
approximately 5% of these DALYs can be assigned to T.
b. rhodesiense and 95% to T. b. gambiense. This assumes
that the duration of disease is similar for both forms. This
may not be the case as the zoonotic form of the disease
may have a duration of 1 year per episode compared to
the non zoonotic form of the disease which is 5 years
(Fevre et al., 2008). Although variations in the duration
and sequaelae may have an impact on the estimate of
the DALY through variations in the YLDs, the main factor
driving the total burden estimate with HAT are the fatalities, especially as the disease is under-reported and non
treated cases are usually fatal. It is believed that between
38 and 41% of T. b. rhodesiense cases go unreported (Fevre
et al., 2005; Odiit et al., 2005). Thus the burden of zoonotic
HAT is likely to be higher than the above data suggests. As

the number of new cases of T. b. rhodesiense reported has
been declining since 1990 when 1933 cases were reported
(WHO, 2006), it is possible that the total burden due to
zoonotic HAT is declining. More accurate surveillance data
and modelling of under-reporting is needed to conrm
this.
6.3.2. American trypanosomosis
American trypanosomosis or Chagas disease is caused
by Trypanosoma cruzi and is a chronic systemic infection.
In approximately 2030% of infected individuals the infection results in severe cardiopathy (cardiomegaly or apical
aneurysms) or mega oesophagus and or mega colon The
disease is a zoonosis with a large number of domestic and
wild vertebrate reservoirs. The disease is mainly conned
to Latin America where there are approximately 28 million
people at risk of infection.
Since the early 1990s a series of control and elimination programmes have been implemented and have
contributed to an interruption in transmission across large
geographical areas. Consequently it is estimated that about
7.5 million people were infected in 2006 which is a reduction of 50% from infection rates in 1990 (WHO, 2007).
In 1993 the global burden of Chagas disease was estimated at 2 million DALYs annually (World Bank, 1993).
In 2001 a revised estimate suggested that it was 584,000
DALYs annually (Lopez et al., 2006) and in 2004 the estimate was 430,000 DALYs with projections for 2008 and
2015 for it to be reduced further to below 300,000 DALYs
annually.
6.4. Leishmaniosis
Human leishmanioses have diverse clinical manifestations. Visceral leishmaniosis (VL), caused by Leishmania
donovani in the Old World and L. infantum in both the
Old and New Worlds, is the most severe form which,
if left untreated, invariably leads to death. A number of
different species of Leishmania cause cutaneous (CL) or
mucocutaneous (MCL) leishmaniosis which, if not fatal, are
responsible for considerable morbidity in a vast number of
people in endemic foci. Amongst the 15 well-recognized
Leishmania species known to cause disease in humans, 13
are zoonotic (Gramiccia and Gradoni, 2005). Two species,
L. donovani and L. tropica, are considered as having an
exclusive or predominant anthroponotic transmission pattern. However, the presence of animal reservoir hosts has
been indicated in several endemic settings, such as eastern Sudan for L. donovani, and Morocco, northern Israel
and Iran for L. tropica. Human leishmaniosis is one disease
whose global burden has been estimated specically under
the GBD project. The global burden is approximately 2 million DALYs per annum (Lopez et al., 2006), although there
is a projected decline in this burden. Substantial underreporting is a recognised problem with this disease (Bern
et al., 2008) so the global burden is likely to be higher.
Incidence of leishmanioses is not uniformly distributed in
endemic areas: about 90% of CL cases occur in only seven
countries (Afghanistan, Algeria, Saudi Arabia, Syria, Iran,
Brazil and Peru), whereas some 90% of VL cases occur in
rural and suburban areas of ve countries (Bangladesh,

India, Nepal, Sudan and Brazil). The relative contribution
to the global burden by zoonotic transmission of Leishmania spp. is unknown. L. infantum is the cause of the most
widespread form of zoonotic VL and occurs in several countries in Central and South America (especially Brazil), in
the Mediterranean basin and in central Asia. The main foci
of zoonotic CL are found in Africa, Asia and in most Latin
American countries. The Leishmania species involved in
the old world are L. major, L. aethiopica and dermotropic
L. infantum. In the new world they are L. braziliensis, L.
guyanensis, L. lainsoni, L. naif, L. panamensis, L. peruviana,
L. shawi, L. mexicana, L. amazonensis, L. venezuelensis and
dermotropic L. infantum.
6.5. Toxoplasmosis
Toxoplasmosis is a major zoonosis with a global distribution. A large proportion of the worlds population
have serological evidence of infection. Humans can become
infected through ingestion of oocysts, for example contaminating food or water or by contact with cats. Epidemiological evidence suggests that in most countries humans
are infected more frequently through the consumption
of undercooked meat containing viable bradyzoites. For
example a sereological survey of pregnant women from
Chile suggested that 43% of seropositive women were also
seropositive to oocyst antigens. This suggested that 57%
acquired the infection through meat (Munoz-Zanzi et al.,
2010). The global burden of disease attributable to toxoplasmosis is presently not known, but there is evidence
to suggest it is considerable. The most well known sequelae of toxoplasmosis results from maternal infection for
the rst time during pregnancy and can result in foetal
death, neonatal death or various congenital defects, such as
hydrocephalus, other CNS abnormalities and chorioretrinitis. A recent study in the Netherlands indicted an incidence
of congenital toxoplasmosis of 2 cases per 1000 births. This
results in approximately 2300 DALYs per annum (Kortbeek
et al., 2009). Extrapolations from a single country nding
into other countries should be undertaken with caution
as transmission rates vary depending on culture, diet and
farming practices. The incidence of congenital toxoplasmosis is believed to be considerably lower in Denmark
and Ireland (Kortbeek et al., 2009) compared to France
(Havelaar et al., 2007). In the Netherlands toxoplasmosis appears to be the most important food transmitted
pathogen in terms of numbers of DALYs, surpassing that
of campylobacteriosis (Kortbeek et al., 2009).
A recent review reports the global seroprevalence of
toxoplasmosis in pregnant women or women of childbearing age varies between 5.3% and 78%, increasing with age
(Pappas et al., 2009). Such variability illustrates differences
in exposure across the globe. In the Americas seroprevalences range from 6.1% in Durango in Mexico to 78% in
Recife in Brazil. In Europe prevalence ranges from 8.2% in
Lausanne and Geneva in Switzerland, to 63% in Western
Pomerania in Germany. In Asia the reported range was from
5.3% in Bangkok Thailand to 64% in Babol, Iran. In Africa
prevalence ranges from 25% in Burkino Faso to 75% in Sao
Tome and Principe. The Netherlands has a mid range preva-
91
lence of 35% for comparison. From this data it is clear that

the global burden of congenital toxoplasmosis is considerable. Studies are on going to estimate this burden and
should be available in the near future.
Toxoplasmosis is not only a problem for the unborn
child through congenital transmission. It is also a serious problem in immunosuppressed individuals such as
HIV patients and transplant patients. However, as discussed earlier, the disease burden in these cases should be
assigned to the primary condition.
Toxoplasmosis has always been assumed to be a mild or
unapparent infection in otherwise healthy individuals with
no signicant health effects. This presumption is increasingly being challenged with reports of seropositivity being
linked to a number of disorders such as epilepsy (Palmer,
2007) and schizophrenia (Torrey et al., 2007). There are
also reports of increased road trafc accidents amongst
seropositive individuals (Flegr et al., 2002, 2009). If toxoplasmosis is attributed to these issues then the global
burden of disease is likely higher still.
Added to the human burden is the burden of abortion,
and barrenness as a result of T. gondii infection particularly
is sheep. The widespread distribution of the parasite and
the importance of sheep in many countries suggest that
such economic losses would also be substantial (Dubey,
2009).
7. Trends in the burden of arthropod zoonoses
Many arthropods are zoonoses including a number of
ea species, Sarcoptes spp. and many dipteran ies that
can result in myiasis. The burden of diseases caused by
zoonotic transmission of these organisms is unknown and
there are few if any advocates investigating the specic
burden of such diseases. In the GBD study many of the conditions caused by these parasites will be included in the
global burden of skin diseases, which presently accounts
for approximately 4 million DALYs per year globally (Lopez
et al., 2006). This is a very small proportion 0.25% of
the global burden of disease. Zoonotic skin parasites are
likely to represent only a small proportion of the global
burden of skin diseases. In an Indian study for example, of 32,078 dermatoses in children, scabies accounted
for 21.5% of cases (Sardana et al., 2009). However, the
overwhelming majority of scabies cases globally will be
the result of human to human transmission rather than
from zoonotic transmission. Myiasis is reported sporadically and, occasionally, migrating y larvae can affect vital
organs. Humans are also frequently bitten by ticks, but tick
born diseases will have a greater signicance than the ticks
themselves.
Despite this there could be diseases where the assumptions of a low burden can be questioned. For example, in
tropical Africa and Latin America there are hundreds of
millions of people at risk from infestation with two ea
species Tunga penetrans and T. trimamillata which can have
reservoirs in many species of mammal. The female ea will
burrow into the skin causing signicant lesions. If these
lesions are localised in the foot, as they frequently are, they
can be both painful and disabling (Pampiglione et al., 2009).
This would indicate a higher disability weight than would
92
normally be expected from many skin diseases and hence

a potentially higher disease burden.
8. Conclusions
The global socioeconomic burden of parasitic zoonoses
is presently unknown. Nevertheless data from recently
published work, data from the GBD studies and on-going
work suggests that the global burden is considerable.
To date evidence indicates that the global burden of
echinococcosis and cysticercosis will each be in the low
millions of DALYs annually with substantial additional
nancial burdens to the livestock industry. The burden of
human toxoplasmosis is likely to be even higher. Likewise
the burden of food born trematodes will be of a similar
order of magnitude. Globally the economic burden of fasciolosis to livestock is also very high. The global burden of
schistosomiosis is believed to be much higher than previously thought and a substantial part of the burden due
to S. japonicum is of zoonotic origin. Globally, diarrhoea
is the cause of 21% of deaths in children under 5 years
of age (Kosek et al., 2003) and over 4% of the total global
burden of disease and injuries is attributable to diarrhoea
(Lopez et al., 2006). If only a modest proportion of the
global DALYs are attributable to zoonotic protozoa then
there will also be a burden of disease in the low millions
of DALYs. There will be other substantive contributions
from zoonotic leishmaniosis and Chagas disease. Collectively it is possible that parasitic zoonoses have a global
burden of disease in humans similar to either tuberculosis
or malaria. This is illustrated in the Table 1. In addition for
many parasitic zoonoses such as Fasciola spp., there is a substantive additional economic burden in livestock. However
these diseases remain neglected and, at least until recently,
burden studies of these diseases were also neglected. This
is now being rectied. Initiatives such as the global burden of food borne (cordinated by the Food Borne Disease
Epidemiology Reference Group), and the burden of child
hood diseases (coordinated by the Child Health Epidemiology Reference Group) (see Stein et al., 2007) are including
some specic parasitic zoonoses in their global estimates.
In addition some parasitic zoonoses are being specically
included in the latest GBD estimates which should be available in the near future. However there is no initiative at
present to specically calculate the burden of zoonotic diseases other than the piecemeal approach described. This
should be addressed as zoonotic diseases often need to
be controlled in the animal hosts to prevent human disease and hence the costs of intervention in animals will
drive cost effectiveness. Furthermore, quality disease burden studies are a powerful advocate to attract attention and
hopefully funding into combating some of the worlds most
neglected diseases.
Conict of interest
The authors declare that there is no conict of interest.
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Veterinary Parasitology 182 (2011) 7995

Contents lists available at ScienceDirect

The socioeconomic burden of parasitic zoonoses: Global trends

Division of Epidemiology, Vetsuisse Faculty, University of Zurich, Zurich, Switzerland

Corresponding author. Tel.: +41 44 635 90 41.

are also being attributed to parasitic zoonoses and hence

P.R. Torgerson, C.N.L. Macpherson / Veterinary Parasitology 182 (2011) 7995

in low income countries due to variations in medical and

animal health. Monetarizing human health losses is one

P.R. Torgerson, C.N.L. Macpherson / Veterinary Parasitology 182 (2011) 7995

Animal Health Costs

Long term is decrease

Food borne trematodes Fasciola spp.

Unknown, but likely to

New sequaelae are

Burden due to Chagas

Assumes new disability

Assumes c 30% of epilepsy

Estimated from GBD

taken in Uruguay (Torgerson et al., 2000) which suggested

The UK has an endemic focus, mainly in Wales and is

P.R. Torgerson, C.N.L. Macpherson / Veterinary Parasitology 182 (2011) 7995

Elsewhere in Asia there are large numbers of CE cases

Ziadinov et al., 2008) and a very high intensity of infection

P.R. Torgerson, C.N.L. Macpherson / Veterinary Parasitology 182 (2011) 7995

as many parts of Africa, prevalences are typically greater

3.2. Adult cestode zoonoses

P.R. Torgerson, C.N.L. Macpherson / Veterinary Parasitology 182 (2011) 7995

trematodes have yet to be calculated but taken as a whole

in the biliary system or intestine: occasionally ectopic

P.R. Torgerson, C.N.L. Macpherson / Veterinary Parasitology 182 (2011) 7995

Paragonimosis is an important food-borne trematode

P.R. Torgerson, C.N.L. Macpherson / Veterinary Parasitology 182 (2011) 7995

water buffaloes were treated with praziquantel and the

Seroprevalence rates have been examined in a few

P.R. Torgerson, C.N.L. Macpherson / Veterinary Parasitology 182 (2011) 7995

5.1.3. Other ascarid species

P.R. Torgerson, C.N.L. Macpherson / Veterinary Parasitology 182 (2011) 7995

lariae are transmitted by a range of mosquito (Culex, Aedes

syndrome can result which manifests as weight loss,

P.R. Torgerson, C.N.L. Macpherson / Veterinary Parasitology 182 (2011) 7995

to humans and it may indeed be humans that transmit the

P.R. Torgerson, C.N.L. Macpherson / Veterinary Parasitology 182 (2011) 7995

veys have demonstrated a high prevalence of antibodies

HAT is likely to be higher than the above data suggests. As

P.R. Torgerson, C.N.L. Macpherson / Veterinary Parasitology 182 (2011) 7995

rural and suburban areas of ve countries (Bangladesh,

lence of 35% for comparison. From this data it is clear that

P.R. Torgerson, C.N.L. Macpherson / Veterinary Parasitology 182 (2011) 7995

normally be expected from many skin diseases and hence

Ethiopia: prevalence, cyst viability distribution and its public health

P.R. Torgerson, C.N.L. Macpherson / Veterinary Parasitology 182 (2011) 7995

Hotez, P.J., Fenwick, A., 2009. Schistosomiasis in Africa: an emerging

P.R. Torgerson, C.N.L. Macpherson / Veterinary Parasitology 182 (2011) 7995

Monis, P.T., Caccio, S.M., Thompson, R.C.A., 2009. Variation in Giardia:

P.R. Torgerson, C.N.L. Macpherson / Veterinary Parasitology 182 (2011) 7995

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