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Improving prenatal nutrition in developing countries: strategies,

prospects, and challenges13


Jose O Mora and Penelope S Nestel

ABSTRACT In developing countries, the health and nutrition programs; and the increased opportunities for policies and pro-
of females throughout their entire life is affected by complex and grams that can be implemented through existing health systems,
highly interrelated biological, social, cultural, and health which are expanding and providing better coverage, particularly in
servicerelated factors. Rather than focusing exclusively on the prenatal care, in most developing countries.
prenatal period, we describe a life cycle approach to improving The situation is not dire, however. By translating and integrat-

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maternal nutrition, which goes beyond the traditional provision of ing existing biological and socioeconomic knowledge into practi-
nutrition services during pregnancy, by addressing risk factors that cal action, a solid basis for policy and program decisions can be
are present well before pregnancy, even before childbearing age. developed. The purposes of this article are 1) to review the ration-
This approach involves specific policy initiatives and a minimum ale for improving prenatal nutrition and strategy, policy, and pro-
package program that is targeted at females. Policy actions and the gram options and 2) to identify the prospects for and challenges
components for effective implementation of the program are to improving prenatal nutrition in developing countries.
described. The prospects and challenges to be overcomewhich
include translating scientific knowledge into action, removing con-
ceptual and implementational constraints, identifying biologically RATIONALE
meaningful indicators for problem identification, and improving Some 200 million women become pregnant each year, most of
understanding of physiologic and social adaptation mechanisms them in developing countries (5). Many of these women suffer
are discussed, as are persistent problems with health care delivery from both ongoing nutritional deficiencies and the long-term
systems. Am J Clin Nutr 2000;71(suppl):1353S63S. cumulative consequences of undernutrition during childhood.
Pregnancy-related health and nutritional problems affect a
KEY WORDS Prenatal nutrition, developing countries, womans quality of life, that of her newborn infant well beyond
nutrition strategies, women, adolescent girls, nutritional delivery, and that of her family and community.
programs, malnutrition The effect of womens prenatal health and nutritional status
on child growth, health, survival, and development occurs both
through reproductive performance and survival and through fetal
INTRODUCTION growth and development. McGuire and Popkins (6) review of
Good maternal nutrition is important for the health and repro- studies on the nutritional status of pregnant and lactating women
ductive performance of women and the health, survival, and devel- showed that women in developing countries consumed only
opment of their children. Malnutrition in women, including preg- about two-thirds of the recommended daily intake of energy and
nant women, is not conspicuous and remains, to a large extent, that their average weight for height was, in most cases, well
uncounted and unreported; thus, insufficient attention has been below the 50th percentile for small-framed women in developed
given to the extent, causes, and consequences of malnutrition in countries. Moreover, the energy and nutrient intakes of pregnant
women (1). As a result, inadequate resources and efforts have been and lactating women tended to be only slightly higher than those
allocated to improving womens nutrition compared with other of nonpregnant women, although the nutritional requirements of
nutritional and public health actions (2). The limited available data pregnant and lactating women were significantly greater. Other
and the few experiences with programs that do exist come mostly studies, for example the study by Black et al (7), showed that
from small-scale efforts to improve nutrition during pregnancy,
often through nutritional supplementation to enhance fetal growth
and birth weight (3). It was suggested that highly publicized ini- 1
From the International Science and Technology Institute, Arlington,
tiatives such as child survival and safe motherhood have not
VA, and the Department of International Health, Johns Hopkins University,
had the expected effect because too little attention has been given Baltimore.
to the nutritional status of women, including mothers (4). This 2
Presented at the symposium Maternal Nutrition: New Developments and
lack of emphasis on womens nutrition is unacceptable given the Implications, held in Paris, June 1112, 1998.
importance of nutrition to womens health, pregnancy outcome, 3
Reprints not available. Address correspondence to JO Mora, 1820 North
and child survival; the availability of effective nutrition-related Fort Myer Drive, Suite 600, Arlington, VA 22209. E-mail: jmora@istiinc.com.

Am J Clin Nutr 2000;71(suppl):1353S63S. Printed in USA. 2000 American Society for Clinical Nutrition 1353S
1354S MORA AND NESTEL

micronutrient deficiencies, particularly deficiencies of iron and Maternal mortality, however, is not the only adverse or most
vitamin B-12, were frequent in pregnant women in Mexico. Poor frequent outcome of pregnancy. More than 40% of pregnancies
health and nutrition are associated with repeated, closely spaced in developing countries result in complications, illness, or per-
pregnancies that progressively reduce womens nutritional manent disability for the mother or child (1). Because of a
reserves to the point of nutritional depletion, known as the womans childbearing and nurturing roles, her pre- and postnatal
maternal depletion syndrome (810). health and nutritional status is an important determinant of the
The definitive negative outcome of poor prenatal health and survival and development of her fetus and newborn child. More
nutrition, as well as inadequate care during pregnancy and delivery, than 7 million newborn deaths are associated with maternal
is reflected in the high prevalence of maternal mortality in devel- health- and nutrition-related problems resulting from poorly
oping countries; nearly 600 000 women die each year from preg- managed pregnancies and deliveries or inadequate care of the
nancy-related causes (11). As shown in Table 1, the global mater- neonate soon after birth (5).
nal mortality rate is 460/100 000 live births; the rate for developing An intergenerational cycle of ill health and growth failure in
countries is 500/100 000 live births, and the rate for developed which undernutrition in childhood leads to small body size in
countries is 10/100 000 live births. Within the developing world, adulthood has been described (16, 17). Malnourished women (ie,
however, there are huge regional variationsfrom 140/100 000 live women who are short, are underweight, do not gain sufficient
births in Central America to 1080/100 000 live births in eastern weight during pregnancy, or are anemic) are more likely to have
Africa (12). Adolescent girls have a 25 times greater risk of mor- miscarriages or stillbirths or to deliver babies with intrauterine
tality than do other women of reproductive age (1). Indeed, of all growth retardation (IUGR) or low birth weight (LBW; 1820),
the human-development indicators, the greatest disparity between which are linked, in turn, to increased risk of perinatal and infant
developed and developing countries is in the risk of maternal mor- mortality (2123). Globally, 15.3% of all babies are born with

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tality (11). Although poor prenatal nutrition contributes directly LBW, > 2.5 times more so in developing (16.4%) than in devel-
and indirectly to this large mortality rate, the extent of its contribu- oped (6.2%) countries (24). Severe anemia in pregnancy is
tion has not been measured because the main reported causes of believed to increase the risk of maternal mortality in childbirth
maternal mortality (hemorrhage, obstructed delivery, eclampsia, (23) and about half of the infants whose mothers have died do
sepsis, and unsafe abortion) greatly overshadow the role of nutri- not survive to celebrate their fifth birthday (25). There is also
tion itself. It is well established, however, that stunted women are evidence to suggest that severe maternal iron deficiency causes
at higher risk of obstructed labor as a result of cephalopelvic dis- reduced iron storage in the fetus and the newborn infant, which
proportion (13). Nationally representative data collected in the predisposes the infant to iron deficiency anemia (18). In addi-
Demographic and Health Surveys show that significant proportions tion, malnourished women do not have adequate capacity to sus-
of nonpregnant women were at risk of adverse pregnancy outcomes tain prolonged lactation (19, 20).
by virtue of their short stature (<145 cm), low body weight (<45 kg), Newborns with IUGR and babies with LBW have the greatest
or both (Table 2) (S Rutstein, personal communication, 1998). risk of infection because of reduced immune competence. Poor
Between 1% and 20% of these women were chronically energy nutrition in early childhood not only increases the risk of perina-
deficient (14), although there is no consensus about the value of tal, infant, and child morbidity and mortality but also affects
body mass index as an indicator (15). long-term physical growth (26, 27), cognitive development and

TABLE 1
Selected maternal health and nutritional indicators, 19981
Women aged Total Contraceptive Prenatal Delivery Maternal
Region All women 1549 y fertility rate use care care mortality
million million per 1000 live births % % % per 100 000 live births
Asia 1753 929 2.9 54 65 61 410
Western 88 44 4.2 61 71 350
South central 701 354 3.8 35 52 36 570
Southeast 253 135 3.2 43 79 53 460
East 711 396 1.8 78 80 87 90
Africa 390 182 5.6 18 63 43 880
Sub-Saharan 321 146 6 12 40 980
Northern 83 42 4 38 56 61 330
Western 115 100 6.2 6 60 34 1020
Eastern 121 108 6.2 12 66 33 1080
Middle 46 41 6.5 58 950
Southern 25 20 3.4 48 89 80 270
Latin America and Caribbean 252 134 3 57 73 75 180
Central 66 34 3.5 52 70 67 140
Caribbean 18 10 2.7 49 88 79 350
South 167 90 2.8 61 73 77 190
World 2941 1514 3 50 68 65 460
Developed 606 297 1.6 61 97 99 10
Developing 2334 1216 3.4 48 65 58 500
1
From references 5 and 12.
PRENATAL NUTRITION IN DEVELOPING COUNTRIES 1355S

TABLE 2
Maternal nutritional status1
Obstetric risk
Short stature Low body wt Both risk Total Neither risk BMI
(<145 cm) (<45 kg) factors at risk factor <18.5 30
%
Africa
Benin (n = 2566) 1.3 11.9 0.8 14.0 86.0 NA NA
Burkina Faso (n = 4233) 0.8 6.7 0.3 7.8 92.2 14.7 1
CAR (n = 2408) 1.6 10.4 1.6 13.7 86.3 NA NA
Comoros (n = 899) 2.4 12.2 1.6 16.1 83.9 NA NA
Cte d Ivoire (n = 3520) 0.7 7.0 0.3 8.0 92.0 NA NA
Ghana (n = 1927) 0.6 9.0 0.5 10.1 89.9 12.2 3.5
Kenya (n = 3822) 0.5 7.9 0.6 9.0 91.1 9.9 2.5
Malawi (n = 2776) 1.3 11.3 1.5 14.2 85.8 9.7 1.1
Mali (n = 5064) 0.5 7.4 0.4 8.3 91.7 NA NA
Namibia (n = 2581) 1.2 8.9 0.4 10.5 89.5 13.9 7.6
Niger (n = 4104) 0.2 12.3 0.3 12.7 87.3 19.6 1.4
Senegal (n = 3483) 0.7 6.6 0.1 7.4 92.6 15.1 3.8
Tanzania (n = 4364) 1.8 10.2 1.7 13.7 86.3 9.8 2
Uganda (n = 4120) 1.4 8.3 0.9 10.6 89.4 NA NA

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Zambia (n = 4525) 0.8 7.6 0.8 9.2 90.8 11.4 2.5
Zimbabwe (n = 2103) 0.4 3.6 0.5 4.6 95.4 5.2 5.9
North Africa
Egypt (n = 7539) 1.4 1.7 0.3 3.3 96.7 1.6 23.9
Morocco (n = 3354) 1.6 4.5 0.5 6.6 93.4 3.8 10.9
Turkey (n = 2650) 2.2 3.3 0.3 5.8 94.2 2.6 18.4
Latin America and Carribean
Bolivia (n = 2670) 10.6 5.0 2.2 17.8 82.2 2.5 8
Brazil (n = 3302) 2.3 6.5 1.5 10.3 89.7 NA NA
Colombia (n = 3817) 4.3 5.1 1.3 10.8 89.2 3.9 9.2
Dominica (n = 2358) 1.8 10.3 1.1 13.1 86.9 9 7.4
Guatemala (n = 5413) 20.1 6.8 12.8 39.8 60.2 3.8 8.2
Haiti (n = 2271) 1.7 13.9 1.2 16.8 83.3 NA NA
Peru (n = 10711) 12.4 3.2 3.1 18.6 81.4 1.3 9.2
Asia
Bangladesh (n = 4497) 2.2 53.7 15.9 71.8 28.2 NA NA
Nepal (n = 3745) 2.8 39.1 12.0 53.9 46.1 NA NA
Newly Independent States
Kazakstan (n = 3707) 0.6 5.4 0.4 6.4 93.7 NA NA
Uzbekistan (n = 4388) 0.7 5.6 0.4 6.7 93.3 NA NA
1
Source: S Rutsetin, personal communication, 1998.

future learning capacity (28), school performance (28, 29) and ease, in adulthood (34, 35). Clearly, the lack of attention to
educational outcomes, and work performance (30). Girls often womens nutrition has enormous implications for social, eco-
experience discriminatory child-care, feeding, and health care nomic, and national development.
compared with boys that can result in protein-energy malnutrition It is difficult to estimate the extent of womens malnutrition,
(PEM) and micronutrient deficiencies. The increased nutritional even in pregnant women, in developing countries because few
demands for adolescent growth, coupled with chronic PEM and nationally representative studies have been done. This is com-
micronutrient deficiencies and often early childbearing, preclude pounded by the lack of consensus on the appropriate indicators and
many teenage girls from fully realizing their growth potential (31, reference standards for women. In 1985, Leslie (2) conservatively
32). Moreover, Bruner et al (33) found that treating anemic US estimated that of the 1130 million women aged > 15 y living in
adolescent girls improved the girls cognitive abilities, which may developing countries, almost 500 million were stunted as a result of
have important implications for the many adolescent mothers in PEM, <250 million were at risk of iodine deficiency disorders, and
developing countries. During their reproductive years, particu- almost 2 million were blind because of vitamin A deficiency. Vita-
larly during pregnancy and lactation, many women continue to min A deficiency is more frequent in Asia and Africa than in other
experience PEM and micronutrient deficiencies, although some countries (36), and in endemic areas night blindness has been
are affected by the consequences of overnutrition. In the postre- observed to be 525 times more frequent in pregnant women than
productive years, undernutrition, anemia, osteoporosis, and other in preschool children (37, 38), indicating womens increased vul-
nutrition-related problems are observed frequently in women (4). nerability to vitamin A deficiency during times of increased vita-
There is also growing concern that poor fetal and infant health min A requirements. On the basis of data collected in 1998 and on
and nutrition determine health risks, such as coronary heart dis- the assumption that 59% of pregnant women and 47% of all
1356S MORA AND NESTEL

women (39) are anemic, > 745 million of the > 1514 million women terns, health-seeking behavior, and use of health and nutritional
of childbearing age (1549 y) are anemic. Prevalence rates of ane- services. Biological factors include age of menarche, menstruation,
mia in pregnant and nonpregnant women are greater in Asia pregnancy, and increased risk of infections.
(<60% and 55%, respectively) and in Africa (51% and 42%, To have an effect on womens health and nutritional status,
respectively) (40) than in Latin America (35% and 20%, respec- programs that are socially, economically, culturally, and biolog-
tively) (41). PEM, iodine deficiency disorders, and iron deficiency ically appropriate are needed throughout the female life cycle,
are known to disproportionately affect females throughout infancy beginning as early as possible. In other words, womens health
and childhood as well as before and during pregnancy. and nutrition have to be considered as part of an intergenera-
The magnitude of female undernutrition and the enormous tional continuum under the rubric of reproductive and child
social, economic, health, and developmental implications of health (ie, pre- and postnatal care, including family planning,
poor prenatal nutrition of women and children provide a com- child survival, child development, school health, and adolescent
pelling rationale for systematic stronger action. Because of the health). This framework highlights the important role for public
reproductive consequences and the long-term effects of child- and private health services and 2 practical conclusions need to be
hood malnutrition on adult physical and intellectual productivity, emphasized. First, the consequences of womens undernutrition
as well as of the widespread effect of womens health and nutri- on child survival and development are at least as important as is
tion on child survival, womens productivity, family welfare, and the direct biological effect of undernutrition on the fetus during
poverty reduction in the community as a whole, securing ade- pregnancy and the infant during lactation. Second, a focus on
quate nutrition of women, particularly before and during preg- prenatal nutrition ignores the more fundamental problem of a
nancy, is a socially and economically important goal for devel- womans nutrition throughout her entire life, of which prenatal
oping countries. nutrition is only a small, albeit important, contributory factor.

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This is significant because nutritional status, unlike disease, is
cumulative over time and not an isolated incident (16).
CONCEPTUAL FRAMEWORK
Throughout womens entire life cycle, their health and nutrition
is affected by complex social, cultural, psychologic, biological, and STRATEGIES
health servicerelated factors that are highly interrelated. A con- Strategies to improve prenatal nutrition need to go beyond the
ceptual framework, adapted from Tinker et al (4), that identifies the conventional approach of providing services to pregnant women
critical points for action is outlined in Figure 1. Social, economic, through the traditional maternal and child health care programs.
and cultural factors include social status, female discrimination, Instead, a more comprehensive life cycle approach is needed that
fertility patterns (eg, pregnancy intervals, teenage pregnancy, and addresses the risk factors present well before pregnancy, ideally
unplanned pregnancies), and disease exposure. Individual behavior beginning in early childhood or, at the very least, before preg-
and psychologic factors include dietary practices, reproductive pat- nancy or before girls reach reproductive age.

FIGURE 1. Determinants of womens health and nutritional status.


PRENATAL NUTRITION IN DEVELOPING COUNTRIES 1357S

The promotion of optimal nutrition in girls during childhood a greater propensity and more- efficient use of health services
is a sound strategy for affecting female nutrition because it can (42), fewer pregnancies, and increased employment opportuni-
result in a build up of the nutritional reserves needed during peri- ties for women (46). It is therefore an important component of
ods of increased nutritional demand, including the adolescent any policy to enhance the status of women.
growth spurt, pregnancy, and lactation. Such action should be
Strengthen legislative and other support for womens nutrition
complemented by specific programs during critical periods, eg,
adolescence, childbearing age, pregnancy, and lactation. Improvements in legislative and other support for womens
Research in Guatemala, for instance, showed that improved nutrition would help provide universal food fortification; provide
nutrition during early childhood had longer-term payoffs than consumer price subsidies and targeted food distribution; provide
was previously thought in terms of greater stature and fat-free labor-saving devices for women; improve womens access to
mass, especially in females; improved work capacity in males; agricultural extension services and credit for small-scale busi-
and enhanced intellectual performance in both sexes (17). ness; reduce discrimination against women in employment prac-
Although primary health care nutritional programs are often tices; encourage womens control over family resources; remove
targeted at women, particularly pregnant women, in practice credit restrictions against women; enact fair marriage legislation;
most are designed primarily to reduce malnutrition in children. abolish practices harmful to womens health (eg, violence
Leslie (2) made an important distinction between being the tar- against women); remove legal impediments to the effective
get and being the beneficiary of a program. Women have been delivery of health services for females (eg, impediments to con-
the targets of health and nutritional programs aimed at improv- traception and barriers to service based on age, sex, or marital
ing fetal growth (birth weight) or childrens growth but paying status); support appropriate training and delegation of responsi-
little attention to the health and nutritional needs of the women bility, particularly for nonphysician health care in rural areas;

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themselves. There is currently a move toward getting consensus and encourage private sector participation in the delivery of
that health and nutritional programs implemented well before health services for women.
women become pregnant, and within a life cycle perspective,
Improve equity and efficiency in financing health and
will have a long-term effect on both the mother and the child,
nutritional services for women
although data to support this are still lacking. It is also probable
that women are more likely to be motivated to participate in pro- Improved equity and efficiency in financing health and nutri-
gram activities that have a clear benefit for themselves as well as tional services for women could be achieved by selecting a pack-
for their children. age of highly cost-effective nutritional programs to be publicly
financed; establishing cost-recovery schemes that target public
expenditures at the poor; and protecting poor women and remov-
POLICY AND PROGRAM OPTIONS ing legal impediments to the effective delivery of health services.
In an ideal world, policy and program options are based on a
Increase womens access to health and nutrition services
generally accepted, research-proven, conceptual framework that
has been tested in an appropriate environment. Unfortunately, Womens access to health and nutritional services could be
this has rarely been the case for prenatal nutrition in developing improved by designing delivery strategies to meet womens
countries. There is an urgent need to identify the conditions and needs; strengthening the health care delivery infrastructure;
circumstances under which prenatal undernutrition (eg, PEM or improving the quality of services for women; increasing the
specific micronutrient deficiencies) can be prevented throughout number of health care providers for women; and delegating
a womans reproductive cycle or improved during pregnancy, responsibilities to nonphysicians.
after which the appropriate strategy can be carefully shaped to
Other policy initiatives
the particular situation in each country or setting.
On the basis of the documents reviewed and of personal expe- Other policy initiatives include integrating women into
riences, the text that follows identifies some general and specific healthcare and nutrition planning via local health committees
policy (4) and program options that have either been shown to be and womens groups; strengthening collaboration with the pri-
effective or are likely to be effective, although there may be no vate sector through nongovernment organizations and for-profit
data to support the latter. More data are needed to show the providers; intensifying public education to promote the use of
effectiveness of programs under the specific conditions that are health services and healthy behaviors; advocating both policy
present in most developing countries. changes and behavior modification; meeting informational
needs on indicators of health status; designing programs based
on culture-specific health needs, formative research, and pro-
Policy options gram-based operations research; and monitoring and evaluating
programs.
Broaden policy support for enhanced investments in female
education Program options
Given the strong evidence associating higher levels of mater- Womens nutrition is expected to be equally or more strongly
nal education with improved child survival and nutritional status influenced by policies and actions intended to improve nutrition
(42) and very likely with better nutritional status of women in the entire household (eg, increased crop yields, higher
themselves, investment in the education of females is expected to income, food price subsidies, better nutrition knowledge, and
have enormous payoffs in health, nutrition, and development food fortification) than by those targeted solely at women. The
(43, 44). These effects are likely to be mediated through more- components that need to be considered in designing effective
efficient purchasing and intrahousehold distribution of food (45), community- and household-level programs that the health care
1358S MORA AND NESTEL

system can target toward women, with the emphasis on prenatal improve prenatal nutrition than are limited prenatal programs,
nutrition, are presented below. which are unlikely to begin early enough in pregnancy to have a
significant biological effect. For example, providing long-term
A comprehensive health and nutritional program preventive weekly iron or multivitamin and mineral supplements
The provision of regular health and nutritional services for to nonpregnant women, ideally beginning during adolescence, or
women requires a comprehensive program rather than single, implementing a widespread iron-fortification program may
isolated programs. Although framed in the context of a life cycle improve the iron reserves of these women to the extent that the
approach, such a program focuses on specific female life peri- need for preventive daily supplementation during pregnancy
ods: prepregnancy, pregnancy, delivery and lactation, early could be reduced significantly.
childhood, adolescence, and childbearing age. An important
Behavioral change programs
aspect is that appropriate information, education, and communi-
cation (IEC) aimed at key behavioral modifications for that life Behavioral change programs include expanded promotion of
period is given. The essential health and nutritional care program positive health and nutritional practices for females, including
includes the components that follow. behavioral changes to improve maternal, infant, and early child-
One important component is the prevention and management hood feeding and to eliminate self-inflicted female discrimina-
of unwanted pregnancies and management of abortion services tion. Most health and nutrition educational activities currently
by improving access to birth-spacing information and services, targeted toward women focus almost exclusively on child feed-
including counseling, education, and family planning. Signifi- ing, particularly breast-feeding. There is a need to redirect some
cant efforts are being made and substantial progress has been of the IEC efforts toward women themselves. Concrete efforts
achieved in several developing countries to reduce fertility and are needed to improve womens eating practices, which is impor-

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increase birth spacing (47). Family planning services still need tant for the health of the women themselves and for that of their
to be fully integrated with other health and nutritional services children, particularly in rural areas where women endure the
for women of childbearing age. IEC family planning strategies dual burden of moderate-to-high levels of physical work and fre-
need to incorporate womens health and nutritional concerns. quent pregnancies without noticeable increases in energy and
Existing service-delivery channels for contraceptive products nutrient intakes. Studies showed that female discrimination in
can be used effectively for the provision of iron supplements and developing countries may to a large extent be self-inflicted (48)
other nutritional services for women. as a result of a self-sacrificing role through which they meet
Another important component is expanded health and nutri- their own needs last. For example, increased female wages were
tional services for nonpregnant women, including adolescents. associated with improved nutrient intakes of most household
This has been a highly neglected area. Both the availability of members except the women themselves (49). IEC activities tar-
and the access to health services by women are often restricted geted toward women could be specifically designed to reduce
to prenatal and delivery services, often involving limited contact and ultimately remove these attitudes.
with health personnel, usually a few times during pregnancy and It is also important to delay childbearing among adolescents.
a few hours during delivery. Womens visits to health services, First births can be delayed by postponing the age of marriage
for either curative or preventive child health care, are excellent and the onset of sexual activity and by using effective methods
opportunities for health workers to tap and provide health and of family planning. This requires culturally sensitive IEC pro-
nutritional preventive services (education, counseling, and grams for changing individual and societal motivations for early
micronutrient supplements) to women. The delivery of micronu- childbearing and enhanced opportunities for formal education
trient and possibly even food supplements to female adolescents of girls.
through the school system can also be considered. Another crucial behavioral change is the removal of sex dis-
A third essential component of a health and nutritional care crimination. Enhancing the social status of women will require
program is enhanced maternity care that is effective, affordable, specific policies and intensive IEC efforts addressed at the pop-
accessible, and acceptable and that includes prenatal health and ulation as a whole and at women in the community, at schools,
nutritional services, safe delivery, and postpartum care. The and in the workplace.
well-documented increase in the coverage of prenatal services, The implementation of a comprehensive health and nutritional
currently > 50% in most developing countries (5), offers a unique program may not be feasible because of financial and resource
opportunity to reach women during pregnancy with a package of limitations. Although a comprehensive approach would be
health and nutritional services, including education and counsel- expected to lead to significant and sustainable improvements in
ing and micronutrient supplements. About a third of women in womens nutrition, and hence prenatal nutrition, a minimal pro-
these countries, however, still do not have access to good-quality gram can be tailored to the local situation in accordance with the
health services during pregnancy (Table 1) and childbirth, espe- resources available. It should be emphasized, however, that
cially poor and uneducated women who live in rural areas. nutritional programs that are restricted to the limited provision
Finally, a health and nutritional care program must include of health and nutritional services during pregnancy may not
extended nutritional assistance to vulnerable female groups to make a significant difference to the health and nutritional status
improve overall nutritional status, including supplementary feed- of the mother and the child.
ing, micronutrient supplements, and food fortification. Nutri-
A minimum health and nutritional program
tional assistance has usually been restricted to limited supple-
mentary feeding and the distribution of iron supplements to Given that financial and resource constraints frequently limit
pregnant women rather than to all women because of resource the number and scope of programs, the minimum package of
constraints. Providing a program of nutritional services to all key nutritional programs identified by Baker et al (50) was mod-
women of childbearing age may be a more effective way to ified and expanded to specify the programs required to improve
PRENATAL NUTRITION IN DEVELOPING COUNTRIES 1359S

the nutrition of adolescent girls and pregnant and lactating 2) Community- and facility-based health and nutritional care
women. The purposes of this minimum package are to delay first should be combined. The provision of health services alone
pregnancy, improve knowledge and practices related to repro- is not enough to improve womens nutrition. Community-
ductive health and nutrition, and improve access to quality pre- based programs can complement regular health services by
natal and postpartum services. focusing on nutritional monitoring and supplementation,
For adolescent girls, the following minimal programs are family planning, hygiene practices, infection prevention and
recommended: control, and identification and referral of complicated ill-
ness. Community health care providers, including commu-
1) improve access to family planning and reproductive health nity health committees, health workers, traditional birth
services; attendants and practitioners, and mobile outreach teams
2) provide nutritional education through schools, religious from health services, need to be trained, supervised, and
organizations, and marketplaces or workplaces and health supported by health service staff. Government policies and
promotion based on research that has identified cultural programs, however, are more likely to influence the cover-
and institutional constraints and detrimental attitudes and age and effectiveness of formal health and nutritional ser-
practices; vices than is the community-based care provided by
3) prevent and treat sexually transmitted diseases, parasites, and untrained community members and traditional practitioners
micronutrient deficiencies; and who are often the major source of advice and counseling on
4) provide supplementary food through school meals to induce nutrition and health care for women in developing countries.
growth catchup and maximize the pubertal growth spurt, 3) Public- and private-sector health and nutritional service-
increase school attendance, and serve as an excellent oppor- delivery systems should be combined. Despite the substan-

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tunity for health and nutrition education (51). tial improvement in health care coverage in recent decades,
the public health sector in most developing countries still
For pregnant and postpartum women, the recommended min- lacks the material and human resources required for provid-
imal programs can be categorized as service-delivery and health- ing sufficient health care coverage to most of the population,
promotion programs. The service-delivery programs 1) provide let alone to those at greatest risk of ill health and malnutri-
iron and folate supplements during pregnancy; 2) monitor preg- tion, who are often not easily accessible geographically and
nancy weight gain; 3) provide antimalarials, antihelminths, and economically. Compounding the limited number of service-
other micronutrient supplements, when appropriate, including delivery points is the fact that health and nutrition services
postpartum vitamin A in vitamin Adeficient areas; 4) provide in developing countries, particularly preventive services for
prompt diagnosis and treatment of illness; and 5) provide and women, are largely underused. This has been attributed to
target supplementary food to at-risk and undernourished women womens preference for seeking care from traditional health
by using appropriate indicators for screening, beginning as early care providers, poor accessibility to services, poor quality of
as possible during pregnancy. care, lack of information, relatively high costs, lack of
A review of randomized, controlled trials on the effectiveness of womens decision-making power and control of family
nutritional programs in pregnancy to reduce IUGR found that only income, and the opportunity cost of womens time (52).
balanced protein-energy supplementation was effective (3). The Although the removal of these constraints to increase the use
authors raised concern about the dearth of data to support recom- of health services by women is a clear priority, delivery
mended nutritional programs during pregnancy, some of which are channels outside the regular health care system need to be
used widely, even in women with no evidence of nutritional defi- identified and tapped (eg, traditional health care providers,
ciencies. Although this review was limited to the effects of pro- secondary schools, womens groups and cooperatives, and
grams on IUGR, it highlights the need for better monitoring and factories).
evaluation of prenatal programs and for further operations 4) Risk assessment should be used for targeting high-risk preg-
research on how to improve the nutrition of women in general. nancies so that appropriate referrals can be made. Risk
Health-promotion programs for pregnant and postpartum women assessment is seen as a logical tool for rationalizing service
1) provide nutritional, breast-feeding, family planning, and HIV delivery to ensure special care of those in need. Experience
counseling and disease prevention education, and 2) involve has shown, however, that a formal risk approach can be
men and other family members in behavior-modification activi- problematic and can divert scarce resources away from most
ties so that they increase the demand for health services for girls women with poor pregnancy outcomes. The World Health
and women. Organization (53) proposed that, because of the absence of
Ten actions are critical to effectively implement a package of data indicating the effectiveness of screening for high-risk
health and nutritional programs for women: pregnancies, risk assessment should not be relied on as the
sole basis for matching the requirements for and provision
1) Existing programs within health services should be inte- of maternity services. Because there are often several objec-
grated. By integrating nutritional programs within the health tives of risk assessments, it is difficult to develop a simple
service, complementary health care activities can be clus- tool as a panacea. It was shown, for example, that the effec-
tered at the same place and time, which will reduce service- tiveness of supplementary feeding to improve fetal growth
delivery costs for both the providers and the clients. There (birth weight) is greater when targeted at undernourished
are opportunities for better integration of all mother and pregnant women identified through anthropometric indica-
child health activities, child survival programs, supplemen- tors (54). Thus, anthropometric indicators can be useful if
tary feeding programs, safe motherhood, and family plan- birth weight is the outcome but will not be useful for identi-
ning and other reproductive health activities. fying women at risk of preeclampsia.
1360S MORA AND NESTEL

5) Health services should be organized by levels of care. Such delayed age of marriage, declining fertility rates, smaller fami-
a strategy is cost-efficient and improves the quality of care lies, longer life expectancy, greater health-system coverage, and
because the responsibilities at each level are thus more increased womens participation in the labor force. On the nega-
clearly defined and it allows for a functional bidirectional tive side, these global trends are characterized by severe resource
referral system (eg, severely anemic patients can receive constraints, slow economic growth, poor use of available health
specialized care and be referred to less-specialized care and nutritional services by females, and slow progress in
when appropriate). improving the social status of women in many countries.
6) Health personnel should be trained and motivated to deliver From a program perspective, possibly the most important fac-
nutrition services. Good quality services indicate that health tor favoring the implementation of enhanced health and nutri-
care providers have adequate clinical and counseling skills tional services for women is the ongoing trend toward increased
and are sensitive to womens needs. This requires appropri- coverage of maternal services. A recent analysis of demographic
ate initial training and periodic retraining and updating, as and health surveys conducted in 12 countries between 1986 and
well as a quality-based system that ensures that health care 1996 showed that, overall, the countries experienced a steady
providers and their supervisors are sufficiently motivated to increase in prenatal and delivery care coverage ranging from 2%
do a good job. to 34% for prenatal care, 2% to 39% for tetanus immunization,
7) IEC should be provided systematically. IEC is essential to and 3% to 79% for delivery care (59). However, prenatal care
any nutritional program and has 2 major purposes. The first coverage fell in 1 country and delivery care coverage declined in
is to disseminate information, sensitize the populace, and 3 countries. Quality of care was not assessed, which is important
mobilize both the providers and the recipients to support because it may not have improved significantly.
policies and programs aimed at enhancing the social status The challenges ahead are not insignificant. There is little doc-

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of women and the provision of health, nutritional, and edu- umentation on program experiences to improve prenatal nutri-
cational services to them. The second purpose is to promote tion, womens food intake, and weight gain during pregnancy in
individual behavioral changes to increase the use of and developing countries. It is disappointing to note that, despite the
demand for available health services for women and to research-based evidence that iron supplementation is efficacious,
improve womens and childrens eating and health practices. this relatively simple program was not effective in reducing the
Changing womens eating habits appears to be one of the prevalence of anemia in women and children (58, 60). Most iron
most difficult things to do and there is no evidence that and folate supplementation programs for pregnant women and
efforts to do so have been effective in the long term. young children have serious operational constraints related to
8) The cost-effectiveness of different programs and delivery supply and distribution systems, access to health care services,
systems should be analyzed. Cost-effectiveness analysis is motivation and behavior of health care providers, and compli-
an important tool for identifying the appropriate mix of pro- ance by the target population. Unresolved problems that affect
grams and service-delivery mechanisms that will achieve the acceptability of and compliance with supplements continue
specific nutrition objectives. For example, the generally to persist and include the lack of good-quality, low-cost generic
accepted view that prenatal care was strongly associated supplements; suitable compounds and dispensing mechanisms
with improved pregnancy outcomes in the early 1980s led to (tablets, pills, syrups, liquid forms, and powder); appropriate
the question of whether prenatal care was cost-effective. The regimens (daily or intermittent) for different environments (areas
ensuing US Institute of Medicines review showed that for of endemic malaria and helminth infection); and potential
every dollar spent on prenatal care, $3.38 was saved in direct adverse effects (real or overestimated).
medical care expenditures (55). Although there is little evidence that an iron-supplementation
9) Opportunities for promoting the nutritional status of adoles- program works, it remains one of the few options available for
cent girls should be identified. This is a relatively new, chal- improving the iron status of the population and appears to be the
lenging (but promising) area for which there are some small- only program likely to meet the high iron requirements during
scale but highly relevant experiences (56). As womens pregnancy and early childhood (23). Operations research is mov-
education improves, increased opportunities for programs ing toward testing systematic, intermittent supplementation of
targeted at adolescents through the school system will adolescent girls in schools and of nonpregnant women in the
become available. workplace to reduce the need for aggressive high-dose supple-
10) Basic supplies required for prenatal and delivery care should mentation, with its associated potential adverse effects and low
be improved. Good-quality care also requires that service compliance, during pregnancy. This approach, however, assumes
facilities have the necessary equipment and supplies, includ- that the most at-risk adolescent girls attend school and that
ing iron and folate supplements (57, 58). This is a frequently women work in organized work settings, which is not yet the
neglected area in developing countries that urgently needs case in most developing countries.
systematic attention. Regrettably, conceptual and implementational constraints
have minimized the effect of efforts to improve womens nutri-
tion, largely because the focus has been almost exclusively on
PROSPECTS AND CHALLENGES the prenatal period (50). Many programs were conducted as
The prospects for improving maternal nutrition are contingent small-scale research activities or vertical interventions or relied
on there being political commitment and national capacity to heavily on manipulating only the biological factors that influ-
develop and implement sound policies and programs. Policy ence womens nutrition. Such approaches are difficult to expand
decisions and program implementation will be affected by the because of the lack of broad-based support and demand for the
context of nutritionally relevant global trends that are character- services. Although, as emphasized above, efforts to improve
ized, on the positive side, by increased womens education, womens nutrition in a sustainable way must involve a life cycle
PRENATAL NUTRITION IN DEVELOPING COUNTRIES 1361S

perspective, the reality in most developing countries is that Understanding the physiologic and social adaptation
financial and resource constraints often reduce action to a few mechanisms during pregnancy
programs that tend to focus on pregnancy and, to a lesser extent, Evidence from several studies suggests that pregnant women
lactation. A stronger political commitment is needed to support subsisting on limited energy intakes adapt to this situation
womens health and nutritional programs and to create the through a physiologic reduction in their basal metabolic rate or a
demand for a minimum package of services. reduction in activity to conserve energy for fetal growth (66).
These mechanisms affect the use and interpretation of nutritional
Major challenges indicators during pregnancy and the guidelines on energy intakes
to sustain adequate weight gain. Irrespective of the physiologic
Translating current knowledge into practice adaptations of the body, Naeye (67) showed that a womans nutri-
It will be a major challenge to translate current knowledge tional store as she enters pregnancy is a more important determi-
into practical application in the context of resource constraints in nant of perinatal mortality than is pregnancy weight gain per se.
developing countries, ie, to move from theory to practice in a Reducing persistent problems with health service development
resource-limited setting. Baker et al (50) identified conceptual and access to quality prenatal care services
and implementational constraints to improvements in female
nutrition that will need to be addressed if womens nutrition is to Prospects for steady increases in the availability of and access
improve. The conceptual constraints include a consistent lack of to quality health services for women in developing countries are
political support for womens nutrition, nutritional programs uncertain given current financial constraints. However, great
narrowly focused on pregnant women, nutritional programs usu- efforts have been made toward improving the efficiency of health
ally designed as pilot projects or small-scale research activities, care expenditures, enhancing coverage within existing resource

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lack of a consensus on the most appropriate and practical indi- constraints and, to a much lesser extent, improving access for
cators of womens nutrition, and lack of information on the cost- poor, uneducated women, especially those in rural areas.
effectiveness of programs. The implementational constraints, Problems with access to and quality of prenatal care services,
which are common to health programs, include limited service- however, are not exclusive to developing countries. In an attempt
delivery capacity and low use of existing services, poor program to understand the poor standing of the United States in the inter-
management, limited focuses on behavioral factors and behav- national rankings of infant mortality rates, a recent situation
ioral change, and inadequate training of health personnel. analysis identified the need for increasing access to prenatal care,
redirecting the content of prenatal care, understanding the behav-
Determining definitions of prenatal nutrition and undernutrition iors of pregnant and lactating women, and facilitating changes in
in women the delivery of nutritional care (68). The new guidelines for the
delivery of nutritional care issued by the US Institute of Medicine
Another major challenge will be to develop acceptable, bio- (69) address the predisposing factors that inhibit health profes-
logically meaningful and programmatically relevant definitions sionals from including nutritional care in their practices, empha-
of prenatal nutrition and undernutrition in women by using size a more culturally sensitive approach to care, and recommend
anthropometric, dietary, and biochemical indicators. This is criti- new tools for screening and targeting prenatal programs.
cal for problem definition, risk identification, program targeting, Womens nutrition remains a global issue with common prob-
and monitoring and evaluation. Current indicators include anemia lems and constraints that will be resolved only if womens health
rates (based on hemoglobin concentration) and womens height, and nutrition are put in the context of the life cycle rather than
weight and weight gain, body mass index, and midupper arm cir- into discrete compartments. This approach includes addressing
cumference (61, 62). There is no general consensus, however, on the underlying social and cultural determinants of behaviors con-
the use and interpretation of anthropometric indicators in preg- nected to womens nutrition at all stages of the life cycle.
nant and nonpregnant women (15, 63, 64). Guidelines on the
application of anthropometric indicators emphasize the use of We thank Leslie Elder and Ritu Nalubola for their comments and sugges-
these indicators as screening tools rather than for surveillance, tions on an earlier draft of the article.
and instruments designed for the latter purpose are pending satis-
factory validation. A related question that needs to be addressed
is the identification and interpretation of maternal undernutrition REFERENCES
in poor communities in which a relatively large proportion of 1. Tinker A, Koblinsky MA. Making motherhood safe. Washington,
women are short but overweight (eg, in parts of Latin America), DC: World Bank, 1994. (World Bank discussion paper 202.)
yet indicators of pregnancy outcomes also are not optimal. 2. Leslie J. Womens nutrition: the key to improving family health in
developing countries. Health Policy Plan 1991;6:119.
Allaying womens concerns about weight gain and delivery 3. De Onis M, Villar J, Gulmezoglu M. Nutritional interventions to
complications prevent intra-uterine growth retardation: evidence from randomized
control trials. Eur J Clin Nutr 1998;52(suppl):S8393.
A review of research from 18 developing countries on changes
4. Tinker A, Daly P, Green C, Saxenian H, Lakshminarayanan R, Gill
in dietary practices during pregnancy found that food intake is
K. Womens health and nutrition: making a difference. Washington,
consciously restricted during pregnancy because of the fear of
DC: World Bank, 1994. (World Bank discussion paper 256.)
delivery complications associated with having a large newborn 5. World Health Organization. Coverage of maternity care: a listing of
(65). Although this concern is rational, there are no data to sup- available information. Geneva: World Health Organization, 1997.
port it. Restricted food intake by pregnant women can compro- (WHO/RHT/MSM/96.28.)
mise their nutritional status and needs to be addressed through 6. McGuire J, Popkin BM. Beating the zero-sum game: women and
behavioral change programs, when appropriate. nutrition in the third world. Part I. Food Nutr Bull 1989;11:3863.
1362S MORA AND NESTEL

7. Black AK, Allen LH, Pelto GH, de Mata MP, Chavez A. Iron, vitamin eds. Protein energy malnutrition in third world children. London: E
B-12 and folate status in Mexico: associated factors in men and Arnold of Hodder Stoughton Ltd, 1992:34460.
women and during pregnancy and lactation. J Nutr 1994;124:117988. 30. Bhatia D, Seshadri S. Growth performance in anemia following iron
8. Jellife DB. The assessment of the nutritional status of the commu- supplementation. Indian Pediatr 1993;30:195200.
nity. Geneva: World Health Organization, 1966. 31. Martorell R, Kettel Khan L, Schroeder DG. Reversibility of stunt-
9. Jellife DB, Maddocks I. Ecological malnutrition in the New Guinea ing: epidemiological findings from children from developing coun-
highlands. Clin Pediatr 1964;3:4328. tries. Eur J Clin Nutr 1994;48(suppl):S4557.
10. Merchant KM, Martorell R. Frequent reproductive cycling: does it 32. World Health Organization. Maternal anthropometry and pregnancy
lead to nutritional depletion of mothers? Prog Food Nutr Sci outcomes: a WHO collaborative study. Bull World Health Organ
1988;12:33969. 1995;73(suppl):198.
11. World Health Organization/United Nations Childrens Fund. Revised 33. Bruner AB, Joffe A, Duggan AK, Casella JF, Brandt J. Randomized
1990 estimates of maternal mortality: a new approach by WHO and study of cognitive effects of iron supplementation in non-anemic
UNICEF. Geneva: WHO, 1996. (WHO/FRH/MSM/96.11.) iron-deficient adolescent girls. Lancet 1996;348:9926.
12. Population Reference Bureau. Women of our world. Washington, 34. Barker DJP. Mothers, babies and disease in later life. London: BMJ
DC: Population Reference Bureau, 1998. Publishing Group, 1994.
13. Royston E, Armstrong S. Preventing maternal deaths. Geneva: 35. Leon DA. Fetal growth and adult disease. Eur J Clin Nutr
World Health Organization, 1989. 1998;52(suppl):S7282.
14. Loaiza E. Maternal nutrition status. Demographic and health survey 36. World Health Organization. Global prevalence of vitamin A defi-
comparative report no. 24. Calverton, MD: Macro International, Inc, ciency. Micronutrient Deficiency Information System (MDIS)
1997. working paper no. 2. Geneva: World Health Organization, 1995.
(WHO/NUT/95.3.)
15. James WPT, Ferro-Luzzi A, Waterlow JL. Definition of chronic
37. International Vitamin A Consultative Group. Maternal night-blind-
energy deficiency in adults. Report of a working party of the Interna-

Downloaded from ajcn.nutrition.org by guest on September 5, 2017


ness: extent and associated risk factors. Washington, DC: ILSI
tional Dietary Consultative Group. Eur J Clin Nutr 1988;42:96981.
Press, 1997.
16. Merchant KM, Kurz KM. Womens nutrition through the life cycle:
38. Katz J, Khatry SK, West KP Jr, et al. Night blindness during preg-
social and biological vulnerabilities. In: Koblinsky M, Timyan J,
nancy and lactation in rural Nepal. J Nutr 1995;125:21227.
Gay J, eds. The health of women: a global perspective. Boulder, CO:
39. DeMaeyer E, Adiels-Tegman M. The prevalence of anemia in the
Preview Press, 1993.
world. World Health Stat Q 1985;38:30216.
17. Martorell R, Rivera J, Kaplowits H, Pollitt E. Long-term consequences
40. United Nations. Second report of the world nutrition situation:
of growth retardation during early childhood. In: Hernandez M,
global and regional trends. Vol 1. A report compiled from informa-
Argente J, eds. Human growth: basic and clinical aspects. Amsterdam:
tion available to the United Nations and the ACC/SCN. Geneva:
Elsevier, 1992.
ACC/SCN, 1992.
18. Scholl TO, Hediger ML. Anemia and iron-deficiency anemia: compilation of
41. Mora JO, Mora OL. Micronutrient deficiencies in Latin America
data on pregnancy outcome. Am J Clin Nutr 1994; 59(suppl):492S500S. and the Caribbean. Washington, DC: US Agency for International
19. Adair LS. Nutrition in the reproductive years. In: Johnson FE, ed. Development, PAHO/WHO, 1999.
Nutritional anthropology. New York: Alan R Liss, 1987. 42. Cleland J, van Ginneken J. The effect of maternal schooling on
20. Lechtig A, Shrimpton R. Maternal nutrition: what relevance for childhood mortality: the search for an explanation. Voorburg, Nether-
childrens survival and development? In: Kretchmer N, Quilligan lands: International Statistical Institute, 1987.
EJ, Johnson JD, eds. Prenatal and perinatal biology and medicine. 43. Behrman JR, Wolfe BL. How does mother schooling affect the fam-
Chur, Switzerland: Harwood Academic Publishers, 1997:93160. ilys health, nutrition, medical care usage, and household sanita-
21. Chatterjee M, Lambert J. Women and nutrition reflections from tion? J Econometrics 1987;36:185204.
India and Pakistan. Food Nutr Bull 1989;11:138. 44. Behrman JR, Wolfe BL. Does more schooling make women better
22. Lettenmeier C, Liskin L, Church C, Harris J. Mothers lives matter: nourished, and healthier? Adult sibling random fixed effect esti-
maternal health in the community. Popul Rep 1989, Series L, no. 7. mates for Nicaragua. J Hum Resour 1989;24:64463.
23. Viteri FE. The consequences of iron deficiency and anemia in preg- 45. Hamilton S, Popkin B, Spicer D. Women and nutrition in third
nancy. In: Allen L, King J, Lonnerdal B, eds. Nutrient regulation world countries. South Hadley, MA: Bergin and Garvey Publishers,
during pregnancy, lactation, and infant growth. New York: Plenum 1984.
Press, 1994:12740. 46. Soysa P. Women and nutrition. World Rev Nutr Diet 1987;52:170.
24. De Onis M, Bloosner M, Villar J. Levels and patterns of intrauterine 47. Arnold F, Blanc AK. Fertility levels and trends. Demographic and
growth retardation in developing countries. Eur J Clin Nutr health surveys comparative studies, no. 1. Calverton, MD: Macro
1998;52(suppl):S515. International, Inc, 1990.
25. World Bank. Investing in health: world development indicators. 48. Holmboe-Ottesen G, Mascarenhas O, Wandel M. Womens role in
Washington, DC: World Bank, 1993. food chain activities and the implications for nutrition. Geneva:
26. Scholl TO, Hediger ML, Ances IG. Maternal growth during preg- World Health Organization, 1989. (ACC/SCN state-of-the-art series
nancy and decreased infant birth weight. Am J Clin Nutr 1990; nutrition policy discussion paper no. 4. 1989.)
51:7903. 49. Behrman JR, Deolalikar AB. The intrahousehold in rural India: indi-
27. Martorell R, Ramakrishnan U, Schroeder DG, Melgar P, Nenfeld L. vidual estimates, fixed effects and permanent income. J Hum
Intrauterine growth retardation, body size, body composition and Resour 1990;25:66596.
physical performance in adolescence. Eur J Clin Nutr 1998; 50. Baker J, Martin L, Piwoz E. The time to act: womens nutrition and
52(suppl):S4353. its consequences for child survival and reproductive health in Africa.
28. Nokes C, van den Bosch C, Bundy DAP. The effects of iron defi- Washington, DC: US Agency for International Development, SARA
ciency and anemia on mental and motor performance, educational Project, 1996.
achievement, and behavior in children: a report to the Interna- 51. United Nations Childrens Fund, World Health Organization Joint
tional Anemia Consultative Group. Washington, DC: ILSI Press, Committee on Health Policy. WHO-UNICEF strategy for improved
1998. nutrition of mothers and children in the developing world. Geneva:
29. Grantham-McGregor SM. The effect of malnutrition on mental World Health Organization, 1989. (JC27/UNICEF-World Health
development. In: Waterlow JC, Grantham-McGregor SM, Tomkins A, Organization/89.4.)
PRENATAL NUTRITION IN DEVELOPING COUNTRIES 1363S

52. Leslie J, Rao Gupta G. Utilization of formal services for maternal 61. Institute of Medicine Committee on Nutritional Status During Preg-
nutrition and health care in the third world. Washington, DC: Inter- nancy and Lactation. Washington, DC: National Academy Press,
national Research Center for Research on Women, 1989. 1990.
53. World Health Organization. Safe motherhood information kit: 62. Galloway R, Cohen A, eds. Indicators for reproductive health pro-
World Health Day. Geneva: World Health Organization, Division of gram evaluation: final report of the subcommittee on womens nutri-
Reproductive Health, 1998. tion. Washington, DC: US Agency for International Development,
54. Herrera MG, Mora JO, de Paredes B, Wagner M. Maternal weight/- Evaluation Project, 1995.
height and the effect of food supplementation during pregnancy and 63. Rasmussen KM, Habicht JP. Malnutrition among women: indicators
lactation. In: Aebi H, Whitehead R, eds. Maternal nutrition during preg- to estimate prevalence. Food Nutr Bull 1989;11:2937.
nancy and lactation. Vienna: Hans Huber Publishers, 1980:25263. 64. World Health Organization. Maternal anthropometry for prediction
55. Institute of Medicine Committee to Study Outreach for Prenatal of pregnancy outcomes: memorandum from US Agency for Interna-
Care. Prenatal care: reaching mothers, reaching infants. Washing- tional Development/WHO/PAHO/MotherCare meeting. Bull World
ton, DC: National Academy Press, 1988. Health Organ 1991;69:52332.
56. Kurz KK, Peplinsky NL, Johnson-Welch C. Investing in the future: 65. Brems S, Berg A. Eating down during pregnancy: nutrition,
six principles for promoting the nutritional status of adolescent girls obstetric and cultural considerations in the third world. Discussion
in developing countries. Washington, DC: International Center for paper prepared for the ACC/ACN. Washington, DC: World Bank,
Research on Women, 1994. Population, Health and Nutrition Division, 1988.
57. Gillespie S, Kevany J, Mason J. Controlling iron deficiency. 66. King JC, Butte NF, Bronstein MN, Kopp LE, Linquist SA. Energy
Geneva: United Nations ACC/SCN. (ACC/SCN state-of-the-art metabolism during pregnancy: influence of maternal energy status.
series nutrition policy discussion paper no. 9.) Am J Clin Nutr 1994;59(suppl):439S45S.
58. Galloway R, McGuire J. Determinants of compliance with iron sup- 67. Naeye RL. Weight gain and the outcome of pregnancy. Am J Obstet
plementation: supplies, side effects of psychology. Soc Sci Med Gynecol 1979;135:39.

Downloaded from ajcn.nutrition.org by guest on September 5, 2017


1994;39:38190. 68. Olson CM. Promoting positive nutritional practices during preg-
59. Stewart MK, Stanton CK, Ahmed O. Maternal health care. Demo- nancy and lactation. Am J Clin Nutr 1994;59(suppl):525S30S.
graphic and health surveys (DHS) comparative studies no. 25. 69. Subcommittee on a Clinical Application Guide, Committee on
Calverton, MD: Macro International, Inc, 1997. Nutritional Status During Pregnancy and Lactation. Nutrition dur-
60. Yip R. Iron supplementation during pregnancy: is it effective? Am J ing pregnancy and lactation: an implementation guide. Washington,
Clin Nutr 1996;63:8535. DC: National Academy Press, 1992.

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