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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-
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
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
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.
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;
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-
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-
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-
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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