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GAPS IN KNOWLEDGE

Gaps in Knowledge Related to Maternal Nutrition

Nutrition Prior to Pregnancy

There is evidence that marginally nourished women entering pregnacy have a greater risk of impaired reproductive performance than better nourished women in similar settings. It would appear that the risk is even more critical in young adolescents. However, the mechanisms of the interaction of stunting as a result of past undernourishment and of maternal and infant risk (particularly in girls less than 16 years of age) are poorly defined. Specific physiological and operational research questions associated with chronic undernutrition and stunting, and with early pregnancy in general, include the following:
- Is pelvic growth in adolescence a critical issue in reproductive risk among stunted populations?
- Are dystotic deliveries (deliveries with difficult labour) more common among these populations, and if so, why?
- Can effects of chronic undernutrition on height and lean body mass persisting into adolescence be ameliorated by improved dietary intake during adolescence or later on in life?
- Is increased gynaecologic age (time after menarche) a favourable factor for a successful pregnancy among these women? If so, the following operational research questions arise:

i. Can socio-cultural interventions that encourage delaying pregnancy be effective in improving reproductive performance and in reducing the number of pregnancies at an early reproductive age?
ii. How important as a means to encourage delaying early pregnancy are social support systems and the perceived value of women by the family and community?
iii. How effective in delaying pregnancy and improving reproductive performance and infant health are measures directed toward encouraging community and family support compared with direct nutrition interventions?
iv. In this context, how effective in reducing risks for a next pregnancy is food supplementation during pregnancy and lactation compared with simple birth-spacing?
v. What is the relative benefit of improved prenatal care exclusive of direct food supplementation in improving reproductive performance of adolescents?
vi. What are the impediments to obtaining improved prenatal care and increasing its coverage?

Another major gap in our understanding of nutrition as a preparation for pregnancy is that there is no clear definition of optimal pre-pregnancy nutritional status. Therefore the effect of interventions often is difficult to determine.

Nutrition during Pregnancy and Lactation

Fundamental gaps still exist in our knowledge of the interplay between the processes of physiological adaptation to pregnancy and lactation and mild to moderate nutrient (and energy) deficiencies and/or the demanding life-styles of many agricultural societies. These gaps, for example, are reflected in the relatively scarce data upon which to base nutrient (and energy) requirements during pregnancy and lactation and to determine their normal variability under usual living conditions of developing populations.

In this section gaps in knowledge have been categorized according to whether they primarily concern physiological mechanisms (a-g) or operational aspects of interventions (h-m). The subcommittee believes that priorities for operational research and specific operational constraints are determined by local situations. Therefore, items hem present general operational research questions that must be further refined and adapted to local conditions and priorities. The following are priority questions related to physiological mechanisms.

a. What are the limits of normality for healthy pregnant and lactating women for both maternal and foetal wellbeing? What is the basis for interpreting changes in the levels of nutrients and other substances in maternal and foetal circulation? Is there a point at which these changes warrant nutritional intervention? Can changes in nutrient levels be useful in monitoring pregnancy and lactation? What energy, protein, and other nutrient reserves are adequate to ensure satisfactory foetal development in the face of various levels of dietary inadequacy during pregnancy? Conversely, what threshold in calorie or protein consumption must be surpassed in order to translate increments in maternal dietary intake into increments in birth weight?

b. What is the effect of physical activity on weight gain and outcome of pregnancy throughout the range of maternal dietary intakes? Specifically:
- Are there harmful effects of physical activity? If so, do they occur throughout pregnancy and lactation, or are certain periods more vulnerable?
- Could increased dietary intake provided by food supplements negate any harmful effects of increased physical activity?
- Are there benefits to continued activity with adequate dietary intakes?
- Can reproductive performance be improved by reducing physical activity when the dietary intake is marginal? Again, are there time constraints?
- Ate there synergistic beneficial effects of increased food intake and reduction in activity? If so, at what point(s) during pregnancy and lactation do these effects occur?

c. What are the mechanisms by which maternal dietary deficits limit transfer of nutrients to the foetus? If blood volume expansion is a critical factor, could such measures as high haemoglobin and haematocrit and absence of hand/facial oedema be used in field settings as indicators of insufficient blood volume expansion? Are there practical measures that can be used in conjunction with nutritional interventions to overcome insufficient transfer of nutrients?

d. If the "normal" ketogenic response to fasting and to negative energy balance is exaggerated during pregnancy, does it have a deleterious effect on the foetus and/or on "normal" mechanisms of labour and delivery? Could ketonuria be a sensitive indicator of energy deficit during pregnancy (operational)?

e. Are the mechanisms by which fatty acids become a more important source of metabolic fuel during pregnancy particularly liable to fail because of infection, thus inducing rapid and acute metabolic energy deficits? Could simple dietary recommendations be conceived to reverse this effect if it exists?

f. Does lactation create special conditions that influence the course and severity of infection? What is the prevalence of mastitis and its impact on the health status of poorly nourished women?

g. Does maternal nutritional status influence a woman's capacity to lactate sufficiently to support her infant's catch-up growth following an infectious episode? In situations where dietary intake is often inadequate, does long-term lactation deplete maternal reserves and affect such factors as pregnancy outcome, maternal quality of life and health, and parenting ability? What is the impact of cultural lactation food restrictions or dietary changes in general on maternal health?

The following priority questions are related to operational (programme-related) aspects of interventions aimed at improving nutrition and health during pregnancy and lactation.

h. What combination of socio-economic and biological risk factors can be used for identifying target populations and monitoring and evaluating interventions? Although sufficient evidence exists to identify some risk factors for pregnant women (see "Nutrition during Pregnancy" above and "General Guidelines" below, as well as reference 126), more methodological/statistical research is needed, for example, to determine best combinations of risk factors for specific purposes. Furthermore, although a number of risk factors have been identified (126), the characteristics (sensitivity, specificity, predictive value) of these factors as indicators of nutritional status of populations and their appropriate uses given different purposes (assessment, monitoring, evaluation) require further study. Until this is done the definition of groups at risk, the institution of potentially effective nutritional interventions, and the evaluation of their impact are hampered (1271 29).

i. What is the cause of maternal complications during the perinatal period (prepartum, labour and delivery, puerperium)? Are there interactions between general nutritional status and/or specific nutrient deficiencies and infection? Are specific behavioural factors and practices prior to, during, and immediately after delivery responsible for complications? What is the predominant cause of complications during delivery? Is dystocia (difficult labour and delivery) a common event and, if so, why? The whole issue of pelvic growth and previous nutrition becomes very relevant in this regard.

j. What is the contribution of specific nutrient deficiencies during pregnancy to pregnancy outcome? In the case of zinc in particular, how can its deficiency be diagnosed during pregnancy? Can improved zinc nutritional status improve defence mechanisms during pregnancy? Can it reduce the frequency of chorioaminonitis and preterm delivery? If so, can zinc supplementation to pregnant women reduce the frequency of these complications without harmful side effects?

k. What are the effects of introduction of complementary foods and of maternal nutritional status on the duration of postpartum anovulation and fertility? Are these effects independent? Synergistic? Do low-dose oestrogen-containing oral contraceptives have a reproducible negative effect on milk quality and quantity and on infant growth? If so, is it of public health significance?

l. What standardized nutrition research methodology and documentation on pregnant and lactating women are required for accurate interpretation and comparison of research during pregnancy? Much of the controversy about the evidence for a detrimental effect of maternal malnutrition on foetal well-being stems from the use of different methodological approaches. Wide differences exist in the severity and character of maternal malnutrition among the groups investigated. These discrepancies are particularly large when comparison is made between industrialized and less developed countries. Surveys have been carried out at different times during pregnancy, and the methods used have not had the same level of precision. The subjects investigated have not always been comparable. In most instances, account has not been taken of these and many other important intervening variables.

m. What are the minimal needs for prenatal care within different human ecological settings? What risk factors are most useful in defining target populations for prenatal care given specific local conditions? Within different cultural settings, what determines the attendance to prenatal care and to delivery in an institution or at home assisted by obstetrically trained personnel?

Gaps in Knowledge Related to Infant and Young Child Nutrition

Although understanding of physiological and biochemical mechanisms related to infant and child nutrition is by no means complete, there is a core of basic knowledge in such areas as breastfeeding, complementary foods, weanling diarrhoea, and growth monitoring upon which interventions can be designed. A number of operational impediments to application of basic knowledge still exist, however.

Therefore, in this section the subcommittee has focused primarily on programme-related (operational) questions, although in some cases operational and physiological questions overlap.

a. The incidence and duration of breast-feeding are declining in populations undergoing transculturation (urbanization, modernization). There are complex reasons for the decline, but changes in the environment, especially the socio-cultural environment, are important (130, 131). Given its importance for infant health, development of effective actions to promote breast-feeding under these conditions is important. This requires more knowledge than currently exists of socio-cultural determinants of breast-feeding practices.

b. In low socio-economic groups in developing countries, what is the growth pattern of fully breast-fed infants during the period when growth appears to proceed normally? How long is this time? What determines the length of the period of adequate growth for individual infants? That is, what are the determinants of growth faltering? Is it due to differences in milk yield and composition? Intercurrent infection? Synergism between breast-milk intake and infection? Are there other possible functional impairments that precede or accompany a decrease in growth velocity?

c. The contribution of complementary foods to a shortening of the duration of breast-feeding is still poorly understood. Questions that need to be answered include: - Is there a ratio of food to breast milk that is optimal for infant growth and maintenance of breast-feeding? - Is there a frequency and sequence of feeding semi-solid complementary food and breast milk that is optimal for infant growth and maintenance of breast-feeding? Preliminary observations indicate that offering semi-solid complementary foods shortly before offering liquid formula or human milk increases the amount of the liquid consumed or at least does not decrease it (Viteri, personal communication). This may occur because the semisolid food does not have the thirst-quenching (water electrolyte) effect of the liquid milk. These findings are contrary to conventional wisdom, which advocates breastfeeding before offering semi-solid foods and, if validated, will have significant practical implications. - Experience suggests that complementary foods should be introduced when an infant is between 4 and 6 months old (121). However, the evidence for beneficial or harmful effects on infant health and nutritional status of introducing foods to infants from low socio-economic groups at 3-4 rather than 5-6 months is insufficient to make a sound pronouncement on the issue. Such results are especially relevant for women who must be away from their infants for large parts of the day or night.

d. Once an infant or young child suffers from diarrhoea and is being rehydrated by mouth or parenterally, what should the child be fed? How should different foods be prepared and how should they be offered to the child? Current practice advises mothers to feed their babies early in these circumstances, although not much is known in this area. Much less is known about the appropriate regimen that will allow catch-up growth or nutritional repletion after diarrhoea. Intensive feeding during or immediately after acute infections (5 to 7 days) may lead to catch-up growth (as seen in malnourished children) with growth rates reaching three to five times normal in spurts of a few days. Studies of intensive feeding in convalescence, including the role and capacity of breast-feeding, are certainly a promising area of inquiry. Whether extensive feeding is practical at the community level is a separate question that must also be answered.

e. Growth monitoring can be a key tool to early detection and effective preventive action to avoid protein-energy malnutrition. However, the practical aspects of frequent weighings of infants and children to monitor their growth and nutrition and to determine feeding pattern sequences need documentation and careful evaluation. Also required are development of communication techniques to ensure that mothers understand growth-i.e., better comprehend the importance and meaning of weight gain and loss (e.g., weight chart, other means of "seeing" growth)-and investigation of alternative monitoring technologies (e.g., is arm circumference a simpler tool than weight or height?).

f. The design and implementation of effective interventions (educational, food supplementation, etc.) have been hampered by lack of knowledge of determinants of intrahousehold distribution of foods in health and disease and specific ways the distribution of food negatively affects the small child. Closely related to this gap in knowledge are concurrent gaps in understanding factors that influence appetite, satiety, thirst, and anorexia in infants and children.

g. There are strong suggestions that "early bonding" may improve breast-feeding and promote health of infants (132). The evidence, however, is not yet sufficient to dictate policies of infant and perinatal care in areas where early bonding is not routinely practiced. In this regard, and in general, maternal education has been shown to be inversely related to infant mortality (133). However, there is inadequate evidence to determine whether infant nutrition and health will improve if mothers are taught about early bonding or about such feeding practices as simple techniques for home-made preparation of complementary or weaning foods combined with general hygiene.

RECOMMENDATIONS

Recommendations for Research

The subcommittee considers all the gaps in knowledge outlined in the preceding section to be important research priorities. From among those the subcommittee has identified four issues of particular urgency and recommends that research required to address those issues receive highest priority. These four research priorities are listed below.

1. Investigation of the mechanisms of the interaction between physical activity and (a) weight gain during pregnancy, (b) pregnancy outcome, and (c) lactation performance and of the implications for interventions. This is a particularly important issue in areas where women routinely engage in labour-intensive activities. Specific research questions are posed in "Nutrition during Pregnancy and Lactation," paragraph b, above.

2. Determination of causes of perinatal complications (including culturally determined practices), particularly in relation to stunting and other growth maturation alterations associated with previous and present nutritional status. Determination of the contribution of specific nutrient deficits, infection, and their possible synergism (or interaction) as a cause of perinatal complications and poor pregnancy outcome (prematurity, low birth weight). Specific questions are posed in "Nutrition Prior to Pregnancy" and in "Nutrition during Pregnancy," paragraphs i and j, above.

3. Selection and application of risk factors to identify communities, families, and persons at risk under different human ecologies (and those who will benefit from intervention). Specific research questions are posed in "Nutrition during Pregnancy," paragraph h, above.

4. Development and evaluation of safe, feasible, and acceptable complementary feeding and weaning practices. This is discussed in "Nutrition of Infants and Young Children," and specific questions are posed in "Gaps in Knowledge Related to Infant and Young Child Nutrition," paragraph c, above.

The task of setting overall priorities for research in developing countries is complicated by the fact that demographic, socio-cultural, economic, and general development characteristics and trends vary. Thus what may be a clear priority in one setting may be relatively unimportant in another. In addition, the opportunity to carry out pertinent research may influence the choice of priority topics and timing of their implementation. The human and operational resources available to accomplish what is considered of high priority are also important considerations. This last consideration is particularly important if the necessary studies are to be conducted in a developing country by, or at least in active collaboration with, local scientists and institutions. The subcommittee considers that one essential component in such collaboration should be to strengthen the research and overall scientific capability of the host country as permitted by the project. When necessary, efforts should be undertaken to remove manpower and material constraints, e.g., by providing scientific training to ensure adequate local expertise in selected research areas.

Recommendations for Intervention

Although epidemiologic data in developing countries are often not precise enough to estimate the prevalence of malnutrition, and evidence is insufficient to understand precise biochemical or physiological mechanisms and adaptations involved in the pathogenesis of disease and malnutrition, the subcommittee, on the basis of this review and their collective experience, is convinced that actions still can be taken within the broad context of health care that will improve the nutrition and health of women and young children in developing countries. Thus, this section presents guidelines for interventions that reflect current knowledge and experiences in pertinent nutritional aspects of maternal and child populations. The general recommendations outlined in this section should form the basis of actions and should be modified as gaps in knowledge are removed and additional experience is gained

General Guidelines

The subcommittee recommends that nutrition and health interventions should form a single unit and be congruent with the general scheme of development for a target population. Unless very powerful operational obstacles exist, an intervention should have the following characteristics:
- The community should participate in its operation, with adequate technical input and supervision.
- The intervention should be aimed at the family.
- The intervention should be an integral part of a strategy of primary health care (as defined by WHO) that actually involves other sectors in addition to health (134).
- The intervention should integrate nutrition care with infection control and family planning.
- The intervention should be adapted to the prevailing local human ecological characteristics, including health care facilities, environmental conditions, cultural concepts, agricultural and food practices and beliefs, etc.

The aim should be that what begins as a well-designed intervention will eventually become a well-established community activity supported within the community.

The relative scarcity of resources, coupled with the concept that nutrition and health interventions should be directed to communities and families who most require them, immediately leads to a "risk approach." A risk approach involves selecting communities, families, or persons for intervention on the basis of characteristics associated with a higher probability of malnutrition and poor health. To implement such an approach effectively, valid, simple surveillance and survey methods adapted to local human ecological settings are essential.

If an intervention is community-based, there are three alternatives: (a) to include the entire population, (b) to include only families with one or more individuals at risk, or (c) to include only individuals at risk. In every case a determination should be made of the severity and extent of risk in the community. The alternative selected depends, in principle, on existing characteristics, feasibility, cost-effectiveness, and type of operational systems that would ensure maximum coverage of the target population.

The choice of the target population hinges on the definition of communities, families, or individuals at risk who would benefit from a specific intervention, or from several interventions, in terms of improved health and reduction in specific risks related to reproduction and growth and development. In general it is preferable to consider the community and the family as the targets for intervention rather than only children under five years of age and pregnant and lactating women.

Based on the evidence reviewed in previous sections of this document, a number of factors are proposed as examples of criteria to define a family at risk. In some cases these criteria may also identify individuals or communities at risk. These are suggested risk factors only. More methodological research is needed, using scaling techniques, for example, to determine the best combination of factors to identify those at risk.

Suggested risk factors include:

- previous reproductive failure and history of low-birth weight deliveries;
- low prepregnancy weight (and, in some cases, height);
- poor weight gain during pregnancy; inadequate mean monthly weight gain during pregnancy;
- complications of pregnancy (bleeding, hypertension, urinary infections);
- pregnancy below 17 years of age;
- presence of malnourished members in the family;
- engagement of women and children in hard physical labour;
- low socio-economic status and little education of women;
- poor parental experience, inadequate social support systems, and negative feelings toward present pregnancy;
- alcohol abuse;
- smoking or smoke exposure (environmental conditions leading to hypoxia in mothers and children);
- family in a community where infant and early childhood mortality rates are above the median for the country or region;
- community undergoing natural or man-made crisis or disasters (unemployment, drought, migration, war, etc.);
- poor system of preventive and curative health care;
- limited availability of foods (in variety, quantity, and quality-by season).

The following short sections provide additional guidelines on specific aspects of the recommendations.

Actions Prior to and between Pregnancies

The subcommittee agrees that the health and nutritional status of pregnant and lactating women must be monitored and, if necessary, improved. In addition, the subcommittee suggests that the aim should be to ensure optimal health and nutrition for women before as well as when they become pregnant and recommends adoption of actions to achieve this aim. For example, the social and economic rights of a woman and her participation as an active member of the family and society should be considered in the design of interventions, as should her right to be well-nourished, healthy, and educated. Attainment of satisfactory nutritional status by changing intra-household food distribution practices so that women and young children obtain a fairer share should also be considered when planning interventions.

A special case is posed by societies where teenage pregnancies and high parities are common. Efforts should be made to provide adequate prenatal care and to bring teenagers into the system to receive such care. Where feasible, and particularly where prenatal care is limited, efforts should be made to delay the first pregnancy, ideally to about age 18 (e.g., through education programmes that take cultural factors determining this practice into consideration). Such a delay in the age of the first pregnancy would bring women to pregnancy after full biological maturity is attained, would reduce the total number of pregnancies, and probably diminish obstetrical and nutritional risks. Thereafter, birth intervals of at least 19 to 24 months should maximize the opportunity to replenish maternal nutrient stores in women with chronic marginally adequate diets. Encouragement of breast-feeding and use of family planning programmes should complement these desirable outcomes.

Actions during Pregnancy and Lactation

In principle, the earlier a pregnant woman enters a well-thought-out and well-implemented programme of prenatal care, the better the outcome of pregnancy is likely to be. A programme of prenatal and perinatal care should be structured to make the best use of the facilities available and should be able to identify women at high nutritional or obstetrical risk using specific risk factors. In communities or populations where high risk is common, the feasibility of providing care to expectant mothers in specially organized centres for a period prior to delivery and in the perinatal period should be investigated. (This practice is being evaluated in several countries.)

Pregnancy and lactation are not the ideal periods to correct nutritional deficiencies, although in some settings this may be all that can be done at present. Thus, the subcommittee recognizes that special nutritional supplementation programmes are needed for nutritionally high-risk pregnant women. As is the case for all food supplementation programmes, such programmes should be carefully conceived and should consider the long-term effects of the programme for the pregnant woman, her family, and her community. Supplementation during pregnancy should be considered as a therapeutic action that attempts to avoid further nutritional deterioration and, if possible, corrects that already present. (As such it should have positive consequences for the foetus and for the process of lactation later.) However, these short-term programmes should neither hamper nor detract from long-term interventions whose aim is to improve social and economic well-being, health status, food availability, and food consumption (135). Rather, they should enhance these actions.

Special cases are those of nutrient fortification of foods and correction of specific deficiencies. These should be continuously operating programmes whose implementation is determined at national or regional levels.

The perinatal period (prepartum, labour and delivery, and puerperium) is a critical period of maternal and infant health, the establishment of breast-feeding, and emotional bonding. Efforts to provide the best care possible within given cultural practices and available facilities and applying appropriate technology are of high priority to reduce maternal and infant perinatal complications and death. Thus, specific efforts during this period should be directed toward providing adequate perinatal care, encouraging breast-feeding, and establishing emotional bonding.

Actions Related to Infants and Young Children

a. Breast-feeding

Every effort should be made to support and encourage breast-feeding. In areas where breast-feeding has been abandoned as the universal mode of feeding, its return should be promoted, and, at the least, programmes should be careful not to be conducive to further decline of breastfeeding.

b. Complementary foods

Complementary foods should be introduced as early as necessary (to prevent growth faltering) and as late as possible (to favour continued breast-feeding and to protect from weanling diarrhoea). Thus, measurement of incremental growth (growth monitoring) and efforts designed to reduce the threat of weanling diarrhoea are of central importance.

There is considerable latitude in what constitutes a desirable complementary food, and the following characteristics are merely general guidelines. Foods should be semi-solid so that they will not quench the thirst mechanism, have a caloric density of not less than 50 kcal/100 grams, provide at least 10 per cent of calories from protein and about 20 to 30 per cent of calories from fat. They should also be palatable for infants and not excessively high in fibre content.

If suitable complementary foods are locally available, e.g., foods meeting the suggested criteria, their use should be encouraged. Where such foods are not locally available, efforts should be made to meet the criteria for a suitable complementary food by teaching about different preparation of foods from indigenous sources or by provision of foods from outside, so that preparation of foods with suitable composition is possible. Of course, development and introduction of appropriate complementary foods should be coupled with efforts to minimize their contamination.

If foods from outside are used, they should be seen in the context of existing traditional feeding practices, provided such practices are not deleterious. In addition, distributed foods should be selected to supplement locally available foods, either by addition to, or alternate feeding with, traditional foods. Thus, distributed food supplements will usually need to be relatively high in protein and fat content and have high caloric density.

Milk and milk products are excellent sources of protein and minerals, but many nutritionists have reservations about administration of liquid milk to adequately breast-fed infants because the milk competes with breast-feeding and may be improperly prepared. There also has been some concern about the use of milk because of possible lactose intolerance among recipients. However, the modest daily quantities of milk or its products needed to upgrade many traditional foods are well tolerated by individuals with limited lactose absorbing capacity (136-137). Therefore, milk and milk products should continue to play an important role in feeding programmes for infants and children, particularly as components of semi-solid foods. For very young infants under about two months who are not breast-fed, a source of milk may be critical to survival where commercial formulas are unavailable.

c. Breast-milk substitutes

Occasionally, a mother may be prevented from nursing because of illness or other compelling circumstances. Rerely, lactation simply fails. In these unusual cases (and when a substitute mother is unacceptable, impractical, or not available), home-made milk-based or commercial infant formulas can be a valuable and sometimes lifesaving option. Formula should be used in a way that is not conducive to discontinuation of breast-feeding by women capable of and choosing to breast-feed When breast-milk substitutes are used, great care should be exerted in instruction regarding preparation of formula and cleaning of bottles and nipples. The latter should be used for feeding liquid substitutes only when use of cup and spoon is not feasible, and complementary foods, and usually even liquid substitutes, should be fed by spoon or cup.

d. Weanling diarrhoea

Prevention of diarrhoea should begin with efforts to prevent malnutrition prior to the introduction of complementary foods so that an infant will have adequate nutritional reserves and intact host defences when exposed to environmental pathogens associated with introduction of complementary foods. Breast-feeding is crucial in this regard. A second component of a prevention programme should be education of the mother (and other care-givers) regarding modes of transmittal of diarrhoeal pathogens and appropriate personal hygiene and food preparation and storage techniques to reduce transmittal. The third component should include efforts to reduce exposure to pathogens from complementary foods and from other environmental sources. Such efforts could include environmental sanitation and development and utilization of appropriate intermediate technologies; emphasis should be placed on the proper use and storage of water when it is scarce.

If the diarrhoea-malnutrition cycle is established, specific efforts should be undertaken to shorten the episodes and to break the cycle. Oral rehydration therapy is of central importance in these curative efforts (138-141). When available and necessary, specific therapy against pathogens responsible for the diarrhoea and/or malabsorption should be provided. Depending upon the state of the child, specific actions should also include provision of suitable and palatable foods and efforts to overcome the anorexia and lethargy that commonly accompany the condition. A child who is nursing should be offered the breast, and efforts should be made to maintain lactation during the diarrhoea episode if the child refuses the breast. Whenever possible, breast milk and food intakes should allow catch-up growth (142) and replenishment of nutritional deficits induced by diarrhoea.

e. Growth monitoring

The subcommittee endorses frequent monitoring of growth in infants and young children as a means of detecting early nutritional deficits and poor health, thus allowing prompt remedial action. Therefore, the subcommittee recommends that research to identify and eliminate operational constraints of growth monitoring receive high priority (see "Gaps in Knowledge Related to Infant and Child Nutrition," paragraph e, above).

APPENDIX. Effect of Lactation on Maternal Energy Balance and Protein, Vitamin, and Mineral Status

Energy Costs of Lactation and Maternal Body Composition

Milk production requires energy over and above the mother's own energy requirements-energy that must come from her food intake and/or her body stores. It is generally assumed that in women who have unrestricted access to food this energy will come from extra body fat stores accumulated during pregnancy. A slow but steady weight loss is therefore postulated to be a normal accompaniment to lactation (143). In fact, reported rates of weight loss of presumably well-nourished lactating women in industrialized countries vary quite widely (143-146). This variation is not surprising, given wide variations reported for energy expenditure and intake. For example, mean reported calorie intakes of lactating women range from 1,600 to 2,950 kilocalories per day (143-151).

The extent to which a mother complements the breast milk her infant receives with other foods also may influence the rate of her weight loss (152,153). A recent study at the University of Connecticut on well-nourished women with adequate pregnancy weight gain found that women who were exclusively breast-feeding consumed more calories and lost less weight than women who used the greatest amount of complementary foods (152). Other investigators have reported that "successful" breast-feeders maintained high levels of caloric intake and experienced little or no weight loss during the first four months postpartum (154, 155).

These studies suggest that much remains to be learned about the energy cost of lactation and weight loss specifically associated with lactation in well-nourished women. Furthermore, none of the studies of weight loss in well-nourished women have examined the composition of the loss, and few even contain data on skinfold thickness changes during lactation.

It is not yet possible to generalize about the relationship of energy intake to weight loss in women on marginal caloric diets in developing countries. Several careful studies suggest that specific local conditions determine how a woman will respond to the additional energy stress of lactation. Generally it appears that when high-energy-expenditure work demands coincide with low food availability, weight loss occurs (156159). This tends to follow a seasonal pattern that is also characteristic of non-lactating women and men (156-158, 160). For example, studies in the Gambia indicate that during the wet season, when food is scarce and the work load is high, weight loss averages one kilogram per month (156). In contrast, in the post-harvest dry season lactating women with average daily caloric intakes of 1,600 to 1,750 kilocalories actually gain weight, especially during early lactation (156).

However, studies in New Guinea (161, 162) and in India (163) suggest that, except under extremes of environmental pressure, weight loss in lactating women is less than one would predict from theoretical requirements and recorded intake. Durnin (161) hypothesizes that maternal body weight is maintained at least partially because women have reduced their energy expenditure, but suggests that explication of the phenomenon will require careful studies of energy expenditure. Physiological adaptation to low energy intake (156) and genetic adaptation in populations that have experienced many generations of energy deficit (164) also have been suggested as explanations. Neither of these has been systematically investigated.

Protein Status and Lactation

There have been very few studies in either well-nourished or poorly nourished women of protein metabolism during lactation. In a nitrogen balance study, King and colleagues (165) demonstrated that nitrogen retention during the last trimester of pregnancy was more than twice the estimated deposition in the products of conception. From 40 K data, Pipe and colleagues (166) calculated that nearly a kilogram of lean tissue is deposited during pregnancy, half of it in the breast. Whether this reserve is used during lactation has not been resolved.

Disturbances in protein status during lactation have been reported for Zaire (131) and India (167-170). In Zaire, where lactating women usually consume low protein diets, Vis and Hennart (131) reported that malnourished women occasionally show kwashiorkor-like signs. The data from India are consistent with the interpretation that, under conditions of low protein and low calorie intake, lean muscle is utilized to sustain lactation (168-170). However, these data must be interpreted cautiously because of methodological problems.

In the Gambia, where the staple foods are higher in protein than in the area of Zaire studied by Vis and Hennart (131), Whitehead and colleagues (unpublished manuscript) found no evidence of abnormal protein status during lactation. They did, however, find changes in amino acid patterns characteristic of pre-clinical kwashiorkor in pregnant women. This contrast between pregnancy and lactation is interpreted by them as consistent with the hypothesis that pregnancy places a greater strain on protein metabolism than does lactation. However, it is possible that inadequate intakes during lactation may be compensated by decreases in milk output, to the detriment of the infant.

Vitamin Status and Lactation

Very little is known about the effect of lactation on the vitamin status of women in developing countries. Information about the status of fat-soluble vitamins in lactating women in developing countries is virtually nonexistent. The major gap in knowledge, at least with regard to water-soluble vitamins, is whether these vitamins are preferentially available to the mother or to the infant through breast milk. Some evidence from milk composition and supplementation studies in well-nourished women could be interpreted to indicate that, at least for vitamins B6 and B12, vitamin levels in milk are more directly affected by maternal vitamin intake than is maternal vitamin status (171-173). On the other hand, it has also been postulated that vitamin B12 may be "trapped" in the mammary gland, thus making it preferentially available to the infant (174).

With respect to folate, several lines of evidence support the possibility that mothers with deficient folate intake are at a greater risk than are their infants.
- Megaloblastic anaemia is not uncommon in lactating women (175), while the incidence of megaloblastic anaemia from folate deficiency in infants is apparently rare (176).
- In two cases where lactating women with megaloblastic anaemia were treated with oral folic acid, there were rapid increases in milk folate concentrations before haematologic responses occurred in the women (177).
- In a Japanese study, women with normal plasma and red blood cell folate levels still had levels considerably below those found in their infants. In the infants, there was a significant correlation between plasma folate and breast milk folate level (176).

Taken together these three points suggest that a regulatory mechanism exists to protect folate levels in human milk. If there is preferential utilization of folate for milk, the lactating woman may be at risk of deficiency.

In a set of careful studies in the Gambia, Bates and colleagues (178, 179) documented exceedingly low levels of riboflavin intake associated with clinical signs of riboflavin deficiency in lactating women. Initial supplements of 1 mg/day failed to produce any clear-cut improvement in riboflavin status. Supplements of 2 mg/day given to lactating women, coupled with the average of 0.5 mg/day from dietary sources, resulted in satisfactory activation co-efficients of erythrocyte glutathione reductase (an indicator of riboflavin status) in 90 per cent of the women. Based on these results, the investigators suggest that current recommendations for riboflavin during lactation are too low.

In summary, in our judgement it is fair to conclude that current knowledge with respect to vitamin nutriture of lactating women is highly inadequate, and it is therefore very difficult to assess the effect of lactation on vitamin status of lactating women in developing countries.

Mineral Reserves and Lactation

With the exception of calcium, there appear to have been no studies relating mineral intake during lactation to the mineral status of the mother. Calcium is the one mineral for which there is a modicum of information. A woman with a milk output of 850 ml/day will excrete about 300 mg/day of calcium in her milk (150). Under optimal conditions she is protected from depleting her own skeletal calcium by drawing on stores laid down during pregnancy (180). However, even with optimal dietary calcium intake, she will still lose some calcium from bone during lactation (108, 181). These losses, however, do not appear to be cumulative. Walker's study of Bantu women suggests that, following lactation and/or the next closely spaced pregnancy, the calcium losses may be recouped (182).

There may be protective mechanisms at work to buffer depletion of the mother's skeletal stores of calcium. It has been suggested that calcium absorption is increased under conditions of chronic calcium deficiency (182). Also, low protein diets, which are characteristic of some women in developing countries, may increase calcium retention (183). While short-term adaptive mechanisms may help protect mothers on low calcium diets, the effect of low calcium intake during repeated pregnancy-lactation cycles needs to be assessed, particularly in relation to calcium-related deficiency disease in later life.

Cases of osteomalacia occurring as a result of calcium loss during lactation are rare. Two studies report such consequences among Asian migrants to the United Kingdom (184) and in Indonesia (185). These, however, were probably caused by insufficient vitamin D and not by calcium deficiency. Other reports describing osteomalacia and tetany associated with lactation are confounded by additional factors (186). However, recent studies from the University of Utah suggest that adolescent mothers on calcium-deficient diets may be at risk of calcium deficiency (187).

Iron is a mineral of particular concern, given the high prevalence of anaemia reported for women in developing countries. Recommendations for iron intake during lactation are usually theoretically set so that iron losses from pregnancy can be recuperated during lactation. However, there are virtually no empirical data on the functional effects of varying levels of iron intake during lactation on maternal nutritional status.

ACKNOWLEDGEMENTS

The Subcommittee would like to express its appreciation to Anne Ferris for her contribution to the review of lactation research; to Judith R. Bale, Staff Officer to June 1982; to Myrtle L. Brown, Executive Secretary, Food and Nutrition Board, and interim Staff Officer, June-October 1982; and to Shirley E. Cole, secretary to the Subcommittee. The Subcommittee also acknowledges the interest and support of Tine Sanghvi, Office of Nutrition, Agency for International Development.

The study summarized in this report was supported by Contract No. AID-ta-C1428 from the US Agency for International Development.

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