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3. Effect of diet on maternal health and lactational performance

Body Size and Composition
Protein Status of the Mother
Maternal Vitamin Status
Diet and Breast-milk Composition
Diet and the Quantity of Milk Produced
The Effect of Maternal Dietary Supplementation on Milk Output and Composition
General Conclusion
References

3.1. Lactation understandably represents a drain on maternal body composition. During the early stages of pregnancy, fat should accumulate in the subcutaneous stores and protein should build up in the muscular tissue. Towards the end of pregnancy and throughout at least the first six months of lactation fat and protein are used to support final foetal growth an subsequently milk production. The main questions that need to be resolved are: What happens to milk output and composition when, for nutritional reasons, the mother has not been able to lay down these stores in pregnancy and her diet during lactation is just as inadequate? What are the physiological consequences for the mother of prolonged breast-feeding under these circumstances? It is the custom in many societies for this to continue up to two years or more. Any ill effects may be compounded by repeated pregnancy-lactation cycles; it is no exaggeration to say that many women in the developing world are either pregnant or lactation almost continually during the whole of their reproductive lives. These questions need to be answered within the context of the heavy manual workload performed by these women.

Body Size and Composition

3.2. An examination of the literature from different parts of the world quickly reveals that dietary energy intake during lactation does have a marked effect on weight and body composition; this is only to be expected. What is surprising is that these physiological responses are not affected as much as one would have anticipated from the low dietary intakes encountered in the developing world. This is readily apparent from studies carried out by Prentice in the Gambial (1) (2). Figure 6 (see FIG. 6. Seasonal Weight Changes in Pregnant and Lactating Women in the Gambia (Source: ref. 1)) shows that during the wet season, from July to December, when food intake is low and farming is at its heaviest, weight gain during the last two trimesters of pregnancy averaged only 0.5 kg/month, and during lactation weight is lost at an average of 1 kg/month up to 12 months. In the dry season, however, when admittedly there is little heavy farm work, the mothers were slowly gaining weight during lactation at about 0.4 kg/month, in spite of the fact that their mean food energy intake is only 1,600-1,750 kcal/d depending on the month. These weight changes were mirrored by alterations in the sum of the skin-fold thickness at three sites: triceps, subscapular and supra-iliac. From January to April women actually appeared to be depositing subcutaneous fat. These astonishing findings can only imply that the Gambian mothers are operating at a totally different plane of energy utilization efficiency. As shown in section 3.18, the mothers were also able to maintain a very satisfactory level of milk production.

TABLE 5. Energy Intake of Indian Women during Pregnancy and Lactation as Compared to Estimated Requirement

a. At 30 calories per m² per hour; (a) at 70 calories per 100 ml providing 10 per cent above the physiological fuel value of milk.
b. On the basis of a 20 per cent increase in BMR found in selected subject.
c. Based on estimates from aliquot collection of all the foods consumed for two consecutive days each month from the sixth or seventh month of pregnancy till six months after child-birth for 50 women in the lower class and 18 women in the upper class.

Source: ref. 3.

The same phenomenon has been discussed by Rajalakshmi from Baroda in India (3), who has produced the energy balance data shown in table 5. Using a very conservative estimate for pre-pregnant basal metabolism of 905 kcal/d and for activity at 10 kcal/kg, a mother producing 725 ml milk/d would theoretically need 1,805 kcal, but the actual intake of an average lower-class Baroda woman is only 1,620 kcal/d. As in the Gambia, there was no dramatic weight loss during lactation; one can only echo Rajalakshmi when she asked: "How does the poor woman maintain her body weight and overall health status in spite of a poor diet and generous secretion of nutrients in her milk?" Clearly this is a subject that merits a greater research input.

There needs to be caution, however, before too many inferences are drawn from observations on one single, pregnancy-lactation cycle. Gebre-Medhin has reported (4), for example, that among poor Ethiopian women there is a slight but definite downward trend in antecedent weight with increasing parity in relation to the weight measured at the beginning of the first pregnancy. This observation may reflect the cumulative effects of repeated pregnancies.

Papua New Guinea is another country where very low energy intakes have been recorded during pregnancy and lactation (5). Only four out of a total of 69 women living in the lowlands had intakes above 2,100 kcal/d, and six had customary intakes below 950 kcal. In spite of this there was little evidence that either pregnancy or lactation led eventually to a major decrease in maternal body weight of fat stores, and this was true even when there were repeated pregnancies. Durnin considered that this could be due to an overall reduction in activity. There was some evidence that the mothers spent less time walking and more sitting, the latter being partly enforced because of breastfeeding.

Durnin concluded that the enigma of low energy intakes during lactation could only be solved by careful studies on population groups: studies that would not be easy to carry out. The investigation of comparatively small changes in physical activity as part of a long-term prospective study covering, ideally, the non-pregnant state, the whole of pregnancy, plus the whole of the lactation period would be necessary, as well as measures of changes in body composition and metabolic rates. It would be desirable if these studies could be coupled with other investigations of general health and well-being, and also of the mothers' capacity to be active in caring for the home and family. These studies would require experienced investigators willing to partake in laborious, painstaking, well-controlled studies, but Durnin has reasoned that unless this occurs our understanding is unlikely to be enhanced and we will continue to make dietary recommendations that are grossly at variance with actuality.

Protein Status of the Mother

3.3. On theoretical grounds (sections 1.5, 2.3), protein status might be expected to be affected more during pregnancy and lactation than energy status. There have unfortunately been far too few studies involving measure meets related to protein nutritional status, such as plasma albumin and amino-acid concentrations, particularly in areas where the oedematous form of early childhood protein-energy malnutrition is more predominant. It is not improbable that specific pathophysiological signs of protein deficiency would be more prevalent within such a community. Vis, for example, has reported (6) the not infrequent appearance of kwashiorkor-like signs in malnourished lactating women in the Kivu province of Zaire, where the diet is made up of beans, sweet potatoes, and bananas. The same features have also often been observed in nearby Rwanda, and also in the Buganda district of Uganda during episodes of political and military strife that have affected the cultivation and distribution of food crops. As shown in section 3.18, there is also evidence that milk production may be more affected when dietary protein is limiting rather than energy.

The WHO/FAO and DHSS in the United Kingdom have both recommended more protein during lactation than pregnancy, while the NRC in the United States reasoned that protein needs are higher in pregnancy. It is not possible to resolve this difference of opinion without more detailed study, but in the Gambia, where the staples are cereal crops, millet, sorghum, and rice, and thus any protein deficiency is likely to be secondary to a lack of energy, biochemical signs attributable to protein deficiency do appear during pregnancy but not in lactation. Plasma amino acid patterns change in a manner identical to those seen in early pre-clinical kwashiorkor, and in some countries but not all, these seem to be related to falls in plasma albumin concentration greater than can be accounted for by haemodilution. Plasma albumin concentrations return to normal, however, during lactation. These results would be compatible with the concept that pregnancy might place a particular strain on protein metabolism. This is clearly an area that merits more intense study.

Maternal Vitamin Status

3.4. All available evidence shows that both the mother's own vitamin status and that of the milk she produces (see 3.12, 3.13) are very sensitive to dietary intake. Table 6 shows the percentage incidence of clinical symptoms and abnormal blood vitamin biochemistry among poor indian women living in Baroda, as reported by Rajalakshmi (3). Similarly, in the Gambia (7) there are marked biochemical signs of vitamin deficiency reflecting the poor maternal diet. The mean erythrocyte glutathione reductase activation coefficient in lactating mothers is 1.6 throughout lactation, with some values over 2.0. The upper limit of acceptability is 1.3 and thus these data must be interpreted as being indicative of widespread deficiency. It needs to emphasized, however, that signs of abnormality were even more marked during the late stages of pregnancy, with mean activation coefficients approaching 2.0. Again, this could mean that pregnancy produces a greater metabolic strain on the mother than lactation, even though the recommended dietary allowance is more during lactation.

TABLE 6. Nutritional Status of Poor Indian Women during Pregnancy and Lactation

a Close to term.
b. In established lactation.
c. As judged by mid-arm skinfold.

Source: ref. 3.

3.5. The vitamin C status of the mother is also very sensitive to dietary intake. Figure 7 (see FIG. 7. Plasma Ascorbic Acid Concentrations in the Gambia by Season (Source: ref. 8)) shows plasma vitamin C levels in lactating women in the Gambia (8). These swing from a high level suggesting tissue saturation during the mango season down to almost unmeasurable levels in the rainy season, when intakes are extremely low. In contrast to riboflavin, plasma vitamin C levels were lower during lactation than in pregnancy. For example, during January 1979 mean lactating maternal values were around 0.2 mg per 100 ml, while in pregnant mothers the values were about 0.5 mg. A similar effect has been reported from Baroda (3), where the corresponding values were 0.58-0.75 mg per 100 ml during pregnancy but only 0.36-0.50 mg in lactation. The extra 40 mg/d of dietary vitamin C during lactation recommended by the NRC, but only an extra 20 mg/d in pregnancy, would therefore not seem unreasonable.

3.6. Vitamin A status can also be affected in lactation, although pregnancy again seems to be the time when the mother is most at risk. Rajalakshmi, for example (3), has found that among poor Indian women, serum levels fall during pregnancy but rise again after parturition, with an associated increase and decrease, respectively, in the prevalence of clinical symptoms of vitamin A deficiency. It was suggested that this could parallel the situation that has been observed in cattle, in which for some reason not completely understood, pregnancy can be associated with an increase in liver stores and the vitamin seems not so generally available to the other tissues.

In the Gambia, in spite of very low intakes, no gross clinical signs of vitamin A deficiency, such as keratomalacia or Bitot spots, have been observed even though plasma carotene levels vary in concentration closely following the seasonal variations in dietary intake, and plasma vitamin A concentrations are consistently lower than those observed in the United Kingdom (C.J. Bates, personal communication). The Gambian data would suggest that, at least within that country, the current RDA is unnecessarily high both for pregnancy and lactation. This could be because carotene rather than vitamin A is the major dietary source of retinol, and estimates of requirements are based on the assumption that six molecules of ,ß-carotene yield approximately only one molecule of retinol in vivo. It is known, however that this conversion varies in different foodstuffs and, more importantly, it may also vary with physiological status. Metabolic efficiency is believed to increase during pregnancy and lactation with energy (see 3.2) and other nutrients, and it is not unreasonable to postulate that this could be the same with ß-carotene and vitamin A. There is clearly a need for the 6:1 conversion factor to be reinvestigated under differing prevailing conditions during pregnancy and lactation in relation to the types of carotene-containing foods customarily consumed.

There is another possible explanation. Clinical vitamin A deficiency may not occur only as a result of exhausted body stores. Interaction with other nutrient deficiencies would also appear to be of crucial importance. Very recent evidence suggests that the classical signs develop from the combined effects of vitamin A deficiency plus protein and zinc deficiency (5, 10). This could well explain variability between countries in the relationship between vitamin A intake and the appearance of signs of clinical deficiency. There is clearly a need for these interactions to be studied on an objective basis to determine their relevance for practical nutritional and dietary planning.

3.7. The amount of folic acid required during lactation understandably depends on the status of the mother at the end of pregnancy. In the Gambia preliminary evidence shows that red-cell concentrations fall steadily during lactation, and some very low values have been obtained towards the end of the second year (Bates, personal communication). The women studied had been given a therapeutic iron-folate preparation during pregnancy as part of a standard clinical routine, but not during lactation. The extent to which it is the strain of pregnancy or the process of milk production that has been the cause of the megaloblastic anaemia observed in other countries early in lactation is uncertain. Chanarin, for example(11), found that 52 per cent of his cases were diagnosed postpartum, mostly in the first few weeks after delivery.

The problem of relating food folate intake to physiological performance has already been discussed (section 1.14). It is readily apparent that more work needs to be carried out, and such studies will have to take account of the effects of intercurrent infection. It is known in children that diseases such as malaria or hookworm can exacerbate poor folate status both in terms of FIGLU excretion and in the incidence of megaloblastic anaemia (12). There is also a close association between folate status and the prevalence of diarrhoeal disease (13).

Diet and Breast-milk Composition

Proximal Constituents

3.8. Generally speaking, it would appear that, except in extreme maternal undernutrition, the concentrations of total energy and protein in breast-milk are maintained at remarkably normal levels. In the Gambia, for example, where even during good times of the year dietary mean intake is only 1,700 kcal/d, the average energy content of the mother's milk is maintained at 72 kcal/100 ml, which compares well with the mean content of British mothers' milk, 69 kcal/100 ml. Even when mean intake was 1,100-1,200 kcal/d the energy content only dropped by about 10 per cent.

3.9. It is not easy to be precise about the effect of maternal diet on fat content, because concentration varies during the course of a feed - the fore-milk being more dilute than hind-milk. Most studies have been based on expressed milk, but more cannot be sure that this reproduces the same value that integrated measurements during actual breast-feeding would. In the Gambia, an estimate of the average fat content as consumed by the baby is 3.86 9/100 ml(14), in comparison with a value for British women of 4.2 9/100 ml(15). Whether the differences truly reflect maternal dietary differences, or whether they are due to different collection methods, is not known.

Hambraeus has reviewed the literature on the fatty acid composition of mothers' milk(16). It would seem that the milk fat resembles that of the mother's diet when her plane of energy intake is good, but when there is a shortage of food energy the milk fatty acid pattern resembles more that of the mother's subcutaneous fat stores. Maternal fat intake has no effect on the total triglyceride content, however, as illustrated by the Gambian data. The fat content of the Gambian diet is no greater than 10 per cent of the total energy, while in United Kingdom it is over 40 per cent, yet the fat concentrations are essentially the same.

3.10. The lactose content of human milk is high, around 7 9 per 100 ml. This component seems very stable in concentration as illustrated in table 7, which show that the milk of non-privileged Ethiopian mothers has very much the same lactose content as their Swedish and privileged Ethiopian counterparts (17).

TABLE 7. Lactose Content in Human Milk (9/100 ml, Means and SD)

Source: ref. 17.

3.11. The overall protein content of human milk also seems remarkably stable to despite changes in the maternal diet, as illustrated in table 8. Once again there is a remarkable similarity between the two sets of data from Swedish and non-privileged Ethiopian mothers(17). In the Gambia also, total protein content was essentially maintained at British levels despite an intake of marginal adequacy. During the period of the year when food intake was especially poor, some fall in milk total nitrogen content was observed, but this was by no more than 10 per cent. It must also be remembered that not all the protein in milk is a dietary source. Some of the fractions have specific functions as protective factors. The effect of diet on these components has still to be evaluated, a task complicated by the need to integrate the effects of dietary change with intercurrent infections afflicting both the mother and her baby.

TABLE 8. Nitrogen and Protein Composition of Mature Human Milk (mg per ml, Means and SD)

Source: ref. 17.

Vitamins and Minerals

3.12. In contrast to the proximal constituents, vitamin content - particularly of the water-soluble vitamins - is very sensitive to dietary intake. In the Far East a maternal diet deficient in thiamin can result in infantile beri-beri(18). Riboflavin content is also affected by maternal diet, as illustrated in table 9 (1). In the Gambia, milk values are only two-thirds of those in the United Kingdom and only about half the reported American ones. Thus, despite the existence of mechanisms that favour the foetus and the suckling child at the expense of maternal stores, the baby is born biochemically deficient; because the breast-milk has a low riboflavin content, and any traditional supplementary food an even lower one, the baby remains deficient throughout infancy (19).

The vitamin C content of milk also parallels closely the monthly variations in vitamin intake and plasma ascorbic acid levels (see FIG. 8. Seasonal Changes in Breast-milk Ascorbic Acid in the Gambia (Source: ref. 8)) (8). Likewise, folic acid content is also affected (table 9). In the Gambian dry season, mean concentrations were 54 ng/ml, while in the wet season these had dropped to 38 ng/ml. A comparison of breast-milk concentrations of other water-soluble vitamins during the two seasons is shown in table 9.

TABLE 9. Seasonal Variations in Breast-milk Composition in the Gambia

Values are means SEM.
a. p < 0.02
b. p < 0.001
N = number of subjects
Source: ref. 1.

3.13. The situation with the fat-soluble vitamins is less dramatic but nevertheless clear-cut. A comparative study of breast-milk samples from well nourished Swedish mothers and underprivileged Ethiopian ones has shown a significantly higher vitamin A level in the former and a greater concentration of 9-carotene in the latter(20).

The fat-soluble vitamin D content of breast-milk is generally low even in well-nourished mothers. Recently, however, there has been a report of a water soluble conjugate, vitamin D sulphate, in human milk (21 ) but the biological activity of this derivative is still in question (22).

3.14. The mineral content of human breast-milk in relation to diet has been insufficiently studied. The calcium content is variable and there have been suggestions that malnourished mothers do produce milk with a lower average calcium content, but there is no concrete evidence to support this statement. Since calcium is crucial to both bone development and growth, this is an uncertainty that surely should be clarified. Most mothers in developing countries from poor socio-economic circumstances consume considerably less than the RDA, only about one-third of their counterparts in the Western world (see section 2.6).

The iron content of milk is very low in concentration, but it appears that it is absorbed with a very high degree of efficiency (23). This is partly, but by no means completely, because of the association of milk iron within a lacto-ferrin protein complex. It has been demonstrated in Ethiopia (17) that mothers on a high iron intake have particularly high concentrations of lacto-ferrin in their milk, even when they are living under poor circumstances. It seems therefore, that the synthesis of this protein is protected, at least under the dietary circumstances prevailing in Ethiopia. The response of lacto-ferrin to a diet low in both iron and protein is not known, however, and there is an obvious need for the effects of maternal iron balance on the various iron components of human milk to be further elucidated.

Diet and the Quantity of Milk Produced

3.15. The general consensus is that the content of the proximal constituents of milk can be maintained within remarkably normal limits even in markedly undernourished mothers, and it is considered more likely to be the total volume produced that suffers. A major problem in defining the precise effect on volume is that we do not know with any degree of certainty how much milk one can expect from the average healthy, well-nourished mother. An arbitrary value of 850 ml has been used for theoretical calculations, but most measured, mean values in the industrial world have been less than this. In virtually every country so far investigated, volume rises steeply during the first month of life, but, as shown in figure 9 (see FIG. 9. Mean Daily Breast-milk Outputs during Infancy from Various Sources Compared with the Range Needed to Meet Estimated Requirements, Based on the Mean Values of the Department of Health and Social Security (DHSS) (36) (Source: ref. 31))(31), the rate of rise in milk output then falls off dramatically and total volumes quickly become less than those theoretically needed to satisfy energy requirements as the child grows older and larger. From table 10 it seems reasonable to conclude that the mean maximum volume in a wealthy country is more likely to be 700-800 ml than 800-900 ml.

TABLE 10. Milk Output (ml/24h) of Well-nourished Mothers from Industrialized Societies

a. Exclusively breast-fed.
b. Includes mixed feeding.
c. Data obtained by weighing the mother, not the child (see text, 3.16).
d. Ranges calculated from mean ±2SD.

It is unwise, however, to think only about mean values; the range in Cambridge around two to three months is 4901,115 ml, and in Sweden the corresponding range from Holvander's data is 600-930 ml. An important and as yet unanswered question is whether mothers with low milk outputs did not have the capacity to produce more milk, or whether a whole variety of social and biological constraints were acting against them, such that they were functioning well below their maximum capacity.

3.16. The highest volumes reported in recent times are those from Hartmann's group in Western Australia (28). These values were obtained by test-weighing the mother. This method is highly correlated with the more usual method of test-weighing the baby. The regression co-efficient of 0.8 indicates that higher values are obtained by weighing the mother. Most of the difference between the two procedures is due to the sweating losses of both the mother and baby. Thus, the mean value for Western Australian mothers at two to three months compared with the European data would be around 1,000 ml rather than 1,200 ml. Clearly, even this value is significantly greater than any others that have been published, with the exception of old reports on "wet nurses" (37). The upper level of Hartmann's data is around 1,600 ml.

It is of obvious importance that the apparently much greater ability of Western Australian mothers to produce milk should be confirmed on a larger representative number of mothers from that community, and that the detailed and varied advice provided by the Australian Nursing Mothers Association is objectively evaluated to determine any crucial difference between European and Australian nursing practices. Recent evidence of the high incidence of breast-feeding in a wider range of Western Australian mothers is provided by the prospective growth study of Hitchcock and Owles (38), who found that 64 per cent of mothers were still breast-feeding at six months.

3.17. The study of twins and the mother's ability to feed two babies rather than one is also likely to be informative. Although twins, in the Third World, frequently suffer from infantile malnutrition, there is evidence that mothers in the industrialized countries can respond by producing milk well in excess of the normal range for singletons. Data obtained by Hartmann in Western Australia (39) on milk outputs in mothers with twins compared with mothers of single infants are given in figure 10 (see FIG. 10. Milk Outputs of Western Australian Women Breast-feeding Twins and Exclusively Breast-feeding Single Babies (Source: ref. 39)). This indicates that the greatly enhanced capacity exists only for the first six months of lactation.

3.18. The importance of the plane of nutrition on milk production has been extensively studied in dairy cows, and feeding standards based on the level of milk production have long been considered to be an important determinant of the profitability of the dairy industry. The influence of maternal diet on the level of milk production in women is much less clear. A summary of a number of studies on breast-milk consumption in developing countries is given in table 11. The ranges for the different countries are remarkably similar to those in table 10 for affluent countries. Mean values are, however, generally about 100 ml/d less at two to three months, though the mothers continue to breast-feed for much longer. These data are surprising when one considers the gross differences in dietary intake between the two types of country. The possibility exists, however, that the European mothers could have produced more milk if they had adopted different feeding practices, such as by feeding more frequently as is the custom in Western Australia, and thus the true effect of a poor diet might be masked. There is an obvious need for the optimization of milk production to be studied in wealthy countries as well as in poor ones.

There is evidence, however, that when food-energy intake falls to exceptionally low levels the mother's capacity to adapt is exceeded and milk output falls dramatically. This is illustrated in figure 11 (see FIG. 11 Seasonal Variation in Energy Intake and Breast-milk Output in the Gambia (Source: ref. 1)), which describes the situation in the Gambia (1) during the rains when food energy intake in August-September drops to as low as, 1,100-1,200 kcal/d. Milk output drops markedly, but the mean volume of milk produced during the 12 hours of daylight is still 280 ml, which corresponds to around 600 ml/24 hr. Values of around 500-600 ml/d have also been reported from India by Gopalan (41), from Zaire by Vis et al. (34), by Van Steenbergen in Kenya (32, 33), and Martinez and Chavez from Mexico (35).

TABLE 11. Milk Output (ml/24h) of Women from the Developing World

a. Ranges calculated from mean ±2SD.

Vis, from his work in Zaire (34), has suggested that milk output may be more affected in primary protein deficiency than in energy deficiency, hence the particularly low values in the Kivu province of Zaire. It is also possible that similar deficiencies may have existed in the Kenya study. It may be concluded that, to be sure of the effect of diet on breast-milk output, both variables, protein and energy intake, need to be measured. We need to determine unequivocally whether dietary composition, particularly a limiting protein content, is associated with an especially reduced milk production.

3.19. The major problem in comparing milk outputs between countries is the difficulty of doing so with a sufficient degree of precision. The test-weighing procedure inevitably interferes with normal life-styles and the interaction between the mother and her child: the child has to be separated from the mother at the beginning and end of each feed, even if just for a short time. Another problem is that the weight difference at each feed can be quite small. In Europe, where women feed their babies on average four to eight times per day, typical weight differences range between 100200 9, while in the developing world, where a child may be fed 10-15 times, this value is only 30-100 9. It is also necessary to modify the procedure to fit in with local circumstances and customs. With such scope for measurement error it is surprising there is so much uniformity in the data emerging from different parts of the world.

3.20. The net benefit of breast-milk to a child clearly depends on the product of volume and nutrient content. Table 12 shows such calculations made by Rajalakshmi (3) for lower and higher income families in India relative to the NRC RDA (42). As might be expected from the discussion in previous sections, infant energy and protein intakes exhibit relatively moderate deficits (20-25 per cent), while folate, vitamin A, and iron intakes suffer dramatically; intakes are of the order of only 10 per cent of the recommended value. Clearly, the effect will be different for different countries; in Ethiopia, for example, infant riboflavin intake would be more affected than in India, while iron intake would be relatively satisfactory.

TABLE 12. Nutrients Derived by Indian Breast-fed Babies as Compared with Recommended Allowances a

a. Calculated from milk composition data for 700 ml milk.
Source: ref. 3.

The Effect of Maternal Dietary Supplementation on Milk Output and Composition

3.21. Table 13 summarizes the results of attempts to influence breast-milk production by providing dietary supplements to mothers of low socioeconomic status. Unfortunately, there have been all too few direct attempts to test the important hypothesis, "feed the nursing mother, thereby the infant", in spite of this crucial importance to public health and infant well-being in the third world. A general comment on the results would be that they have not been inspiring. There are a number of theoretical reasons why this might have been so, but one stands out: there has been generally too little attention given to the size of the deficit that needs to be filled. From the data in section 2.2 it is clear that the energy gap between mean intake and the RDA is at least 1,000 kcal/d, but few investigators have attempted to provide anything like this amount. Some of the studies have also been short-term ones and it would not be surprising if this failed to overcome a chronic problem. Furthermore, few investigators have attempted to assess the effect of their supplement on customary home intake, and it is always possible that it had only a substitution effect. For these and other reasons to be discussed, some circumspection is necessary before too firm a conclusion is arrived at on the basis of current knowledge.

TABLE 13. Dietary Supplementation and Milk Output: Studies Throughout the Years

3.22. Although there have been very few studies, interest in this subject has spanned a number of years. As long ago as 1925, Adair (43) attempted such intervention studies but, like Kleiner et al. in 1928(44) also working in the United States, were only able to increase milk output slightly and then only in very early lactation. It must be recognized, however, that the supplement provided was largely carbohydrate in nature. A little later, in 1931, Deem (45), working in New Zealand, investigated the effect of supplementation using a variety of diets, but unfortunately these were only given for a relatively short time, and perhaps because of this the increased milk yield was no greater than 10 per cent.

A study carried out on undernourished mothers in Wuppertal, Germany, just after the Second World War by Gunther and Stanier (46) actually produced lower breast-milk outputs in supplemented mothers in the first week postpartum, and this occurred whether they were given fat or protein and carbohydrate. The only rational conclusion one can make is that there must have been sample selection anomalies!

3.23. Returning to the Third World, in 1954 in what was then the Belgian Congo, Holemans(40) investigated the milk yield of 27 women who had been receiving 40 9 of skimmed milk per day for one year. The results are given in figure 12 (see FIG. 12. The Effect of Maternal Dietary Supplementation on the Milk Intake of Young Babies from Zaire (Source: ref. 40)). Although there was some improvement during the first trimester of lactation, the resultant milk output was still very low in comparison with data collected from non-supplemented mothers in other countries. Here the problem could have been that the supplement, although given for a long time, both before and during lactation, supplied only relatively small amounts of dietary energy. The investigators were primarily concerned with filling a protein gap.

A little later, in 1958, Gopalan(41) fed a small group of mothers of 5-to13-month-old babies a series of diets containing 61, 99 and 114 9 of protein, respectively, for three consecutive ten-day periods. The diets were iso-caloric and supplied 2,900 kcal/d. The test-weighed mean milk outputs, however, were only 402, 512, and 490 ml/d. The explanation could have been the short duration of the study {only 30 days in total), and the fact that the children were mostly in the second half of infancy when the maternal supplementation commenced.

3.24. One of the best of the recent studies is that reported by Chavez et al. in 1975 from Mexico (48). This was a two-year longitudinal study in a poor and inadequately nourished rural community. The diet of the mothers was supplemented from the 45th day of gestation until weaning with 300 kcal/d. There were effects on both volume and composition, but these were such that benefits of an increased milk volume were mostly negated by the milk's becoming more dilute, by 15-20 per cent (see FIG. 13. Effect of Maternal Dietary Supplementation on the Solids Content of Mexican Mothers' Milk (Source: ref. 48)). Nevertheless, the impact on child growth was measurable. In this study the total mean protein and food energy consumed by the mothers by the eighth month of pregnancy was 74.9 9 and 2,225 kcal/d, and in lactation 78.6 9 and 2,365 kcal: the mean maximum milk yield achieved was 718 ml at four months.

3.25. Two other important studies in Latin America have been those of Herrera et al. in Bogota, Colombia(49), and Lechtig and Klein in Guatemala (50). Unfortunately, in neither investigation was breast-milk output measured and interpretation has to be confined to growth data. In the Colombian study (49) a supplement of 850 kcal and 38 9 protein/d unfortunately resulted in a net intake increment of only 133 kcal and 20 9 protein, because the supplement merely acted as a substitute for much of the food normally consumed at home. It therefore increased dietary intake but not to the expected level. Maternal prenatal nutritional status was shown to influence birth-weight and child growth during lactation but this was limited to the thinner women of the sample. The faster rate of infant growth was that which would have been predicted from the higher birth weight. It is arguable that a higher milk output must have been achieved in the supplemented thin women for their babies to respond in this way, but the more normal women were totally unaffected.

In the Guatemala study 150), too, the mother's diet was supplemented both during pregnancy and lactation, but unfortunately so also was the child's diet, and thus it is not easy to define with any exactness the relative contributions of each to infant growth. Nevertheless, the combined programme did achieve a statistically significant increase in attained height at 12 months of about one centimetre, and similar benefits were claimed for weight and head circumference. For the total population the increase in mean weight at 12 months of age was from 220 to 430 9, depending on the specific diet consumed.

3.26. The effect of diet on milk output and child growth is currently being studied in the Gambia(14). This investigation has a step-wise design; during the initial phase of the study the supplement was given during the whole of the first 18 months of lactation, in the second phase the supplementation has begun from the time pregnancy was diagnosed and then continued throughout lactation. By the time the third phase starts, women will have been supplemented throughout their previous lactation and will thus enter the supplemented new pregnancy cycle having enjoyed a much better plane of nutrition over a longer period of time.

After an initial year in which baseline dietary, anthropometric, and lactational data were collected for retrospective comparison, all the lactating mothers in the village were invited to take part. Attendance at supplement sessions has exceeded 97 per cent throughout the year, and consumption of the supplement at each attended session was always over 95 per cent. The supplement consists of a locally prepared groundnut-based biscuit also containing wheat-soy flour, dried skim milk, sugar, and oil. This is supplied six days a week, excluding public holidays, together with a tea drink fortified with a multivitamin supplement. The biscuit has a high energy density, about 4.7 kcal/g, and this type of supplement was chosen in the hope that it would have only a minimal effect on home food intake, which was also quantified. The mean daily intake of energy, home food plus supplement, rose from 1,568 to 2,291 kcal/d. Unfortunately, as shown in figure 14 (see FIG. 14. Seasonal Changes in 12 h Breast-milk Output at Different Stages of Lactation in Unsupplemented and Supplemented Women. Mean and SEM and number of women are shown at each point (Source: ref. 14)), the effect on milk output has been negligible, as has the effect on milk composition.

General Conclusion

3.27. It has to be concluded that the cost-effectiveness of maternal dietary supplementation as far as improving lactational capacity is concerned still has to be proved. One thing is certain, any public health programme adopting this approach will have to be carefully designed and administered if a truly convincing result is to be achieved. An improved diet during pregnancy leading to a reduction in the number of small-for-age babies seems to offer a greater potential. It is not improbable, however, that dietary well-being over a much longer time-span will be needed before an improvement in the overall pregnancy-lactation cycle will be achieved. This emphasizes the need for agencies funding applied research of this type to be prepared to do so for as long as is necessary to adequately establish the crucial biological facts. It is feared that the present inconclusive situation has been partly brought about by the lack of long-term funding for community-based fundamental and applied research. As will also be discussed, the mother and her well-being must also not be ignored in these investigations.

A major difficulty in assessing the success of dietary supplementation programmes is identifying the magnitude of change that it is reasonable to expect. The "standard" that has been used for most theoretical reasoning is 850 ml, although to satisfy the total energy needs of the average child up to the WHO/FAO estimated requirement solely from breast-feeding, for up to six months as advocated by authorities, would indicate a figure nearer 1,200 ml. We have seen, however, that the majority of studies among well-fed mothers have revealed a mean peak production value of only 760 ml. In these circumstances, it is arguable that a greater volume could not have been expected in the Gambia, as the mothers were already providing milk up to the customary norm. Chavez in Mexico (48) also achieved a mean peak value of only 718 ml in his supplemented mothers. Perhaps it is only under conditions of extreme dietary deprivation, when milk volume is very low, that maternal supplementation is likely to achieve a meaningful and worthwhile increment. It is quite obvious that a realistic and biologically attainable target needs to be identified with more certainty.

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