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Energy Requirements
Protein
Vitamins and Minerals
Other Nutrients
General Conclusion
References
1.1. All expert committees responsible for defining recommended allowances have reasoned that there should be a substantially greater dietary energy and nutrient intake during lactation (table 1). In fact, nutrient recommendations for lactating women are frequently higher than for any other person within the family group. The basis of most recommendations is that the average lactating mother produces 850 ml of milk each day and thus she needs to consume sufficient food to cover each dietary component secreted in her milk, after making due allowance for the efficiency with which the maternal diet can be utilized for milk production. While in principle this is a perfectly rational approach, there are a number of complicating factors that need to be taken into account; in particular it is becoming increasingly obvious that many of the allowances derived in this way greatly exceed the customary intake of mothers, particularly those living in the developing world, yet there may be no sign of any adverse effect. It is essential that this discrepancy is examined more closely, but it must be emphasized that current knowledge is inadequate to provide anything like a satisfactory explanation.
TABLE 1. Extra Daily Nutrient Allowances for Lactation
| Nutrient | Non-pregnant non-lactating |
Lactating |
Increase |
| Energy (kcal) | 2,100 |
2,600 |
500 |
| Protein (g) | 44 |
64 |
20 |
| Retinol (µg) | 800 |
1,200 |
400 |
| Vitamin D (µg) | 7.5 |
12.5 |
5 |
| Vitamin E (mg) | 8 |
11 |
3 |
| Vitamin C (mg) | 60 |
100 |
40 |
| Riboflavin (mg) | 1.3 |
1.8 |
0.5 |
| Nicotinic acid (mg) | 14 |
19 |
5 |
| Vitamin B6 (mg) | 2.0 |
2.5 |
0.5 |
| Folate (µg) | 400 |
500 |
100 |
| Thiamin (mg) | 1.1 |
1.6 |
0.5 |
| Calcium (mg) | 800 |
1,200 |
400 |
| Iron (mg) | 18 |
Sa |
Sa |
| Zinc (mg) | 15 |
25 |
10 |
1.2. The estimation of how much extra dietary energy must be provided during lactation is complicated by a number of physiological and social factors. The amount of work a woman does while lactating in contrast to that done during her pre-lactation state can vary considerably. In some societies breast-feeding is not allowed to make a difference, and women continue with hard manual work. In other countries or social classes, women are protected at this time and assume a more or less sedentary existence. The basis of the WHO/FAO recommendations(2) may be summarized as follows. If a mother delivers 850 ml of milk per day for six months, the total amount of energy required to make that milk be in the order of 135,000 kcal on the assumption that dietary energy is converted to milk energy with an efficiency of 90 per cent. The mother should, however, have laid down anticipatory reserves of fat during pregnancy, and if this has been of the recommended amount, 36,000 kcal, the net need for lactation will therefore be only 100,000 kcal, or around 550 kcal/d. Since the energy requirements for the average moderately active woman are 2,200 kcal/d, the total recommendation becomes 2,750 kcal/d. Clearly, however, if a woman breast-feeds beyond six months - and it must be recognized that the majority of mothers in the developing world breast-feed their children for about 18 to 24 months - the fat stores will have become used up and thus extra dietary energy after six months is theoretically necessary. Likewise, if a woman is forced to continue with heavy manual labour, the base-line value for calculating requirements is not 2,200 kcal/d but higher. Again, this consideration is not an unusual one as the majority of women engaged in subsistence farming are forced to work just as hard during lactation as at other times. Thus, in theory, lactating mothers in the developing world could need anything up to 3,300 kcal/d after the sixth month.
1.3. Recommendations developed for less arduous life-styles in the industrialized countries exhibit significant differences. In the United Kingdom, it is assumed that very few women will lactate beyond six months, and therefore no special consideration was given to "prolonged lactation." It was also assumed that mothers will be only moderately active and on average will therefore never need more than 2,700 kcal/d during lactation. In the United States the most recent NRC recommended daily dietary allowances for energy(1) recognize that there will be a range of needs and quote 2,2003,000 kcal/d for 19-22-year-old lactating women and 2,100-2,900 kcal/d for those over 23 years. Since the energy expenditure mode for the American nursing mother is likely to be lower than the midpoint of the range, it is clearly assumed that her intake can be considerably less than that of her counterpart in the developing world. It will be shown, however, that this assumption may require considerable qualification. It is becoming increasingly apparent that the efficiency with which the human body can utilize dietary energy for work and other physiological functions can vary with the level of dietary intake as well as with physiological status and environmental factors.
1.4. One further point deserves to be mentioned. In the calculation of these requirements it has been assumed that the mean energy content of breast-milk is 70 kcal/100 ml. In nearly every study on composition, milk has been obtained from the breast using a technique of manual or mechanical expression, the assumption being that expressed milk has the same composition as the milk the infant would have obtained during physiological suckling. The potential fallacy in this assumption has already been indicated by a number of investigations and, strictly speaking, we have no precise information on the energy intake of the infant and hence the true drain on the mother.
1.5. Fortunately, calculating protein allowances for lactation is not as complicated. On the basis of an 850 ml output, assuming it contains 1.2 9 of protein per 100 ml and that dietary nitrogen utilization is operating with normal efficiency, an extra 24 g/d of protein with a chemical score of 70 was recommended for lactation by FAO/WHO(2). The NRC(1) recommended an extra 20 g/d of good quality protein.
Generally speaking, the recommended lactation increment for a given nutrient is greater than for dietary energy. Thus, an examination of the protein and energy recommendations of FAO/WHO 12), for example, reveals a suggested increase of 59 per cent in the case of protein with a chemical score of 70, but only 25 per cent with energy, assuming the mother remains moderately active and is not lactating after the first six months. These recommendations would imply that, for women living on diets with a marginal protein content, the quality of food should improve during lactation. As it will be shown, however, there is little sign of this occurring in practice.
1.6. It is not unreasonable to claim that the most scientifically satisfactory recommendations are for energy and protein. To say this in spite of the shortcomings in our knowledge is a reflection of an even greater paucity of objective information concerning the other nutrients.
1.7. Vitamin A. Breast-milk contains about 50 µg of retinol/100 ml and, on the assumption that a mother will secrete 850 ml, an extra dietary allowance of 400 µg retinol equivalents has been made by most authorities. In the developing world much of the retinol is consumed in the form of ß-carotene, and in practice this can only be achieved if there is a considerable change in dietary pattern from that of the mother's pre-pregnant, non-lactating state: she would need to eat food quite different from that consumed by the rest of the family. One of the difficulties in defining retinol requirements is that the body contains substantial stores that may take many months, or even years, to deplete. When it is realized, however, that in many impoverished countries a mother may be pregnant or lactating virtually continually from 18 to 45 years, the value of the stores in providing temporary protection during pregnancy and lactation must be limited.
1.8. Vitamin D. It is a problem to make rational recommendations for vitamin D, as the natural source of cholecalciferol is via sunlight and synthesis in the skin. Some authorities would suggest there is no primary need for vitamin D, at least in adults, unless their life-styles force them to keep out of the sun, as might be the case with mothers lactating during the winter in northern latitudes, or where social customs keep women mainly indoors or heavily covered up when outside. The NRC (1) recommends an extra 5 µg cholecalciferol during lactation, which makes a total of 12.5 µg for women between 19 and 22 years old. Vitamin D is, however, not distributed widely in foods. Natural sources are fatty fish, eggs, liver, and butter, as well as fortified margarine. In some countries cow's milk is also fortified, but in most, this is limited to some brands of tinned milk. It is unlikely, however, that the typical poor mother in the developing world will have access to such foods. There is a growing body of opinion that the only practical way of ensuring an adequate vitamin D intake, if the photosynthetic process fails for whatever reason, is to take vitamin D capsules prophylactically as a medicine.
1.9. Vitamin C. Considerable extra allowances have been recommended for vitamin C in order to cover the vitamin C content of breast-milk. In the United States an additional 40 mg/d has been recommended in the most recent NRC report(1). This was justified by the fact that breast-milk normally contains 4055 mg ascorbic acid/litre. Once again this recommendation represents a far greater increment than that for energy and, in the developing world - where vitamin tablets are only available for the rich - the suggested level could only be achieved by major dietary modification: the total American recommendation for lactating women is 100 mg/d.
1.10. Thiamin. Estimated thiamin requirements have been based on energy intake, mainly because the vitamin is important in the intermediary metabolism of carbohydrates and fats, particularly the oxidation of pyruvic acid. Because human milk contains around 0.2 mg of thiamin in a typical day's supply, and because extra dietary energy is recommended for lactation, allowances for women have been raised at these times by an average of 0.5 mg/d. This represents an increase of about 50 per cent.
1.11. Riboflavin. Riboflavin is not widely distributed in foods in high concentrations, and if a lactating mother's diet is devoid of milk, liver, or fortified cereal products it is likely her intake will be below current recommended dietary allowances. The amount of riboflavin secreted in the milk by healthy breast-feeding mothers ranges from 0.3 to 0.5 mg per day, and the upper value has become the recommended dietary increment for lactation. Since the basic allowance for a woman during her reproductive years is 1.2-1.3 mg/d, the total allowance for a lactating woman is usually quoted as 1.8 mg/d.
Recent work in the Gambia, however, has indicated this may not be sufficient. Using a community-based approach, Bates and colleagues (3) determined, under prevailing circumstances, the intake of riboflavin compatible with accepted biochemical normality - an erythrocyte glutathione reductase activation coefficient of no more than 1.3. They concluded that an intake of 2.5 mg/d was necessary before 70 per cent of women achieved this desired level of function. Although these studies were carried out in the Gambia, parallel investigations in the United Kingdom indicated that such an intake was relevant there too. Intakes of this magnitude are, however, difficult to achieve in practice, which inevitably raises the question of whether prophylactic vitamin therapy, including riboflavin, may be just as necessary during pregnancy and lactation in the developing world as some authorities consider it to be in industrialized countries.
1.12. Nicotinic acid and its derivatives. The problem with defining requirements for nicotinic acid is that the vitamin is also synthesizable from tryptophan, although probably at low rate of efficiency. It is usually assumed that for every 60 mg of tryptophan consumed about 1 mg of nicotinic acid is made available to supplement the vitamin intake. There is, however, considerable variation between individuals, and the amount converted may be subject to nutritional state and status.
Another difficulty in defining requirements is availability. Much of the nicotinic acid in cereal foods is in a bound form and the extent to which this bound nicotinic acid is truly metabolically available is not known with certainty, but it is thought that this could be limited. The marginal protein intake of most lactating women in the developing world, plus the low tryptophan content of cereal proteins and the bound state of the nicotinic acid, all indicate that nicotinic acid could become a limiting nutrient. As with many nutrients discussed, however, the efficiency of food utilization, in this case the conversion of tryptophan to nicotinic acid, may be greater during pregnancy and lactation, but this is by no means certain. Because of a lack of fundamental scientific knowledge, most expert committees have been forced to assume that vitamin allowances should be increased proportionately with energy during lactation. It must be recognized, however, that this is rule-of-thumb reasoning; it has no physiological validity, as nicotinic acid, unlike thiamin, is not directly involved in energy metabolism. Because of the complex sources of nicotinic acid, allowances are usually quoted in "niacin equivalents," that for lactating women being 18-19 mg/d.
1.13. Vitamin B6. Vitamin B6 also presents a number of unsolved scientific problems, which makes the recommendation of dietary allowances difficult. Requirements seemingly vary according to the general composition of the diet; for example, they seem to rise with the level of protein and may also be greater with high-fat diets. There are also physiological factors influencing efficiency of utilization: for example, young men have been reported to utilize B6 more readily than older men. Thus it would not be unreasonable to suppose that lactating women may be able to compensate for a poor intake, although there is no proof for this. The low-fat and the moderate protein contents of the diets of women in the developing world may also "compensate" or a low intake of B6. Oral contraceptives, however, probably increase dietary needs, and the increasing use of this method of birth control, during lactation as well as at other times, might mitigate against this protective effect. Recommended dietary allowances for B6 during lactation must therefore be regarded with circumspection, and the extra allowance of 0.5 mg/d, making a total of 2.5 mg/d must be recognized as largely arbitrary.
1.14. Folic acid. Folic acid deficiency is always a potential problem during pregnancy because of the greatly enhanced physiological needs at that time. It is, in fact, the only vitamin for which the recommended increment is vastly greater during pregnancy than for lactation. In the industrialized world these needs are routinely overcome by the administration of commercial vitamin preparations in which folate is often given together with extra iron. Clearly, this service is not available to the vast majority of mothers in the developing world and thus the extra metabolic drain of pregnancy might be carried forward into lactation.
One difficulty in defining the adequacy of folate intake from traditional foods is the complex chemical nature of the folic acid derivatives found therein, which are chiefly in the form of formyl or methyl derivatives of tetrahydrofolic acid conjugated with additional glutamic acid residues. It is recognized that the efficiency of digestion and absorption of these derivatives is variable and incompletely understood. Once absorbed they exhibit different degrees of efficiency in their capacity to be converted into the co-enzyme form of the vitamin. Another problem is that tables of food composition, particularly those currently in use in the developing world, can be quite misleading in terms of folate content. Nutrient composition data are now obtained by a standardized microbiological assay procedure using Lactobacillus cased after incubation with chick-pancreas deconjugase. Gas chromatographic methods to separate the different folate derivatives are also being introduced.
The most recent NRC recommendations have retained an intake of 400 µg/d for non-pregnant, non-lactating mothers but have reduced the total allowance during lactation from 600 to 500 µg/d. The DHSS in the United Kingdom (4), on the other hand, originally set their basic allowance for women at 300 µg/d and for lactation 400,ug/d. The RDA difference between the two countries is even larger during pregnancy, 800 µg/d in the USA and only 500 µg/d in the United Kingdom. Even these lower values are rarely achieved in practice by pregnant and lactating women in the United Kingdom from dietary sources alone. At this moment in time it can only be concluded that much more research needs to be carried out before a truly meaningful RDA can be defined.
1.15. Vitamin B12. At the risk of seeming repetitious, requirements for B12, too, are difficult to define, the main reason being that healthy people have substantial liver stores that are readily available to the body as a whole. Proven deficiency is rare and is usually associated with poor digestion and absorption. Food of animal origin, particularly liver, is the best dietary source of B12, and thus vegans or people living almost exclusively on vegetable foods are potentially at risk. In the industrialized countries such people are protected by prophylactic B12, but, needless to say, this does not occur in the developing countries. The allowance for non-pregnant, non-lactating women of 3 µg/d is largely arbitrary. The extra 1 µg during lactation is based on the average B12, concentration in the milk of healthy women.
1.16. Calcium. Milk contains an appreciable amount of calcium, around 300 µg in a typical day's supply, and thus the RDA for this mineral is of especial importance during lactation. Physiological measures of calcium requirements in young adults have mainly been based on the amount needed to replace body losses. Interpretation of the data is difficult, however, since one gets quite different answers in studies carried out in people from the developing world vis-a-vis the industrialized countries. In men, 500 mg/d would appear to cover the needs of the vast majority in the former countries, while 800-900 mg/d seems necessary in Europe and North America. It would appear that a person who has become accustomed to a relatively large calcium intake becomes relatively inefficient in the ability to absorb calcium. Adaptation to low intakes has been shown to occur, but this can be slow and considerable differences have been noted in the ability of different individuals to re-accommodate to the new circumstances.
There is also an association between calcium balance and the protein content of the diet: the higher the level of dietary protein, the lower the efficiency of calcium maintenance. This nutrient interaction could partially explain why people in the developing world manage to survive on what seem to be impossible low intakes. Another dietary factor is the calcium-to-phosphorus ratio. In countries like the United States this ratio is unfavourable to positive calcium balance since the level of dietary phosphorus increases urinary excretion.
Thus, while women consuming less than the North American or European intakes of protein and phosphorus may maintain calcium balance on lower intakes of calcium, an allowance of 1,000-1,200 mg/d has nevertheless been made for all countries. Unless women have a reasonable supply of cow's milk in their diet it is unlikely that this recommendation will be met. The FAO acknowledges that many women receiving only a small amount or no milk in their diet have gone through several successful pregnancies and lactations on much lower calcium intakes. The FAO has stated, however, that the high recommendation is compatible with the best system of diet that can be given to mothers, even though unfortunately such advice cannot always be put into practice. It has to be borne in mind that the later loss of calcium from the bones that afflicts women after the menopause can lead to disabilities such as fractured femurs. Calcium provides a good example of where it is essential to define dietary needs on the basis of a mother's long-term well-being, not just upon an immediate, single physiological function such as capacity for lactation.
1.17. Iron. Iron is unique among the nutrients in that the recommended allowance is considerably greater for adult women than men, even when they are not pregnant or lactating. This is because of iron losses during menstruation, which can be a particular problem in heavy bleeders. Calculating the amount of dietary iron necessary to compensate for iron losses is complicated by the different chemical forms of iron found in food. Essentially it exists in two forms, haem iron and non-haem iron. Haem iron is relatively well absorbed and the NRC has stated (1) that the proportion can be as high as 23 per cent. The non-haem iron has a variable absorption and is affected by a number of factors, including the amount of dietary phytate that can bind iron and make it unavailable. This can be a particular problem in cereal foods, which are the basis of most people's diets in the developing world.
Ascorbic acid can enhance the absorption of non-haem iron, and there are also reports that the presence of haem iron can increase the absorption of non-haem iron. Thus it is clear that subtle changes in dietary composition can greatly affect the intrinsic value of a given food.
The intestine is the main organ of homoeostatic control. It is estimated that the customary efficiency of iron absorption from a Western diet is about 10 per cent of that ingested. When this become insufficient to meet needs, however, such as may occur during pregnancy, lactation, or after bleeding, or when iron intake is low, the efficiency can increase up to 20 or 30 per cent. There is a clear need for more detailed work on iron requirements to be carried out before meaningful RDAs can be defined. Such studies will need to take full account of local dietary habits, the iron state of individuals, and overall food composition.
In considering the needs of lactating women it is, as with most nutrients, difficult to separate considerations of pregnancy from those of lactation. To some extent the extra needs of the foetus and milk production are compensated for by absent or reduced menstruation losses. In the industrialized countries it is recognized, however, that at least during pregnancy the woman may not be able to satisfy her iron needs from dietary sources alone, and hence administration of iron-containing tablets is considered necessary. The NRC has recommended that for American women this prophylactic procedure should continue post-parturition, at least for the first two to three months, to restore iron reserves to pre-pregnancy levels. This would be of particular importance in those who are actively lactating, especially those who lactate for extended periods of time after menstruation may have returned.
In the developing world these clinical services may be totally absent. It is important not just to consider this in terms of anaemia; the socio-economic implications are just as crucial. Many women are forced to engage in heavy manual labour but their work capacity may well be impaired by iron deficiency, as has recently been demonstrated in Sri Lanka (P.E. Sousa, personal communication). It has to be accepted that there will be a considerable portion of women for whom dietary sources of iron will be totally inadequate and from whom repeated pregnancy-lactation cycles will take an increasing toll.
1.18. Zinc. Zinc is a mineral that has been of increasing interest to nutritionists studying human dietary requirements in recent years. Zinc is predominantly found in animal foods. It is also present in cereal products, amounts depending on the zinc content of the soils in which they were grown, but availability may be low due to binding with phytates. The most authoritative set of recommended dietary allowances for zinc and other trace elements are those of the American NRC(1). In practice, a high zinc intake is dependent on the proportion of animal foods consumed. Data from the developing world are indicative of potential deficiency even in non-lactating women. As with calcium, however, it seems not unlikely that need and efficiency of utilization will depend on the dietary level to which the individual has become accustomed, and uncritical extrapolation from American experiences to the developing countries may not be fully justified.
The RDA for zinc, as judged by the NRC, for non-pregnant, non-lactating women is 15 mg/d and an extra 10 mg is recommended for lactation. This 6070 per cent increase, which is considerably in excess of the dietary energy intake, could only be achieved in the developing world by a major switch to animal products in the diet. As with iron and calcium, it would be a very enlightened community indeed that provided a woman with a diet of considerably enhanced desirability compared with what the rest of the family were eating, especially the men!
1.19. The list of nutrients considered essential for human health is constantly increasing and it would not be practical to discuss each and every one. The ninth edition of the NRC's Recommended Dietary Allowances (1) has included six additional trace elements - copper, manganese, fluoride, chromium, selenium, and molybdenum - in addition to sodium, potassium, magnesium, and iodine. There are, however, no special allowances made for lactation and one must assume that the basic allowance should be supplemented either to make an allowance for the quantities of nutrients secreted into the milk or, alternatively, in line with enhanced recommendations for dietary energy.
Some of the trace elements raise an additional problem in that they can be toxic at high intakes and thus upper safe levels are also supplied. It is unlikely, however, that these levels would ever be exceeded in a normal diet, and upper limits really act as a warning to those who may be tempted to consume excessive amounts of proprietary preparations. For lactating mothers in the developing world the major concern is more the impossibility of achieving anything approaching the lower safe level in a diet virtually devoid of animal products.
1.20. It is quite apparent that there are numerous major gaps in our knowledge about physiological responses during lactation that make the definition of meaningful recommended allowances for individual nutrients difficult. It is also clear that interaction between nutrients is a topic the importance of which has been grossly underestimated. Likewise, metabolic adaptation to low intakes leading to enhanced digestion, absorption, and utilization of dietary constituents also needs to be investigated. This is particularly important for the lactating mother who, for most nutrients, has a significantly greater recommended allowance than any other member of the household, including the husband.
On the basis of current recommendations, the quality of the diet in terms of the amount of nutrient per 1,000 kcal needs to be much better during pregnancy and lactation. If this is true, one would be shutting one's eyes to reality not to recognize the social improbability of such a recommendation ever being put into practice by a poor family in the developing world. Metabolic adaptations might minimize the need for such changes, but it is essential to examine the cost of such adaptations.
A woman plays a multiplicity of functions in addition to baby and milk production. In most communities she is an essential component of the country's agricultural economy; one needs to ensure that her capacity for work has not been compromised. Additionally, it is always possible that, while current function can be maintained at a reasonable level on a low nutrient intake, deficiencies may build up that can impair health and well-being later in life. The poorer countries of the world may well be forced to make sacrifices in this regard as part of the cost of achieving ultimate economic improvement. Be this as it may, scientists should clarify the health consequences of such politically motivated decisions and, wherever possible, develop sufficient factual understanding so that the worst effects can be alleviated.