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If women in Bangladesh were to use contraception while they were breastfeeding, what would be the result?
I think the answer is that there is no reason to overlap other means of fertility control with breastfeeding in the first six months of life.
But what if breastfeeding were to be replaced by a contraceptive device?
If you look at Hong Kong as a developing country, you find limited breastfeeding and massive use of contraception, leading to very low fertility (see table 5). If you look at the developed countries in the same table, it was assumed women breastfed for three months, but for most of those countries, breastfeeding was actually very limited. The damping of fertility came about through contraceptive use, so that if contraception is effective enough, it has a far more powerful effect overall than breastfeeding. Lactational amenorrhoea only prolongs birth intervals by a maximum of, say, 18 months. Long-term contraception can prolong them very much more, so that breastfeeding is not a competitor in the statistical race.
No, no. You have not answered my question. You shifted to Hong Kong. I am asking you about Bangladesh. If you replaced breastfeeding by contraception in the Bangladesh conditions, what would happen?
In Bangladesh fertility has dropped radically as a result of family planning. There's been a long-term family planning programme that has offered contraception within people's homes in a society in which purdah is the common practice, so that women don't move freely out of their homes. The total fertility rate in Bangladesh is now under five, probably closer to four, and that decline has been achieved through the adoption of contraception. There has been some drop in breastfeeding, but it's mostly contraceptive use in combination with breastfeeding. Now, if you were to substitute poor contraception for the very good lactation practices (in terms of fertility-reducing effects), you might have a different effect. Suppose, for instance, you took women just post-partum and urged them to use DepoProvera and gave them the injection. If they stopped lactating and after three months decided they didn't like Depo-Provera, what would happen? Fertility would go up. But that has not happened in most societies.
What one wants is to promote a system in which women can lactate, but not necessarily forever, if that means they can't work. One wants to promote a society in which women can combine these various roles. We need to try to make it feasible to breastfeed enough to benefit the child and to have fertility-controlling effects.
Two small questions. One is very technical about Dr. Bongaarts' list. He speaks of the biological probability that conception will follow a single act of intercourse. What can he mean by that? A single act of intercourse has a probability that changes along the menstrual cycle. It is zero for most times of the cycle. Even in the fertility window, it is not a rectangular distribution. The second question is this. In aggregating studies of historical demography, it has been found that there was a seasonal pattern in the birth rate. If we now compare the seasonal pattern north of the equator, it is opposite to that south of the equator. Is that biological or is it social?
Those are very good questions. I have been intrigued by the profound seasonality in fertility in Bangladesh for the last 20 years. Close to 50% of births occur in four months of the year, and you see this year after year. Some people said it was nutrition, and we did everything up, down, and sideways that we could do as demographers and yet found very little effect of nutrition. It turns out there is profound seasonality in the introduction of supplementation, that is, the move from full to partial breastfeeding. That appears to be related to the needs of the agricultural calendar and the jobs that women do. This move to supplementation appears to determine a great deal of the seasonality. We are about to do a study in Bangladesh, trying to measure ovulation to see whether there are differences in different seasons of the year, or whether differences in the intensity of breastfeeding explain part of the seasonality.
So it's not a difference in the frequency of intercourse?
My hypothesis at the moment is that there are real differences in frequency of intercourse in different parts of the year. It would seem to me that seasonality is almost entirely socially determined, so it is not surprising that seasonality is different in different parts of the world, especially north and south of the equator.
Could you respond to Dr. Colombo's other question about what Bongaarts meant about the chance of pregnancy?
If one figure is given, it is usually an average taken over the course of the month, so that if you assume there was a random chance of intercourse on any day, that average probably would apply. Bongaarts does include in his discussions of fecundability models the variation over the menstrual cycle in the probability that conception follows a single act of intercourse.
I have a comment on the statement that breastfeeding has no effect on mortality after 12 months of age. I am not sure the literature is very clear-cut on that. I know at least two or three good studies that have shown an effect. The literature on morbidity certainly shows that the incidence of the number of infectious diseases is higher among nonbreastfed children, even after one year of age. The protective effect certainly goes down with age, but I think it's hard to draw a line, particularly in societies where the alternative to breastfeeding, even in the second year of life, will certainly expose the child to a high level of infection.
The data that I was referring to came from several countries in Latin America. These are reports rather than prospective studies. There is no question that the benefits of breastfeeding are greatest for the poorest. Those who have the least access to other alternatives protect their children the most through their breastfeeding practices. In fairly careful searches of the literature, the large population samples I found have not shown any significant effect after the first year. It is an important area of research, and I'd like to see the references you have. I should add, though, that even if mortality consequences exist, by that age overall mortality rates have gone down enough that even if the relative risk is high, it's not going to have a large effect on the overall mortality.
In support of what you've just said, we followed a very large cohort of children prospectively in Pakistan, and it turned out that 90% of the infant mortality occurred before the age of six months; 34% occurred in the first week of life. Mortality is, indeed, very early.
Thank you again. Our last paper today is by Dr. Kathleen Rasmussen. We've heard a lot so far about the benefits of breastfeeding for the baby, the effects of breastfeeding on fertility, but Dr. Rasmussen is going to tell us about the effects of breastfeeding on maternal health and well-being.
Kathleen M. Rasmussen and Michelle K. McGuire
Lactation occurs as part of a reproductive and may have different effects on maternal nutritional status, depending on its duration and intensity. Thus, its effect on maternal health will differ with cultural setting and level of development. Lactation helps women to maintain a healthy body weight. Among well-nour-shed women, it may help to prevent obesity. Among poorly pour/shed women, breastfeeding also leads to weight loss, but with adequate birth spacing brought about by lactational anovulation, maternal depletion can be avoided. Lactation is probably not responsible for osteoporosis. Current evidence suggests that breastfeeding helps to prevent pre-menopausal breast cancer and is not associated with post-menopausal disease Furthermore, breastfeeding may also help reduce ovarian cancer. Positive effects of breastfeeding occur at all levels of development and are most likely when biological, political, and sociocultural conditions interact to support its initiation and continuation.
The effects of lactation on maternal health and wellbeing are many and varied. For example, lactation helps women maintain a healthy body weight. This is perhaps the most obvious biological effect of breastfeeding on women's health and is one that will be considered in detail. In addition, the hormonal changes characteristic of lactation influence maternal behaviour in ways that are supportive of both breastfeeding itself and positive mothering behaviours in general [1-4]. There is even evidence from animal studies that there are factors in milk that influence the behaviour of the nursing young [5, 6].
Lactation occurs within a reproductive cycle
Lactation occurs as part of the reproductive cycle, and it may have different effects on maternal nutritional status, depending on its duration and intensity. Each time a woman reproduces, she goes through the cycle diagrammed in figure 1.
Each cycle may have very different characteristics. For example, the child could die in the neonatal period, and the cycle would then be very short. Alternatively, the woman might become pregnant while still breastfeeding; in this case there would be no non-pregnant, non-lactating interval. The woman and her husband could adopt some effective means of birth spacing and thus prolong the non-pregnant, nonlactating interval substantially.
The biological effect of breastfeeding on the nutritional status of the mother needs to be evaluated in the context of the whole reproductive cycle . This is because some portions of the reproductive cycle deplete the mother, and some periods allow the mother to gain. Breastfeeding is commonly thought of as a time of depletion, but this is probably true only of the period of exclusive breastfeeding. Even this is not so in severely undernourished experimental rats, which actually gain fat while their nursing pups are starving .
In contrast, the period of partial breastfeeding may be one of repletion, and the longer it is, the more repletion may be possible . Inasmuch as breastfeeding itself delays ovulation and therefore conception, breastfeeding may be associated with first depletion and then repletion of the mother. It is expected that the non-pregnant, non-lactating interval will serve as an opportunity for repletion. This assumption requires that the woman's food intake remain the same after the caloric demand of lactation has been removed and also that her workload does not increase above that which she experienced while nursing her infant. These assumptions may or may not be true and must be evaluated in a particular cultural or individual context.
FIG. 1. Diagram of the reproductive cycle showing birth interval and the periods of maternal depletion and repletion. *Non-pregnant, non-lactating
It should be clear, therefore, that the effects of breastfeeding on maternal health will be different in different cultural contexts or at different levels of development. The effects of breastfeeding on maternal health will also depend on the usual practices for exclusive or partial breastfeeding and on birth spacing. The effects of reproduction on a woman's health are cumulative over her lifetime, but because of the possibility that reproduction will result in net positive or net negative effects, the effects are not a simple multiple of the number of children borne. A more sophisticated analytical approach than this is needed if we are to understand the cumulative effects of reproduction, including lactation, on maternal health .
Lactation affects maternal health and well-being
Change In body weight
Women gain weight and body fat during pregnancy and tend to lose it during lactation . The amount of weight gained during pregnancy is higher with better living circumstances . The amount of weight retained after delivery shows this same discrepancy between poor and rich countries. In the United States, the rate of weight loss post-partum is often higher among lactating women than among non-lactating women (assuming that the women are not consciously dieting) . The rate of weight loss is not constant . It is greatest in the first few months postpartum and slows as solid foods are introduced into the infant's diet. Women may gain weight during partial breastfeeding and are especially likely to do so after weaning their infants.
Prevention of obesity
Among well-nourished women, lactation may help to prevent the weight and fat retention often associated with child-bearing. In fact, the effect of breastfeeding on helping a well-nourished woman return to a healthy body weight after delivery is fairly dependable . Weight retention at the end of a reproductive cycle is influenced by the intensity and duration of breastfeeding. The data of Öhlin and Rössner  from Swedish women illustrate this point. They developed a "lactation score" that combined frequency and duration of breastfeeding. Among their subjects, weight loss from 2.5 to 6 months postpartum was greater as the intensity of breastfeeding increased. All women, however, lost weight in the subsequent 6 months, whether they breastfed or not, and the total weight loss after 12 months was the same among those who had been intensive breastfeeders as it was among those who had not. Unfortunately, in this study the investigators did not measure the weight change that occurred during the first 2.5 months post-partum, the time of greatest weight loss among breastfeeding women.
The data of Forsum and her co-workers  also provide information about the change in body fat that occurs during pregnancy and lactation among well-nourished women. They studied 22 Swedish women before and during pregnancy and during the first six months of lactation. Although by six months post-panum, women in this population of enthusiastic breastfeeders had lost nearly all of the weight and several kilograms of the fat that they had gained during pregnancy, they still retained almost 4 kg of the fat that they had gained. This fat was available to support continued breastfeeding in the second half of infancy and beyond. Unfortunately, no comparable data are available for non-lactating women.
In contrast, women living under poor circumstances are concerned about becoming too thin as a result of childbearing.* Data from more than 1,000 women in the Cebu Longitudinal Health Study in the Philippines  show that the direction of weight change in the post-partum period is associated with maternal weight immediately after delivery. Those who were the heaviest at this time gained weight during lactation, but women in other groups lost weight. Longer birth spacing might allow women in the other groups to return to their prepregnant weight before conceiving again.
A particularly relevant recent study  from Bangladesh goes even further. It accounts for initial maternal weight, duration of breastfeeding, and season in examining the effect of breastfeeding on maternal weight change. Weight loss was higher in lactating than in nonlactating women, and lower in women with low initial weight than in those with high initial weight. In this study, the rate of weight loss was highest 5 to 9 months post-partum and was near zero at 16 months post-partum. After this time, women gained weight. Nevertheless, season and time postpartum interacted so that women who reached the time of most intensive breastfeeding at a time of low food supply lost the most weight. Each additional birth was associated with a 280 g decrease in the mother's weight at conception. Furthermore, interpregnancy intervals of less than 18 months were far more important: each of these was associated with an 800-g decrease in the mother's weight at conception. The authors concluded that "women in Bangladesh have the potential to regain the weight they lose during the first 15 months or so of lactation despite a high and varying level of nutritional stress," but that this depends on adequate spacing between pregnancies to permit a woman to replace her reserves.
In summary, like their better-nourished counterparts, women living under poor circumstances lose weight during lactation. Furthermore, their weight loss is magnified by seasonal changes in their environment. Nonetheless, with adequate birth spacing brought about by lactational anovulation, women living under poor circumstances should be able to maintain a healthy body weight from one reproductive cycle to the next.
Changes in incidence of chronic diseases
As women live longer, osteoporosis is becoming a much more serious problem [17, 18]. It has been postulated that lactation might contribute to the development of osteoporosis because so much calcium is transferred from the mother to the infant in the milk during breastfeeding. Although the rate of calcium transfer from mother to infant is actually higher during the third trimester of pregnancy than it is during lactation [19, 20], the total amount of calcium transferred may be greater during lactation than during pregnancy if lactation is long enough . However, many features of calcium metabolism change during lactation to compensate for the high rate of transfer of calcium from the mother to the infant . For example, the rate of bone resorption increases , and renal calcium conservation also increases [20, 23].
Research presented or published recently shows clearly that bone mineralization returns to normal after lactation among well-nourished women with ample calcium intakes [21, 24]. The shorter the period of lactation, the sooner bone mineralization returns to normal. Nevertheless, if birth spacing is adequate, bone mineral densities will have returned to pre-pregnant values before the next conception. In a recently completed year-long trial, the milk calcium output of calcium-supplemented Gambian women with habitually low calcium intakes did not increase, and neither did bone mineral content . Bone mineral content, however, did not decline during the first year of lactation, as has been previously observed among women with higher calcium intakes.
The effect of breastfeeding on hip fracture, one of the most debilitating consequences of osteoporosis, has not been studied often, but the three studies that have investigated this association among women living under good circumstances have come to the same conclusion . In all of them, there was a reduction in the incidence of hip fracture with increased duration of lactation.
Thus, it appears that lactation per se is probably not responsible for osteoporosis or its consequences. A woman's body can adapt to varying calcium intakes and lengths of lactation. Thus, this concern, although intriguing at one time, can now be eliminated.
It has long been known that the incidence of breast cancer is associated with a woman's reproductive history. In particular, breast cancer is higher among women with late onset of menstrual periods, late age at first birth, and few total births . Evidence of an association between lactation and breast cancer has been inconsistent [27, 28].
The most recent work , using a large sample of women from a multicentre case-control study, showed that breastfeeding reduces the risk of pre-menopausal breast cancer in a dose-dependent fashion (the longer the total period of breastfeeding, the lower the risk of breast cancer). In the same study, there was no association of lactation with post-menopausal breast cancer. Many researchers think that breast cancer in these two periods has different origins, so this lack of consistency is perhaps not surprising. In summary, the current evidence points to a beneficial effect of breastfeeding in preventing premenopausal breast cancer, and no association of breastfeeding with the post-menopausal disease.
There are also conflicting findings about a possible association of breastfeeding with ovarian cancer. In a recent multicentre collaborative study, there was a 20% reduction in the incidence of ovarian cancer with lactation , but this was not statistically significant. Nevertheless, the reduction in cancer incidence with increasing time spent pregnant was even greater. The authors speculate that this is because pregnancy is even more effective than lactation in suppressing ovulation.
Overall, we can say that lactation is not responsible for increasing the incidence of some chronic diseases in women and, in the case of pre-menopausal breast cancer, probably has a role in preventing this condition.
The effects of lactation vary with the circumstances of the woman's life
For women living in traditional societies (fig. 2), investigators have historically been concerned about undernutrition. In this situation, breastfeeding has both direct effects on maternal health and wellbeing and indirect effects that are mediated through fewer reproductive cycles. Some of the effects on the mother benefit the infant, in addition to the nutritional value inherent in the direct transfer of human milk. The infant also benefits from breastfeeding indirectly from the lengthening of the birth interval.
In transitional societies there is now concern about overnutrition in addition to concern about the undernutrition that skill remains. This creates a more complex picture than the last, because chronic diseases, particularly those associated with obesity, are becoming a problem (fig. 3).
In industrialized societies the concern is primarily about overoutrition and the "diseases of affluence." In this situation few women use breastfeeding for birth spacing, so the indirect effects of breastfeeding on maternal and child health via prolonged birth spacing are eliminated, but the direct effects remain and are important (fig. 4).
FIG. 2. Diagram showing how breastfeeding affects maternal and child health in a traditional society. Note that the effects of breastfeeding are both direct and indirect, via its effect on reducing the number of reproductive cycles
FIG. 3. Diagram showing how breastfeeding affects maternal and child health in a society in transition. Note that the effects of breastfeeding are both direct and indirect, via its effect on reducing the number of reproductive cycles
FIG. 4. Diagram showing how breastfeeding affects maternal and child health in an industrialized society
FIG. 5. Factors required to realize the benefits of breastfeeding for maternal and child health. Note that the appropriate biological, sociocultural, and political factors must all be present for the maximal positive effect
Conclusions and implications
This article has focused on the biological ways in which breastfeeding affects maternal health and well-being. To achieve these benefits, women must initiate and continue breastfeeding. As described earlier, for this to occur, the biological, political, and sociocultural environments must interact in a way that is supportive of breastfeeding (the shaded area of fig. 5).
As the figures illustrate, this interaction occurs in different ways under different living conditions. Appropriate interventions to promote and sustain breastfeeding will, therefore, differ with the circumstances. For example, in societies in which breastfeeding is the usual practice and mother and infant can be together all day, the usual activities to promote initiation of breastfeeding can work well. This may involve, for instance, supporting the Baby-Friendly Hospital Initiative. Supporting an adequate duration of breastfeeding and the timely introduction of complementary foods is more difficult but is, nonetheless, important. This may involve developing policies that are not now in place, especially for women who work in the informal employment sector. The principal future threat is urbanization and disruption of the culture in which breastfeeding is the norm.
In societies in which breastfeeding is not the usual practice, there are other concerns. In these societies, just getting women to consider breastfeeding is a problem, because there are strong societal pressures against starting to breastfeed. Therefore, supporting women to initiate breastfeeding in a relatively hostile environment is necessary, and this means more than just following the principles that are part of the Baby-Friendly Hospital Initiative. There are also pressures against women continuing to breastfeed. This is because women have taken on new roles in society that separate them from their infants and are living in situations in which their infants cannot be cared for by relatives. Thus, better maternity leave policies need to be developed, and child care near the mother's place of employment also needs to be provided.
In summary, lactation influences maternal and infant health in a number of positive ways. These vary with the circumstances in which women live, but positive effects are present at all levels of development. These positive effects of breastfeeding are most likely to occur when the biological, political, and sociocultural environments interact in ways that support both the initiation and the continuation of breastfeeding.
The thoughtful comments of Drs. Jean-Pierre Habicht, Cutberto Garza, and Grace Marquis are greatly appreciated.
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