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The effects of lactation on the mother
The effects of lactation on the mother Imogen S. Rogers*, Jean Golding, Pauline M. Emmett Unit of Puediatric and Perinatal Epidemiology, Institute of Child Health, llniversity 24 Tyndall Avenue, Bristol BS8 1TQ. UK
qf I3ristol.
-Abstract Undernourished mothers are likely to have limited fat reserves to draw on during lactation. In order to supply nutrition to her child the mother may therefore become more malnourished and suffer from bone resorption. Repeated or overlapping pregnancies with lactation are likely to compound the issue. Little research has been carried out into the health of mothers while breast feeding, or subsequently. There are theoretical reasons to think that the malnourished mother in the developing world may be particularly vulnerable, but no studies appear to have been undertaken. Investigations in the developed world have concentrated on cancers of the reproductive organs and shown consistent evidence in large case-control studies for a reduced risk of pre-menopausal breast cancer in mothers with a history of prolonged breast feeding. In contrast there have been a number of studies in the developed world concerned with emotional well-being with some indications that mothers who breast feed are more likely to be depressed and are less likely to be positive about their baby. 0 1997 Elsevier Science Ireland Ltd.
1. Introduction
Most breast feeding mothers are aware that whilst breast feeding they are in a different psychological and physical state than when not breast feeding. Whether this has any effect on their current and future health and well-being has received little discussion. In this paper we examine the evidence for relationships between lactation and the nutritional status, health and well-being of the mother in both the short and long term, distinguishing where we can between effects on malnourished and well-nourished mothers.
*Corresponding author. 037%3782/97/$17.00 0 1997 Elsevier Science Ireland Ltd. All rights reserved PII
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2. Nutritional
needs of lactating mothers
In the exclusively breast-fed infant the mother must supply all the nutrients needed for growth and maintenance by that infant. The resulting nutritional demands on the mother are considerable, far outstripping those of pregnancy. The Committee on Medical Aspects of Food Policy has estimated the average energy cost to the mother of lactation in the third month post-partum to be 690 kcal per day, and the estimated requirements of most other nutrients have an incremental value added for lactation [13]. It was assumed by the committee that about 120 kcal per day of the energy cost of lactation would be met by mobilization of a maternal ‘energy reserve’ consisting of 2-2.4 kg of adipose tissue deposited during pregnancy. Women in many developing countries will not gain nearly this amount of adipose tissue during pregnancy. For example, a longitudinal study of 2500 women in Matlab, Bangladesh [24] found that not only did they commence pregnancy with a poor nutritional status (mean pre-pregnant arm circumference was only 22.1 cm as compared to 26 cm in US women) but weight gains during pregnancy were extremely small (4.8 kg on average as compared to 12.5 kg for British women). Judging by arm circumference, mothers in Matlab had lower stores at the end of pregnancy and at three months post-partum than prior to pregnancy. Lacking the fat and muscle reserves to help them cope with the nutritional demands of lactation these women would need a higher energy intake or a more reduced energy expenditure than better-nourished women to prevent their stores becoming further depleted. However, it is very likely that their energy intake during lactation also fell short of the recommended values. 2.1. Effects of lactation on maternal nutritional
status and bone mass
Much of the available evidence suggests that in the malnourished mother the quality and quantity of the breastmilk will be maintained at the expense of maternal health. For example, in a study by Prentice et al. a high-energy dietary supplement was given to lactating Gambian women [37]. Consumption of the supplement did not cause any change in the energy content of the breastmilk produced. However, it appeared to result in an improvement in the health of the supplemented women. There was an average weight gain of 1.8 kg over the course of a year of supplementation, markedly improved riboflavin status and a decrease in the incidence of gastrointestinal problems and upper respiratory tract infections. Plasma levels of prolactin, insulin and T, were all lower in supplemented than unsupplemented women, as was cortisol in the early post-par-turn period. The authors suggested that the higher hormone concentrations in unsupplemented women were ‘part of a concerted endocrine response to maintain milk output in spite of considerable metabolic stress on the mother’this response could be relaxed on receiving supplementary food. In a study of 26 lactating Nepalese women the calcium concentration of the milk was found to be similar to that of American women despite their having less than half the dietary intake [32]. These Nepalese women had an elevated excretion of hydroxyproline, suggesting that milk calcium concentrations were maintained by an
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increasein bone resorption, creating a risk of bone demineralisation. Anthropometric measurements of these women suggested mild protein-energy-malnutrition (e.g. evaluating by arm circumference [17] 54% were below the 5th percentile for protein reservesas compared to the 1971-4 HANES survey of US women [34]), there was also evidence of multiple infections and some of the women showed signs of B-vitamin deficiency [39]. In contrast their breast-fed infants appearedhealthy, with low-normal weight and length for age and no physical signs of mdnutrition. implying that breast milk production had been maintained at the expense of the mother’s health. Several other studies have suggesteda negative effect of lactation on the bone mass of the mother. Atkinson and West measuredthe mineral loss from the femorai shaft during lactation in ten British women and found an average loss of 2.2% over 100 days [6]. Wardlaw and Pike compared fore-arm bone mass in two groups of women each of whom had breast fed three or four children - a long term lactation group (n = 10, averageduration of lactation = 10.7 months for each child) and a short term lactation group (n = 11, average duration of lactation = 2.8 months per child) [49]. Bone mass was significantly lower in the longer term breast-feeding group, and in this group calcium intakes considerably above the RDA did not protect against bone loss. A study of lactating adolescentsfound that a group who consumed around 900 mg calcium/day lost 10% of their bone mineral content over 16 weeks of lactation. However, in an experimental group consuming at least 1600 mg/day this bone mineral loss was prevented [lo]. A study by Drinkwater and Chestnut [ 151 showed that the effects of lactation on bone mineral density varied from site to site. They measuredthe bone mineral density of six women at seven sites, before pregnancy, within six weeks of parturition and after six months of lactation, and also measured the bone mineral density of 25 non-pregnant controls of similar age, height, weight and activity level during the sameperiod. During pregnancy there was a decreasein bone mineral density at the femoral neck and radial shaft (while this remained constant in the non-pregnant women) and an increase in bone mineral density of the tibia in both the pregnant women and the controls (this was the only significant changein bone density observedin the controls during the study). After six months of lactation the bone density of the radial shaft had returned to pre-pregnancylevels, but the density of the femoral neck had declined further. The long-term effects of lactation on bone mineral density are unclear. A study by Kent et al. of bone turnover during and after lactation suggestedthat the bone mineral content lost during lactation is replaced during the weaning period [23]. This is concordant with the results of a survey of American women in Washington which found the risk of hip and forearm fracture to be unaffected by parity and duration of lactation [4]. Furthermore, a separateanalysis of hip fracture only suggesteda slight protective effect of increased months of breast feeding. 2.2. Overlap of pregnancy and lactation
Pregnancy and lactation both impose a nutritional strain upon the mother. Various social and biological factors operate to decreasethe chancesof these statesoccurring simultaneously. Lactation results in hormonal changeswhich depressfertility [40], in
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addition the steroids of pregnancy inhibit the onset of lactation [28] (although not preventing it if it is already established). In many societies there are taboos against sexual intercourse during the period of lactation. Conversely, pregnancy is often cited as a reason for weaning [48], the belief being either that continuing breastfeedingwill result in damageto the fetus or that pregnancy in some way ‘spoils’ the breast milk. Despite this, pregnancy and lactation frequently do overlap. Such a situation might be expected to impose a particular threat to the nutritional status of the mother. A study in Guatemala set out to investigate the effect of overlapping pregnancy and lactation on maternal nutritional status [30]. The effect of the length of the ‘recuperative period’ between the weaning of one child and the conception of the next was also examined. This recuperative period, being free of the nutritional stressesof pregnancy and lactation might allow the mother to replenish stores depleted by these processes. The Guatemalan study found evidence that lactation concurrent with pregnancy and short recuperative intervals were nutritionally stressful conditions, resulting in increasedfood supplement intake by the mother and reduced maternal fat stores. They recommended that to reduce the risk of depletion in women with marginal energy intakes their pregnancies should be well spaced,such that the next conception occurred more than six months after weaning the previous child. 2.3. Effects of lactation on bodyweight
It has been widely assumedthat the fat stores deposited during pregnancy in both well-nourished women and animals representa reserveto support the energy demands of lactation. Similarly, the decreasein body weight and body fat of many mothers during lactation is presumedto be a result of the energy demandsof lactation. These assumptionshave been challenged by Dugdale et al. [16], who measuredchangesin maternal bodyweight from one month to twelve months post-partum. They found a pattern of weight loss from the first month until the sixth month. However, this weight loss was unrelated to duration of breastfeeding, implying that the negative energy balance causing it could not be ascribedto lactation. Desire to lose weight had a significant effect on the amount of weight loss, suggestingdeliberate maternal food restriction was an important factor. Quandt measuredbody fat changes in lactating women over six months and found an increase in adiposity in the majority of them (29 out of 46) [38]. However this finding was based largely on changes in triceps skinfold. This may increase after pregnancy due to a redistribution (rather than an increase) of fat stores. Brewer et al. comparedthe weight and body fat changesin three groups of women (exclusive breast feeders, combination breast and bottle feeders and bottle feeders) during the first six months after delivery [7]. They also found that the feeding regime made no difference to the total weight loss of the women over the six month period. However, the pattern of weight loss was different with only the breastfeedinggroup experiencing a significant weight loss from the third to the sixth month after delivery, even though the mean (S.D.) energy intake was considerably higher in both groups of lactating women (2055(435), 2005(515) and 1453(503) kcal/day in exclusive breast, supplementedbreast and bottle feeders respectively). A study by Dewey et al. also
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found a particularly marked difference between the weight loss of breastfeedingand formula feeding women from the third to the sixth month post-partum [14]. In their group the breastfeederslost more weight than the formula feeders over the first twelve months (4.4 vs. 2.4 kg). They also lost triceps skinfold thickness from nine to twelve months post-partum, while formula feedersgained it. It may be that the effect of breastfeeding on changes in maternal bodyweight is only apparent when breast feeding is continued for more than six months.
2.4. The energy cost of lactation
The effect of lactation upon post-partum weight loss will depend largely on its energy cost. This remains a matter of debate. Many women in developing countries produce sufficient breast milk to sustain satisfactory growth in their infants for several months despite energy intakes considerably below the recommendedlevels. In some extreme casesof food shortage a degree of maternal depletion may result. However, there are several reasons to believe that successful lactation may occur in women consuming considerably less energy than currently recommendedwithout the risk of maternal depletion. The results of several studies of well-nourished lactating women suggestthat then actual energy requirements are lower than the acceptedestimates.Butte et al. looked at the bodyweight changesand dietary intake in 45 well-nourished lactating American women at the first, second, third and fourth months post-partum [8]. They found a gradual decline in maternal bodyweight over the four months, with an estimated energy contribution of 156 kcal/day from maternal body stores- similar to the 120 kcal assumedin the COMA report. However, me energy intakes were lower than the COMA recommendationsat all stages.Brewer et al. consideredthat at energy intakes of around 2500 kcal/day body fat losses in lactating women would be unlikely to occur. In the exclusively breast feeding women in their study a dietary intake of 2055 kcal/day produced only a 225 kcal loss from body fat stores [7]. Van Raaij et al. also considered the estimated energy requirements of lactation to be too high. They found lactating Dutch women to consume only 289 kcal/day more at nine weeks postpartum than at twelve weeks gestation, or 415 kcal more than at one year post-parturn [47]. These women lost no body fat during the first two months post-partum. In 23 lactating Swedish women the energy intake two months after delivery was only 280 kcal/day greater than before pregnancy, and no body fat was lost during these two months of lactation [43]. The apparent overestimate of the energy cost of lactation could arise for several reasons. It may be that the estimates of the volume of milk produced or its energy value are too high (as the results of studies using doubly labelled water would suggest 1261).An efficiency value of 80% is assumedfor the conversion of maternal dietary energy to gross milk energy. It is possible that the true efficiency is higher than this. However, even assuming an efficiency of 100% would lead to only a small reduction in the estimatedenergy requirements. Another possibility is that the energy needsfor maintenance and physical activity are lower in the lactating woman. Energy
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requirements could be reduced by a reduction in physical activity or an increase in metabolic efficiency. 2.5. Changes in metabolic efJiciency during lactation
The evidence for changesin metabolic efficiency during lactation is contradictory. Illingworth et al. found metabolic efficiency to be greater in lactating women than in bottle-feeding women or non-pregnant, non-lactating controls [22]. The increase in metabolic rate in responseto a meal or an injection of noradrenaline was lower in the lactating women. When the women were remeasuredafter the complete cessation of lactation their metabolic responsesto noradrenaline or a meal had increasedto normal levels. The authors suggestedthat thesemetabolic changeswould result in a reduction of the non-lactational component of energy expenditure in lactating women. Lactating Phillipine women were found to have a lower basal metabolic rate (BMR) at six, twelve and eighteen weeks post-pat-turnthan at thirteen weeks gestation [19]. Von Raaij et al. also found a reduced basal metabolic rate in lactating women at nine weeks post-partum compared to the twelve weeks gestation values (a similar reduction was found in non-lactating women) [47]. The basal metabolic rate was also lower than at twelve months after delivery, suggesting an ‘enhanced efficiency of energy metabolism throughout the first three months’. In addition a study by Motil et al. suggeststhat nitrogen metabolism is altered in lactating women [33]. On intakes of 1 g protein/kg/day the urinary 3-methylhistidine excretion was lower in lactating than non-lactating women (106.5(27.7) and 150.7(55.6) kmol/day respectively). The authors suggested that this represented an adaptive metabolic response to reduced protein intake in the lactating women, promoting the conservation of skeletal muscle protein stores. However, the resting metabolic rate of Swedish women was found to be higher during lactation than before pregnancy [43]. In addition Illingworth et al. found no difference between the resting metabolic rates of the three groups of women studied (although the numbers were relatively small) [22]. 2.6. Changes in physical activity level during lactation
It may be that some lactating women are constrained from reducing their physical activity level (PAL) by occupational demands.However, where a decreasein PAL is possible it would obviously reduce the increase in energy requirements associated with lactation. The literature on PAL changesduring lactation is inconsistent. Some studies have found a reduction. The measuredPAL of well-nourished lactating Dutch women was 1.47 X the basal metabolic rate (BMR) at 5 weeks post-partum and 1.51 X BMR at 27 weeks [47], significantly lower values than the measuredPAL at 56 weeks post-partum (1.54 X BMR). This suggestedthat in this group some of the energy cost of lactation was met by a reduction in physical activity. However, there was no difference in the measured PAL of 23 lactating Swedish women before pregnancy and at 2 months post-partum [43]. Based on 24-h activity records Brewer et al. found no difference between lactating and non-lactating women in the predicted energy needs for maintenance and activity. In Filipino women the measured PAL
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increased from 1.61 X BMR at 6 weeks lactation to 1.80 X BMR at 12 weeks and 1.97 X BMR at thirty weeks [ 191. This represents a very high level of physical activity - the estimated energy expenditure of a British woman with a moderate/ heavy occupation and very active leisure activity being 1.7 X BMR [ 131.The PAL at 13 weeks pregnancy was similar to the value at 12 weeks lactation (1.77 X Bh4R). Thus the PAL of these women did not appear to be reduced beyond the first few weeks of lactation.
3. Psychological
effects during lactation
We could find no studies that specifically startedwith the aim of looking at the way in which the breast feeding mother differed in terms of post-pat-turn blues and post-natal depressionfrom the mother who was bottle feeding. There are, however, a number of studies of post-party blues and post-natal depressionthat have incidentally documented whether the mother was breast feeding or not. Six studies have indicated an increased depression rate among the breast feeders. Dalton [l l] found an increased depression rate in those mothers who were breast feeding at two months. Alder and Cox [3] found that those who were totally breast feeding at twelve weeks had a higher incidence of depression than those who were partially breast feeding. Alder and Bancroft [2] found that breast feeders showed slightly more depression at three months post-partum and also scored significantly higher on social dysfunction, anxiety and insomnia scales. They were still scoring higher depressionlevels at six months. Romito [42] only studied 44 women but found the women most likely to be depressedone month after birth were those who failed to breast feed in spite of having wanting to do so. The next most depressedwere those women who were successfully breast feeding. None of the eleven mothers who had planned and succeededin bottle feeding became depressed. An investigation of 90 mothers in Finland showed that mothers who breast fed had more depression, which the authors thought was more prevalent among those who had difficulty in breast feeding [45]. A major multicultural study of post-natal depression followed 293 women in Australia, Italy and the Netherlands [12]. Although there were no significant differences between the countries, multivariate analysis highlighted unsupplemented breast feeding until four months as being significantly related to depression at that time. A study from Iowa [36] showed no effect with breast or bottle feeding. This used a depression inventory and followed women from the second trimester of pregnancy until nine weeks post-partum but found no relationship with breastfeeding. A British study [20] measureddepressionat the first week after delivery and again at six weeks post-delivery. Significant predictors of depressionat this stagewere a low birthweight baby, delivery by Caesareansection, the delivery less difficult than expected and bottle feeding (3 1% of those with depressionwere bottle feeding comparedwith 13% of those who were not depressed).No logistic regression analysis was undertaken to determine whether the association with bottle feeding was an association of having
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had a Caesareansection or a baby being ill. The only study using logistic regression [5] is from Australia. A study of 790 women eight to nine months after birth showed that 80% of those who were currently depressedhad breast fed compared with 89% of the rest of the population. Logistic regression taking account of a variety of confounders including maternal age and parity found the adjusted odds associated with bottle feeding as 1.86 [95% C.I. 1.01, 3.451 (P < 0.05). It should be noted that the positive relationships with breast feeding are with concurrent breast feeding. There are a number of factors that may explain this relationship. The breast feeding mother is the one who will wake at night to breast feed, with the consequencethat she is almost bound to be more fatigued than the bottle feeding mother who has a supportive partner or other members of the family who can take on the role of giving a bottle during the night. An additional problem is that breast feeding mothers cannot predict the time and length of feeding and therefore are less likely to be able to plan their day efficiently. A number of studies have found that mothers who bottle feed are significantly more likely than breast feeders to go out whether alone or with their partners and breast-feeding mothers resume sexual activity later and have less intercourse than bottle-feeding mothers [1,41]. Romito [42] comments that ‘these results suggest that breast feeding can contribute to that estrangementbetween spousesafter the birth of a child which is so often described in studies of parenthood transition’. However, she goes on to point out that there are also advantagesto breast feeding. Breast feeding mothers express pride, satisfaction and great pleasurein breast feeding. The pleasurable side of breast feeding is linked with the physical closenessof the baby and the mother’s awareness of being able to satisfy the child’s needs wholly. The negative side is closely linked with the social organisation of motherhood. Another major hypothesis to explain the positive relationship between post-natal depressionand breast feeding (particularly prolonged unsupplementedbreast feeding) is hormonal. Such women are likely to have higher levels of prolactin and with suppression of ovarian function [ 121, low levels of oestrogen and progestogen, and therefore may be more prone to depression mirroring that found with premenstrual tension. If indeed there is a relationship between depression and breast feeding, it is important to determine whether this has any effect on the way in which the mother views her infant. Among 710 mothers in Cambridge [18] breast feeding was associated with negative descriptions of the baby especially among multiparous mothers. The mothers who did not breast feed included 64% whose description of the baby was very positive comparedwith 45% of those who were still breast feeding and 46% of those who had breast fed but stopped (P < 0.01). 4. Long-term
consequences
In view of the physical effects of lactation on the mothers’ nutritional status, one might hypothesize that prolonged lactation among deprived mothers in the developing world may well have long-term effects with increased risk of osteoporosis and
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reduced survival. The only study we could find that addressed the question of osteoporosis [4] was in an affluent community and no major studies appear to have assessedmaternal survival in relation to lactation history. Conversely in the affluent communities, where prolonged lactation results in a reduction in adiposity (not to mention the excretion of potentially harmful pollutants such as the polychlorinated biphenyls [27]), one might predict a reduced incidence of any diseases linked to a diet high in fat. Some evidence exists to support this hypothesis in regard to breast cancer in young women. For example, McTiernan and Thomas [29] carried out a study of 329 women diagnosed with breast cancer in 1982-83 aged between 25 and 54 and compared them with a set of 332 control women in the same age band identified by random-digit dialling. They divided mothers and controls according to whether or not they had reached the menopause. They found, after allowing for age, parity and age at first full-term pregnancy, a significant relationship between a history of ever breast feeding and breast cancer for those who were diagnosed pre-menopause(relative risk (RR) 0.49, 95% confidence interval (CI) 0.30-0.82) but not for those diagnosedpost-menopause(RR = 1.0; 95% CI 0.58, 1.70). Similar effects have been shown by four studies that have divided by age at diagnosis in this way, and allowed for potential confounders [9,25,35,46]. The largest study [25] cannot be dismissed easily. It compared 4599 women diagnosed with breast cancer at ages 20-55 with 4536 controls obtained by random dialling. Casesand controls came from eight different areas in the US. Allowance for age at first full-term pregnancy, parity, age at diagnosis, menopausalstatus, Quetelet index and familial history of breast cancer resulted in a significant relationship with duration of breast feeding, but no interaction with menopausal state. The adjusted odds ratios (with 95% confidence intervals) were: Duration of lactation in parous women Not at all < 6 months 6- 12 months 13-24 months 25 months +
1,OOreference 0.92 (0.82, 1.02) 0.85 (0.73, 0.98) 0.75 (0.62, 0.90) 0.67 (0.52, 0.85)
Trend test: x2 = 22.6, df= 1, P < 0.0001 It is difficult to find any convincing biases in this study or the other large studies [25,35,46]. Nevertheless, it, and all the other case-control studies do rely on retrospective recall, with potential biases between cancer cases and controls. Mach more reliable, therefore should be the prospective study [31], the US Nurses’ H&&h Study, which followed 89 887 women for six years during which time 1459 women developed breast cancer. Those who had breast fed were only slightly less likely to develop cancer [or 0.93, 95% C.I. 0.83, 1.031 and if attention is confined to premenopausalcasesthe risk is actually slightly higher if there was a history of breast feeding [OR 1.14, 95% C.I. 0.87, 1.501.The problem with the study must be the age from which the follow-up took place, for many women would already have been well
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past the menopause.Thus it is not possible to dismiss the findings from the case control studies. However, interpretation of the data may be prone to error; by using the term ‘a protective effect of duration of breast feeding’ the implication is that mothers could alter their risk by lactating for longer. This may be far from the case; reasonsfor non-breastfeeding (or for short duration of feeding) in these mothers may be the explanation (e.g. failure because of breast abscess,inverted nipple or other mechanical problem); alternatively mothers who don’t breast feed may have an underlying hormonal profile that results in a distaste for breast feeding or an inability to do so (some evidence for this derives from one study of premenopausalbreast cancer, where an excess of mothers reported early cessation of lactation becauseof insufficient milk [9]). If, however, the relationship is more direct possible explanations are that increasedprolactin and/or decreasedoestrogen during lactation inhibit tumour development in someway. The possibly more likely explanation is that breast feeding has removed carcinogens from the breast tissue. Evidence for this derives from serum samplesof women enrolled in the New York University Women’s Health Study; the serum of the 58 women who were diagnosedwith breast cancer within six months had significantly higher levels of DDE, a metabolite of the pesticide DDT, than the serum of 171 matched controls [50]. The only other diagnosis reported to be negatively associatedwith breast feeding is ovarian cancer. This problem has several of the same risk factors as breast cancer (e.g. negative relationship with parity), and two studies have shown negative associationswith breast feeding [21,44], but the studies were relatively small and the findings far from convincing.
5. Discussion
That more researchhas not been carried out into the health of mothers who breast feed is in line with the fact that mothers have largely been ignored by most epidemiological studies of health. Indeed maternal mortality, i.e. mortality related to childbirth has only just become a focus of attention, although extremely common in many developing countries. There is some suggestion from the data presented here that mothers who breast feed may have emotional problems during the first months after delivery and appear to have a less positive relationship with their child, contrary to all predictions. Whether this is just a phenomenonof western culture, or whether it is also true in the developing world needs some basic research. While there is a consistent and enthusiastic focus on the positive effects of breast feeding on the child, it is important to become aware that successfulbreast feeding is more likely to be achieved if the pregnant mother can see that her friends who are breast feeding are thriving both physically and psychologically. From available data, this is unlikely to always be true. It may then be important to investigate the immediate negative effects of breast feeding on the mother so that appropriate advice and interventions may be initiated. This should be far more important to the mother than a promise of a slight reduction in risk of early breast cancer if she breast feeds.
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It appearsthat successfullactation may occur on energy intakes considerably lower than the current estimated energy requirements. It is uncertain how far the energy demands are met by behavioural and metabolic adaptation of the lactating mother. Where the shortageof food and/or reservesexceedsthe capacity to adapt, prolonged lactation is likely to lead to maternal depletion. That maternal health and well-being is far more crucial to the infant in the developing world is obvious and yet little attention is paid to the mother’s needs as opposedto those of the child. If policy is to encouragethe mother to breast feed at all costs, then perhaps the marketing of appropriate maternal supplements should be promoted as enthusiastically as breast milk substitutes are discouraged. References [l] Alder E, Bancroft J. Sexual behaviour of lactating women: a preliminary communication. J Reprod Infant Psycho11983;1:47-52. [2] Aider E, Bancroft J. The relationship between breast feeding persistence, sexuality and mood in postpartum women. PsychoI Med 1988;18:386-96. 131Alder E, Cox J. Breast feeding and post-nataI depression.J PsychosomaticRes 1983;27:139-44. [4] Alderman SW, Weiss NS, Daling JR, Ure CL, Ballard JH. Reproductive history and postmenopausal risk of hip and forearm fracture. Am J Epidemiol 1986;124:262-7. [5] Astbury J, Brown S, Lumley J, Small R. Birth events, birth experiences and social differences in postnatal depression.Am J Public Health 1994;18:176-84. [6] Atkinson PJ, West RR. Loss of skeletal calcium in lactating women, J Obstet Gynaecol Br Commonwealth 1970;77:555-60. [7] Brewer MM, Bates MR,Vannoy LP Postpartumchangesin maternal weight and body fat depots in lactating vs non-lactating women. Am J Clin Nutr 1989:49:259-65. [8] Butte NF, Garza C, Stuff JE, O’Brian Smith E, Nichols BL. Effect of maternal diet and body composition on lactational performance. Am J Clin Nutr 1984;39:296-306. [9] Byers T, Graham S, Rzepka T, Marshall J. Lactation and breast cancer: evidence for a negative association in premenopausalwomen. Am J Epidemiol 1985;121:664-74. [IO] Chan GM, McMurry M, Westover K, Engelbert-FentonK, Thomas MR. Effects of increaseddietary calcium intake upon the calcium and bone mineral status of lactating adolescentand adult women. Am J Clin Nutr 1987;46:319-23. [I l] Dalton K. Prospective study into puerperal depression.Br J Psychiatry 1971;118:689-92. [I 21 Dennerstein L, Lehert I-‘, Riphagen F. Postpartum depression-risk factors. J Psychosom Gbstet Gynaecol 1989;lO Suppl:S53-S67. [I 31 Department of Health. Dietary Reference Values for Food Energy and Nutrients for the United Kingdom: London, 1991HMSO. [ 141 Dewey KG, Heinig JM, NommsenLA. Maternal weight-loss patternsduring prolonged lactation. Am J Clin Nutr 1993;58:162-6. 1151Drinkwater BL, ChestnutCH. Bone density changesduring pregnancy and lactation in active women: a longitudinal study. Bone Miner 1991;14:153-60. [16] Dugdale AE, Eaton-Evans J. The effect of lactation and other factors on postpartum changes in body-weight and triceps skinfold thickness. Br J Nutr 1989;61:149-53. [17] Frisancho AR. New norms of upper limb fat and muscle areas for assessmentof nutritional status. Am J Clin Nutr 1981;34:2540-5. [ 181 Green JM, Richards MPM, Kitzinger JV, Coupland VA. Mothers’ perceptions of their 6 week old babies: relationship with antenatal, intrapartum and postnatal factors. Ir J Psycho11991;12:133-44. [19] Guillermo-Tuazon MA, Barba CVC, van Raaij JMA, Hautvast JGAJ. Energy intake, energy expenditure, and body composition of poor rural Phillipine women throughout the first 6 months of lactation. Am J Clin Nutr 1992:56:874-80.
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[20] Hannah P, Adams D, Lee A et al. Links between early post-partum mood and post-natal depression. Br J Psychiatry 1992;160:777-80. [21] Hartge P, Schiffman MH, Hoover E, McGowan L, Lesher L, Norris HJ. A case-control study of epithelial ovarian cancer. Am J Obstet Gynecol 1989;161:10-6. [22] Illingworth PJ, Jung RT, Howie PW, Leslie P, Isles TE. Diminution in energy expenditure during lactation. Br Med J 1986;292:437-42. [23] Kent GN, Price RI, Gutteridge DH, Smith M, Allen JR, Bhagat CI, Barnes MP, Hickling CJ, Retallack RW, Wilson SG, Devlin RD, Davies C, St John A. Human lactation: Forearm trabecular bone loss, increasedbone turnover, and renal conservation of calcium and inorganic phosphatewith recovery of bone mass following weaning. J Bone Miner Res 1990;4:361-9. [24] Krasovec K. The implications of poor maternal nutritional status during pregnancy for future lactational performance. J Trop Ped 1991;37 SupplS3-SlO. [25] Layde PM, Webster LA, Baughman AL, Wingo PA, Rubin GL, Ory HW. Cancer Steroid Hormone Study Group: The independentassociationsof parity, age at first full term pregnancy and duration of breast feeding with the risk of breast cancer. J Clin Epidemiol 1989;42:963-73. [26] Lucas A, Ewing G, Roberts SB, Coward WA. How much energy does the breast fed infant consume and expend?. Br Med J 1987;295:75-7. [27] Luck W, Nau H. Nicotine and cotinine concentrationsin serum and milk of nursing smokers. Br J Clin Pharmacol 1984;18:9-15. [28] McNeilly AS. Physiology of lactation. J Biosocial Sci 1977;4 SupplSS-S21. [29] McTueman A, Thomas DB. Evidence for a protective effect of lactation on risk of breast cancer in young women. Am J Epidemiol 1986;124:353-8. [30] Merchant KM, Martorell R, Haas JD. Nutritional adjustmentsin response to reproductive stresses within Guatemalan women. J Trop Pediatrics 1991;37 Suppl:Sll-4. [31] Michels KB, Willett WC, Rosner BA, Manson JE, Hunter DJ, Colditz GA, Hankinson SE et al. Prospective assessmentof breastfeeding and breast cancer incidence among 89 887 women. Lancet 1996;347:431-6. [32] Moser PB, Reynolds RD, Acharya S, Howard MP, Andon MB. Calcium and magnesium dietary intakes and plasma and milk concentrations of Nepalese lactating women. Am J Clin Nutr 1988;47:735-9. [33] Motil KJ, Montandon CM, Thotathuchery M, Garza C. Dietary protein and nitrogen balance in lactating and non-lactating women. Am J Clin Nutr 1990,51:378-84. [34] National Centre for Health Statistics.Weight by height and age for adults 18-74 years: United states 1971-74.: Hyattsville, MD, US Department of Health, Education and Welfare, 1979. [35] Newcomb PA, StoreerBE, Longnecker MP, Mittendorf MP, GreenbergER, Clapp RW et al. Lactation and a reduced risk of premenopausalbreast cancer. New Engl J Med 1994;330:81-7. [36] O’Hara MW, Schelecte JA, Lewis DA, Wright EJ. Prospective study of postpartum blues. Biologic and psychosocial factors. Arch Gen Psychiatry 1991;48:801-6. [37] Prentice AM, Lunn PG. WatkinsonM, WhiteheadRG. Dietary Supplementationof Lactating Gambian Women. II. Effect on Maternal Health, Nutritional Status and Biochemistry. Human Nutr: Clin Nutr 1983;37C:65-74. [38] Quandt SA. Changes in Maternal PostpamUn Adiposity and Infant Feeding Patterns. Am J Phys Anthropol 1983;60:455-61. [39] Reynolds RD, Moser PB, Acharya S, McConnell W, Andon MB, Howard MP. Nutritional and medical status of lactating women and their infants in the Kathmandu valley of Nepal. Am J Clin Nutr 1988;47:722-8. [40] Rogers IS. Lactation and fertility. Early Hum Dev 1997;49 Suppl:S185-S190. [41] Romito, P. La naissancedu premier enfant. Etude psychosocialede l’experience de la matemite et de la depressionpost-partum. Lausamie, Delachaux et Nestle, 1990. [42] Romito P. Postpartum depression and the experience of motherhood. Acta Obstet Gynecol Scandinavica 1990;154 Suppl:Sl-S37. [43] Sadurskis A, Kabir N, Wager J, Forsum E. Energy metabolism, body composition and milk production in healthy Swedish women during lactation. Am J Clin Nutr 1988;48:44-9. [44] Schneider AP. Risk factors for ovarian cancer. New Engl J Med 1987;317:508-9.
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1451 Tamminen T. The impact of mother’s depression on her breastfeeding attitudes and experiences. J Psychosom Obstet Gynaecol 1989;lO Suppl:S69-S78. [46] United Kingdom National Case-Control Study. Breast feeding and risk of breast cancer in young women. Br Med J, 1993:307:17-20. 1471 van Raaij JMA, Schonk CM, Vermaat-Miedema SH, Peek MEM, Hautvast JGAJ. Energy cost or lactation, and energy balance of well-nourished Dutch lactating women: reappraisal of the extra energy requirements of lactation. Am J Clin Nutr 1991;53:612-9. 1481 Vis HL, Hemmrt PH. Decline in breastfeeding: about some of its cause. Acta Paediatrica Belgium 1978;31:195-206. [49] Wardlaw GM, Pike AM. The effect of lactation on peak adult shaft and ultra-distal forearm bone mass in women. Am J Clin Nutr 1986;44:283-6. [50] Wolff MS, Toni010 PG, Lee RW, Rivera M, Dubin N. Blood levels of organochlorine residues and risk of breast cancer. J Nat Cancer Inst 1993;85:648-52.
qf I3ristol.
-Abstract Undernourished mothers are likely to have limited fat reserves to draw on during lactation. In order to supply nutrition to her child the mother may therefore become more malnourished and suffer from bone resorption. Repeated or overlapping pregnancies with lactation are likely to compound the issue. Little research has been carried out into the health of mothers while breast feeding, or subsequently. There are theoretical reasons to think that the malnourished mother in the developing world may be particularly vulnerable, but no studies appear to have been undertaken. Investigations in the developed world have concentrated on cancers of the reproductive organs and shown consistent evidence in large case-control studies for a reduced risk of pre-menopausal breast cancer in mothers with a history of prolonged breast feeding. In contrast there have been a number of studies in the developed world concerned with emotional well-being with some indications that mothers who breast feed are more likely to be depressed and are less likely to be positive about their baby. 0 1997 Elsevier Science Ireland Ltd.
1. Introduction
Most breast feeding mothers are aware that whilst breast feeding they are in a different psychological and physical state than when not breast feeding. Whether this has any effect on their current and future health and well-being has received little discussion. In this paper we examine the evidence for relationships between lactation and the nutritional status, health and well-being of the mother in both the short and long term, distinguishing where we can between effects on malnourished and well-nourished mothers.
*Corresponding author. 037%3782/97/$17.00 0 1997 Elsevier Science Ireland Ltd. All rights reserved PII
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2. Nutritional
needs of lactating mothers
In the exclusively breast-fed infant the mother must supply all the nutrients needed for growth and maintenance by that infant. The resulting nutritional demands on the mother are considerable, far outstripping those of pregnancy. The Committee on Medical Aspects of Food Policy has estimated the average energy cost to the mother of lactation in the third month post-partum to be 690 kcal per day, and the estimated requirements of most other nutrients have an incremental value added for lactation [13]. It was assumed by the committee that about 120 kcal per day of the energy cost of lactation would be met by mobilization of a maternal ‘energy reserve’ consisting of 2-2.4 kg of adipose tissue deposited during pregnancy. Women in many developing countries will not gain nearly this amount of adipose tissue during pregnancy. For example, a longitudinal study of 2500 women in Matlab, Bangladesh [24] found that not only did they commence pregnancy with a poor nutritional status (mean pre-pregnant arm circumference was only 22.1 cm as compared to 26 cm in US women) but weight gains during pregnancy were extremely small (4.8 kg on average as compared to 12.5 kg for British women). Judging by arm circumference, mothers in Matlab had lower stores at the end of pregnancy and at three months post-partum than prior to pregnancy. Lacking the fat and muscle reserves to help them cope with the nutritional demands of lactation these women would need a higher energy intake or a more reduced energy expenditure than better-nourished women to prevent their stores becoming further depleted. However, it is very likely that their energy intake during lactation also fell short of the recommended values. 2.1. Effects of lactation on maternal nutritional
status and bone mass
Much of the available evidence suggests that in the malnourished mother the quality and quantity of the breastmilk will be maintained at the expense of maternal health. For example, in a study by Prentice et al. a high-energy dietary supplement was given to lactating Gambian women [37]. Consumption of the supplement did not cause any change in the energy content of the breastmilk produced. However, it appeared to result in an improvement in the health of the supplemented women. There was an average weight gain of 1.8 kg over the course of a year of supplementation, markedly improved riboflavin status and a decrease in the incidence of gastrointestinal problems and upper respiratory tract infections. Plasma levels of prolactin, insulin and T, were all lower in supplemented than unsupplemented women, as was cortisol in the early post-par-turn period. The authors suggested that the higher hormone concentrations in unsupplemented women were ‘part of a concerted endocrine response to maintain milk output in spite of considerable metabolic stress on the mother’this response could be relaxed on receiving supplementary food. In a study of 26 lactating Nepalese women the calcium concentration of the milk was found to be similar to that of American women despite their having less than half the dietary intake [32]. These Nepalese women had an elevated excretion of hydroxyproline, suggesting that milk calcium concentrations were maintained by an
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increasein bone resorption, creating a risk of bone demineralisation. Anthropometric measurements of these women suggested mild protein-energy-malnutrition (e.g. evaluating by arm circumference [17] 54% were below the 5th percentile for protein reservesas compared to the 1971-4 HANES survey of US women [34]), there was also evidence of multiple infections and some of the women showed signs of B-vitamin deficiency [39]. In contrast their breast-fed infants appearedhealthy, with low-normal weight and length for age and no physical signs of mdnutrition. implying that breast milk production had been maintained at the expense of the mother’s health. Several other studies have suggesteda negative effect of lactation on the bone mass of the mother. Atkinson and West measuredthe mineral loss from the femorai shaft during lactation in ten British women and found an average loss of 2.2% over 100 days [6]. Wardlaw and Pike compared fore-arm bone mass in two groups of women each of whom had breast fed three or four children - a long term lactation group (n = 10, averageduration of lactation = 10.7 months for each child) and a short term lactation group (n = 11, average duration of lactation = 2.8 months per child) [49]. Bone mass was significantly lower in the longer term breast-feeding group, and in this group calcium intakes considerably above the RDA did not protect against bone loss. A study of lactating adolescentsfound that a group who consumed around 900 mg calcium/day lost 10% of their bone mineral content over 16 weeks of lactation. However, in an experimental group consuming at least 1600 mg/day this bone mineral loss was prevented [lo]. A study by Drinkwater and Chestnut [ 151 showed that the effects of lactation on bone mineral density varied from site to site. They measuredthe bone mineral density of six women at seven sites, before pregnancy, within six weeks of parturition and after six months of lactation, and also measured the bone mineral density of 25 non-pregnant controls of similar age, height, weight and activity level during the sameperiod. During pregnancy there was a decreasein bone mineral density at the femoral neck and radial shaft (while this remained constant in the non-pregnant women) and an increase in bone mineral density of the tibia in both the pregnant women and the controls (this was the only significant changein bone density observedin the controls during the study). After six months of lactation the bone density of the radial shaft had returned to pre-pregnancylevels, but the density of the femoral neck had declined further. The long-term effects of lactation on bone mineral density are unclear. A study by Kent et al. of bone turnover during and after lactation suggestedthat the bone mineral content lost during lactation is replaced during the weaning period [23]. This is concordant with the results of a survey of American women in Washington which found the risk of hip and forearm fracture to be unaffected by parity and duration of lactation [4]. Furthermore, a separateanalysis of hip fracture only suggesteda slight protective effect of increased months of breast feeding. 2.2. Overlap of pregnancy and lactation
Pregnancy and lactation both impose a nutritional strain upon the mother. Various social and biological factors operate to decreasethe chancesof these statesoccurring simultaneously. Lactation results in hormonal changeswhich depressfertility [40], in
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addition the steroids of pregnancy inhibit the onset of lactation [28] (although not preventing it if it is already established). In many societies there are taboos against sexual intercourse during the period of lactation. Conversely, pregnancy is often cited as a reason for weaning [48], the belief being either that continuing breastfeedingwill result in damageto the fetus or that pregnancy in some way ‘spoils’ the breast milk. Despite this, pregnancy and lactation frequently do overlap. Such a situation might be expected to impose a particular threat to the nutritional status of the mother. A study in Guatemala set out to investigate the effect of overlapping pregnancy and lactation on maternal nutritional status [30]. The effect of the length of the ‘recuperative period’ between the weaning of one child and the conception of the next was also examined. This recuperative period, being free of the nutritional stressesof pregnancy and lactation might allow the mother to replenish stores depleted by these processes. The Guatemalan study found evidence that lactation concurrent with pregnancy and short recuperative intervals were nutritionally stressful conditions, resulting in increasedfood supplement intake by the mother and reduced maternal fat stores. They recommended that to reduce the risk of depletion in women with marginal energy intakes their pregnancies should be well spaced,such that the next conception occurred more than six months after weaning the previous child. 2.3. Effects of lactation on bodyweight
It has been widely assumedthat the fat stores deposited during pregnancy in both well-nourished women and animals representa reserveto support the energy demands of lactation. Similarly, the decreasein body weight and body fat of many mothers during lactation is presumedto be a result of the energy demandsof lactation. These assumptionshave been challenged by Dugdale et al. [16], who measuredchangesin maternal bodyweight from one month to twelve months post-partum. They found a pattern of weight loss from the first month until the sixth month. However, this weight loss was unrelated to duration of breastfeeding, implying that the negative energy balance causing it could not be ascribedto lactation. Desire to lose weight had a significant effect on the amount of weight loss, suggestingdeliberate maternal food restriction was an important factor. Quandt measuredbody fat changes in lactating women over six months and found an increase in adiposity in the majority of them (29 out of 46) [38]. However this finding was based largely on changes in triceps skinfold. This may increase after pregnancy due to a redistribution (rather than an increase) of fat stores. Brewer et al. comparedthe weight and body fat changesin three groups of women (exclusive breast feeders, combination breast and bottle feeders and bottle feeders) during the first six months after delivery [7]. They also found that the feeding regime made no difference to the total weight loss of the women over the six month period. However, the pattern of weight loss was different with only the breastfeedinggroup experiencing a significant weight loss from the third to the sixth month after delivery, even though the mean (S.D.) energy intake was considerably higher in both groups of lactating women (2055(435), 2005(515) and 1453(503) kcal/day in exclusive breast, supplementedbreast and bottle feeders respectively). A study by Dewey et al. also
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found a particularly marked difference between the weight loss of breastfeedingand formula feeding women from the third to the sixth month post-partum [14]. In their group the breastfeederslost more weight than the formula feeders over the first twelve months (4.4 vs. 2.4 kg). They also lost triceps skinfold thickness from nine to twelve months post-partum, while formula feedersgained it. It may be that the effect of breastfeeding on changes in maternal bodyweight is only apparent when breast feeding is continued for more than six months.
2.4. The energy cost of lactation
The effect of lactation upon post-partum weight loss will depend largely on its energy cost. This remains a matter of debate. Many women in developing countries produce sufficient breast milk to sustain satisfactory growth in their infants for several months despite energy intakes considerably below the recommendedlevels. In some extreme casesof food shortage a degree of maternal depletion may result. However, there are several reasons to believe that successful lactation may occur in women consuming considerably less energy than currently recommendedwithout the risk of maternal depletion. The results of several studies of well-nourished lactating women suggestthat then actual energy requirements are lower than the acceptedestimates.Butte et al. looked at the bodyweight changesand dietary intake in 45 well-nourished lactating American women at the first, second, third and fourth months post-partum [8]. They found a gradual decline in maternal bodyweight over the four months, with an estimated energy contribution of 156 kcal/day from maternal body stores- similar to the 120 kcal assumedin the COMA report. However, me energy intakes were lower than the COMA recommendationsat all stages.Brewer et al. consideredthat at energy intakes of around 2500 kcal/day body fat losses in lactating women would be unlikely to occur. In the exclusively breast feeding women in their study a dietary intake of 2055 kcal/day produced only a 225 kcal loss from body fat stores [7]. Van Raaij et al. also considered the estimated energy requirements of lactation to be too high. They found lactating Dutch women to consume only 289 kcal/day more at nine weeks postpartum than at twelve weeks gestation, or 415 kcal more than at one year post-parturn [47]. These women lost no body fat during the first two months post-partum. In 23 lactating Swedish women the energy intake two months after delivery was only 280 kcal/day greater than before pregnancy, and no body fat was lost during these two months of lactation [43]. The apparent overestimate of the energy cost of lactation could arise for several reasons. It may be that the estimates of the volume of milk produced or its energy value are too high (as the results of studies using doubly labelled water would suggest 1261).An efficiency value of 80% is assumedfor the conversion of maternal dietary energy to gross milk energy. It is possible that the true efficiency is higher than this. However, even assuming an efficiency of 100% would lead to only a small reduction in the estimatedenergy requirements. Another possibility is that the energy needsfor maintenance and physical activity are lower in the lactating woman. Energy
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requirements could be reduced by a reduction in physical activity or an increase in metabolic efficiency. 2.5. Changes in metabolic efJiciency during lactation
The evidence for changesin metabolic efficiency during lactation is contradictory. Illingworth et al. found metabolic efficiency to be greater in lactating women than in bottle-feeding women or non-pregnant, non-lactating controls [22]. The increase in metabolic rate in responseto a meal or an injection of noradrenaline was lower in the lactating women. When the women were remeasuredafter the complete cessation of lactation their metabolic responsesto noradrenaline or a meal had increasedto normal levels. The authors suggestedthat thesemetabolic changeswould result in a reduction of the non-lactational component of energy expenditure in lactating women. Lactating Phillipine women were found to have a lower basal metabolic rate (BMR) at six, twelve and eighteen weeks post-pat-turnthan at thirteen weeks gestation [19]. Von Raaij et al. also found a reduced basal metabolic rate in lactating women at nine weeks post-partum compared to the twelve weeks gestation values (a similar reduction was found in non-lactating women) [47]. The basal metabolic rate was also lower than at twelve months after delivery, suggesting an ‘enhanced efficiency of energy metabolism throughout the first three months’. In addition a study by Motil et al. suggeststhat nitrogen metabolism is altered in lactating women [33]. On intakes of 1 g protein/kg/day the urinary 3-methylhistidine excretion was lower in lactating than non-lactating women (106.5(27.7) and 150.7(55.6) kmol/day respectively). The authors suggested that this represented an adaptive metabolic response to reduced protein intake in the lactating women, promoting the conservation of skeletal muscle protein stores. However, the resting metabolic rate of Swedish women was found to be higher during lactation than before pregnancy [43]. In addition Illingworth et al. found no difference between the resting metabolic rates of the three groups of women studied (although the numbers were relatively small) [22]. 2.6. Changes in physical activity level during lactation
It may be that some lactating women are constrained from reducing their physical activity level (PAL) by occupational demands.However, where a decreasein PAL is possible it would obviously reduce the increase in energy requirements associated with lactation. The literature on PAL changesduring lactation is inconsistent. Some studies have found a reduction. The measuredPAL of well-nourished lactating Dutch women was 1.47 X the basal metabolic rate (BMR) at 5 weeks post-partum and 1.51 X BMR at 27 weeks [47], significantly lower values than the measuredPAL at 56 weeks post-partum (1.54 X BMR). This suggestedthat in this group some of the energy cost of lactation was met by a reduction in physical activity. However, there was no difference in the measured PAL of 23 lactating Swedish women before pregnancy and at 2 months post-partum [43]. Based on 24-h activity records Brewer et al. found no difference between lactating and non-lactating women in the predicted energy needs for maintenance and activity. In Filipino women the measured PAL
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increased from 1.61 X BMR at 6 weeks lactation to 1.80 X BMR at 12 weeks and 1.97 X BMR at thirty weeks [ 191. This represents a very high level of physical activity - the estimated energy expenditure of a British woman with a moderate/ heavy occupation and very active leisure activity being 1.7 X BMR [ 131.The PAL at 13 weeks pregnancy was similar to the value at 12 weeks lactation (1.77 X Bh4R). Thus the PAL of these women did not appear to be reduced beyond the first few weeks of lactation.
3. Psychological
effects during lactation
We could find no studies that specifically startedwith the aim of looking at the way in which the breast feeding mother differed in terms of post-pat-turn blues and post-natal depressionfrom the mother who was bottle feeding. There are, however, a number of studies of post-party blues and post-natal depressionthat have incidentally documented whether the mother was breast feeding or not. Six studies have indicated an increased depression rate among the breast feeders. Dalton [l l] found an increased depression rate in those mothers who were breast feeding at two months. Alder and Cox [3] found that those who were totally breast feeding at twelve weeks had a higher incidence of depression than those who were partially breast feeding. Alder and Bancroft [2] found that breast feeders showed slightly more depression at three months post-partum and also scored significantly higher on social dysfunction, anxiety and insomnia scales. They were still scoring higher depressionlevels at six months. Romito [42] only studied 44 women but found the women most likely to be depressedone month after birth were those who failed to breast feed in spite of having wanting to do so. The next most depressedwere those women who were successfully breast feeding. None of the eleven mothers who had planned and succeededin bottle feeding became depressed. An investigation of 90 mothers in Finland showed that mothers who breast fed had more depression, which the authors thought was more prevalent among those who had difficulty in breast feeding [45]. A major multicultural study of post-natal depression followed 293 women in Australia, Italy and the Netherlands [12]. Although there were no significant differences between the countries, multivariate analysis highlighted unsupplemented breast feeding until four months as being significantly related to depression at that time. A study from Iowa [36] showed no effect with breast or bottle feeding. This used a depression inventory and followed women from the second trimester of pregnancy until nine weeks post-partum but found no relationship with breastfeeding. A British study [20] measureddepressionat the first week after delivery and again at six weeks post-delivery. Significant predictors of depressionat this stagewere a low birthweight baby, delivery by Caesareansection, the delivery less difficult than expected and bottle feeding (3 1% of those with depressionwere bottle feeding comparedwith 13% of those who were not depressed).No logistic regression analysis was undertaken to determine whether the association with bottle feeding was an association of having
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had a Caesareansection or a baby being ill. The only study using logistic regression [5] is from Australia. A study of 790 women eight to nine months after birth showed that 80% of those who were currently depressedhad breast fed compared with 89% of the rest of the population. Logistic regression taking account of a variety of confounders including maternal age and parity found the adjusted odds associated with bottle feeding as 1.86 [95% C.I. 1.01, 3.451 (P < 0.05). It should be noted that the positive relationships with breast feeding are with concurrent breast feeding. There are a number of factors that may explain this relationship. The breast feeding mother is the one who will wake at night to breast feed, with the consequencethat she is almost bound to be more fatigued than the bottle feeding mother who has a supportive partner or other members of the family who can take on the role of giving a bottle during the night. An additional problem is that breast feeding mothers cannot predict the time and length of feeding and therefore are less likely to be able to plan their day efficiently. A number of studies have found that mothers who bottle feed are significantly more likely than breast feeders to go out whether alone or with their partners and breast-feeding mothers resume sexual activity later and have less intercourse than bottle-feeding mothers [1,41]. Romito [42] comments that ‘these results suggest that breast feeding can contribute to that estrangementbetween spousesafter the birth of a child which is so often described in studies of parenthood transition’. However, she goes on to point out that there are also advantagesto breast feeding. Breast feeding mothers express pride, satisfaction and great pleasurein breast feeding. The pleasurable side of breast feeding is linked with the physical closenessof the baby and the mother’s awareness of being able to satisfy the child’s needs wholly. The negative side is closely linked with the social organisation of motherhood. Another major hypothesis to explain the positive relationship between post-natal depressionand breast feeding (particularly prolonged unsupplementedbreast feeding) is hormonal. Such women are likely to have higher levels of prolactin and with suppression of ovarian function [ 121, low levels of oestrogen and progestogen, and therefore may be more prone to depression mirroring that found with premenstrual tension. If indeed there is a relationship between depression and breast feeding, it is important to determine whether this has any effect on the way in which the mother views her infant. Among 710 mothers in Cambridge [18] breast feeding was associated with negative descriptions of the baby especially among multiparous mothers. The mothers who did not breast feed included 64% whose description of the baby was very positive comparedwith 45% of those who were still breast feeding and 46% of those who had breast fed but stopped (P < 0.01). 4. Long-term
consequences
In view of the physical effects of lactation on the mothers’ nutritional status, one might hypothesize that prolonged lactation among deprived mothers in the developing world may well have long-term effects with increased risk of osteoporosis and
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reduced survival. The only study we could find that addressed the question of osteoporosis [4] was in an affluent community and no major studies appear to have assessedmaternal survival in relation to lactation history. Conversely in the affluent communities, where prolonged lactation results in a reduction in adiposity (not to mention the excretion of potentially harmful pollutants such as the polychlorinated biphenyls [27]), one might predict a reduced incidence of any diseases linked to a diet high in fat. Some evidence exists to support this hypothesis in regard to breast cancer in young women. For example, McTiernan and Thomas [29] carried out a study of 329 women diagnosed with breast cancer in 1982-83 aged between 25 and 54 and compared them with a set of 332 control women in the same age band identified by random-digit dialling. They divided mothers and controls according to whether or not they had reached the menopause. They found, after allowing for age, parity and age at first full-term pregnancy, a significant relationship between a history of ever breast feeding and breast cancer for those who were diagnosed pre-menopause(relative risk (RR) 0.49, 95% confidence interval (CI) 0.30-0.82) but not for those diagnosedpost-menopause(RR = 1.0; 95% CI 0.58, 1.70). Similar effects have been shown by four studies that have divided by age at diagnosis in this way, and allowed for potential confounders [9,25,35,46]. The largest study [25] cannot be dismissed easily. It compared 4599 women diagnosed with breast cancer at ages 20-55 with 4536 controls obtained by random dialling. Casesand controls came from eight different areas in the US. Allowance for age at first full-term pregnancy, parity, age at diagnosis, menopausalstatus, Quetelet index and familial history of breast cancer resulted in a significant relationship with duration of breast feeding, but no interaction with menopausal state. The adjusted odds ratios (with 95% confidence intervals) were: Duration of lactation in parous women Not at all < 6 months 6- 12 months 13-24 months 25 months +
1,OOreference 0.92 (0.82, 1.02) 0.85 (0.73, 0.98) 0.75 (0.62, 0.90) 0.67 (0.52, 0.85)
Trend test: x2 = 22.6, df= 1, P < 0.0001 It is difficult to find any convincing biases in this study or the other large studies [25,35,46]. Nevertheless, it, and all the other case-control studies do rely on retrospective recall, with potential biases between cancer cases and controls. Mach more reliable, therefore should be the prospective study [31], the US Nurses’ H&&h Study, which followed 89 887 women for six years during which time 1459 women developed breast cancer. Those who had breast fed were only slightly less likely to develop cancer [or 0.93, 95% C.I. 0.83, 1.031 and if attention is confined to premenopausalcasesthe risk is actually slightly higher if there was a history of breast feeding [OR 1.14, 95% C.I. 0.87, 1.501.The problem with the study must be the age from which the follow-up took place, for many women would already have been well
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past the menopause.Thus it is not possible to dismiss the findings from the case control studies. However, interpretation of the data may be prone to error; by using the term ‘a protective effect of duration of breast feeding’ the implication is that mothers could alter their risk by lactating for longer. This may be far from the case; reasonsfor non-breastfeeding (or for short duration of feeding) in these mothers may be the explanation (e.g. failure because of breast abscess,inverted nipple or other mechanical problem); alternatively mothers who don’t breast feed may have an underlying hormonal profile that results in a distaste for breast feeding or an inability to do so (some evidence for this derives from one study of premenopausalbreast cancer, where an excess of mothers reported early cessation of lactation becauseof insufficient milk [9]). If, however, the relationship is more direct possible explanations are that increasedprolactin and/or decreasedoestrogen during lactation inhibit tumour development in someway. The possibly more likely explanation is that breast feeding has removed carcinogens from the breast tissue. Evidence for this derives from serum samplesof women enrolled in the New York University Women’s Health Study; the serum of the 58 women who were diagnosedwith breast cancer within six months had significantly higher levels of DDE, a metabolite of the pesticide DDT, than the serum of 171 matched controls [50]. The only other diagnosis reported to be negatively associatedwith breast feeding is ovarian cancer. This problem has several of the same risk factors as breast cancer (e.g. negative relationship with parity), and two studies have shown negative associationswith breast feeding [21,44], but the studies were relatively small and the findings far from convincing.
5. Discussion
That more researchhas not been carried out into the health of mothers who breast feed is in line with the fact that mothers have largely been ignored by most epidemiological studies of health. Indeed maternal mortality, i.e. mortality related to childbirth has only just become a focus of attention, although extremely common in many developing countries. There is some suggestion from the data presented here that mothers who breast feed may have emotional problems during the first months after delivery and appear to have a less positive relationship with their child, contrary to all predictions. Whether this is just a phenomenonof western culture, or whether it is also true in the developing world needs some basic research. While there is a consistent and enthusiastic focus on the positive effects of breast feeding on the child, it is important to become aware that successfulbreast feeding is more likely to be achieved if the pregnant mother can see that her friends who are breast feeding are thriving both physically and psychologically. From available data, this is unlikely to always be true. It may then be important to investigate the immediate negative effects of breast feeding on the mother so that appropriate advice and interventions may be initiated. This should be far more important to the mother than a promise of a slight reduction in risk of early breast cancer if she breast feeds.
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It appearsthat successfullactation may occur on energy intakes considerably lower than the current estimated energy requirements. It is uncertain how far the energy demands are met by behavioural and metabolic adaptation of the lactating mother. Where the shortageof food and/or reservesexceedsthe capacity to adapt, prolonged lactation is likely to lead to maternal depletion. That maternal health and well-being is far more crucial to the infant in the developing world is obvious and yet little attention is paid to the mother’s needs as opposedto those of the child. If policy is to encouragethe mother to breast feed at all costs, then perhaps the marketing of appropriate maternal supplements should be promoted as enthusiastically as breast milk substitutes are discouraged. References [l] Alder E, Bancroft J. Sexual behaviour of lactating women: a preliminary communication. J Reprod Infant Psycho11983;1:47-52. [2] Aider E, Bancroft J. The relationship between breast feeding persistence, sexuality and mood in postpartum women. PsychoI Med 1988;18:386-96. 131Alder E, Cox J. Breast feeding and post-nataI depression.J PsychosomaticRes 1983;27:139-44. [4] Alderman SW, Weiss NS, Daling JR, Ure CL, Ballard JH. Reproductive history and postmenopausal risk of hip and forearm fracture. Am J Epidemiol 1986;124:262-7. [5] Astbury J, Brown S, Lumley J, Small R. Birth events, birth experiences and social differences in postnatal depression.Am J Public Health 1994;18:176-84. [6] Atkinson PJ, West RR. Loss of skeletal calcium in lactating women, J Obstet Gynaecol Br Commonwealth 1970;77:555-60. [7] Brewer MM, Bates MR,Vannoy LP Postpartumchangesin maternal weight and body fat depots in lactating vs non-lactating women. Am J Clin Nutr 1989:49:259-65. [8] Butte NF, Garza C, Stuff JE, O’Brian Smith E, Nichols BL. Effect of maternal diet and body composition on lactational performance. Am J Clin Nutr 1984;39:296-306. [9] Byers T, Graham S, Rzepka T, Marshall J. Lactation and breast cancer: evidence for a negative association in premenopausalwomen. Am J Epidemiol 1985;121:664-74. [IO] Chan GM, McMurry M, Westover K, Engelbert-FentonK, Thomas MR. Effects of increaseddietary calcium intake upon the calcium and bone mineral status of lactating adolescentand adult women. Am J Clin Nutr 1987;46:319-23. [I l] Dalton K. Prospective study into puerperal depression.Br J Psychiatry 1971;118:689-92. [I 21 Dennerstein L, Lehert I-‘, Riphagen F. Postpartum depression-risk factors. J Psychosom Gbstet Gynaecol 1989;lO Suppl:S53-S67. [I 31 Department of Health. Dietary Reference Values for Food Energy and Nutrients for the United Kingdom: London, 1991HMSO. [ 141 Dewey KG, Heinig JM, NommsenLA. Maternal weight-loss patternsduring prolonged lactation. Am J Clin Nutr 1993;58:162-6. 1151Drinkwater BL, ChestnutCH. Bone density changesduring pregnancy and lactation in active women: a longitudinal study. Bone Miner 1991;14:153-60. [16] Dugdale AE, Eaton-Evans J. The effect of lactation and other factors on postpartum changes in body-weight and triceps skinfold thickness. Br J Nutr 1989;61:149-53. [17] Frisancho AR. New norms of upper limb fat and muscle areas for assessmentof nutritional status. Am J Clin Nutr 1981;34:2540-5. [ 181 Green JM, Richards MPM, Kitzinger JV, Coupland VA. Mothers’ perceptions of their 6 week old babies: relationship with antenatal, intrapartum and postnatal factors. Ir J Psycho11991;12:133-44. [19] Guillermo-Tuazon MA, Barba CVC, van Raaij JMA, Hautvast JGAJ. Energy intake, energy expenditure, and body composition of poor rural Phillipine women throughout the first 6 months of lactation. Am J Clin Nutr 1992:56:874-80.
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