BREASTFEEDING 2001, ?ART I THE EVIDENCE FOR BREASTFEEDING
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EFFECTS OF BREASTFEEDING ON THE MOTHER Miriam H. Labbok, MD, MPH, IBCLC
Breastfeeding is a unique biological heritage potentially shared by women everywhere. The hormones of breastfeeding aid in the adjustment to mothering, in conservation of energy, and in subsequent nutrient recovery. Because the physiologic processes of breastfeeding are a normal part of the maturation of the female body, it is not surprising that breastfeeding seems to have the .attributes of a preventive health measure for women: Breastfeeding is beneficial for women’s health. The sequelae of breastfeeding, and of having breastfed, are not minor: Breastfeeding, sometimes referred to as the final stage of Zubor, reduces the risk for (1) postpartum blood loss by increasing the rate of uterine contraction, (2) premenopausal breast cancer, and (3) ovarian cancer. In addition to reducing the severity of anemia, breastfeeding may cause other changes that may help to protect mothers against bladder and other infections. Also, epidemiologic studies seem to indicate that, despite the apparent bone loss that occurs in women during lactation, women who breastfeed may be at reduced risk for spinal and hip Basic review prepared while Associate Professor and Director, Breastfeeding and MCH, WHO Collaborating Center on Breastfeeding (IBCC), Department of Obstetrics and Gynecology, Georgetown University Medical Center. Preparation of this review was supported in part under a Cooperative Agreement with United States Agency for Intemational Development (USAID). The views expressed by the author in this article d o not necessarily reflect the views or policies of Georgetown, USAID, Johns Hopkins University, or Tulane University. Earlier versions of this article were printed in the newsletter of the Australian College of Lactation in 1997 and as a review in Clinics in Pm’natology 26491-503, 1999. From the Nutritional and Maternal Health Division, United States Agency for International Development, Washington, DC;Johns Hopkins University School of Public Health; and Tulane University School of Public Health, Baltimore, Maryland ~
PEDIATRIC CLINICS OF NORTH AMERICA VOLUME 48 NLTMBER 1 FEBRUARY 2001
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fracture after menopause. In, addition to the direct health effects, breastfeeding seems to provide a sense of bonding, a sense of wellbeing, and an improved sense of self-esteem for many women. These statements are considered controversial. This article explores several of these issues in a manner designed to aid in the understanding of why controversy surrounds breastfeeding research findings and, perhaps, why emotions or personal experiences may affect scientific interpretation in this field. REASONS FOR CONFLICTING INTERPRETATION OF FINDINGS
Research-design and analysis-based and conviction-based reasons exist for conflicting interpretation of the studies of breastfeeding. Research design-based issues include:
Different definitions of the characteristic under study. Internationally recognized definitions of breastfeeding exist.29Nonetheless, many journals still accept articles without definitions of terms. Some publications, for example, still use the term exclusive breastfeeding to mean that breastfeeding is the only source of milk but allow all other foods to be given. Clearly, this misdefinition views breastfeeding only as a substitute for formula, not as a maternal, or even a child, health issue. Sampling frame. Much of what is known worldwide about breastfeeding trends is drawn from demographic and health surveys, which have a household-based sample size in which all women are interviewed. The result is that the population that should be the target for breastfeeding, that is, postpartum mothers or children of certain months and years of age, are only a small portion of the study population and may be insufficient in size for specific issues. Also, this approach undersamples children in motherless households, yielding any analysis nonrepresentative of the population. Sample size. A sufficient number of individuals with certain characteristics must be included to reach statistical significance. Many studies include samples that are far too small to adequately address the hypothesis. Selection bias in selection of cases. Because breastfeeding has a wide variation of patterns that are influenced by the age of the child, sample selection must take multiple factors into account. Lack of, or inappropriate, controls. In many studies of the sequelae of breastfeeding among women, controls are hospital based, that is, they are women with other illnesses. Because lack of breastfeeding may affect various systems, selection of controls in this way may mask any significance of the hypothesis. Also, it is not ethically possible nor probable that women would agree to
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be assigned to groups of women who breastfeed or do not breastfeed. Therefore, confounding factors and elements of selfselection bias may be present. Research-analysis issues may include: Confounding. When a separate factor interacts with both cases and controls differently, it may confuse findings. An example of this would be the retrospective study of having been breastfed and having had dental braces. Since maternal socioeconomic status can be related to both of these, it is important to control for this to avoid hiding important results.3o Analytic techniques used. Proper selection of statistical approach is vital. Many textbooks are designed for clinicians and researchers for this purpose. Planned analyses may be limited by data results. The analysis plan should be designed before data gathering because it may dictate, to some extent, the sample frame and size; however, investigators should reassess the plan after the data are collected. The data set may have insufficient numbers in proposed subgroups because of limited variability within the sample or may not reflect other assumptions used in planning. For example, if all women in the sample breastfeed for approximately the same duration, the variability in the data set will be insufficient to assess the biological effects of varying durations of breastfeeding. Selective presentation of findings caused by journal space limitations. Because journals commonly limit article length, important facts in the interpretation of the findings may be inadvertently omitted. Also, articles with negative results rarely are accepted for publication. Misinterpretation or confused conclusions. In statistics, terms such as association and determinant may be misinterpreted as meaning musation. Two things may be statistically significantly associated but have no meaningful relationship. A classic example is one study that showed that the suicide rate in New York City was statistically associated with the rate of ice cream consumption in Tokyo. Another common problem is when findings are not significant but are consistent. If 20 studies show the same trend, although none of them achieve statistical significance individually, this trend becomes a significant finding through its statistically significant recurrence. Conviction-based issues include: Selected presentation of findings based on preferred outcomes. Although scientists should be objective, each works from a personal understanding of the issue in question that may affect how the hypothesis is stated and tested and which data are presented.
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Decision not to publish findings that disprove an investigator’s beliefs and hypotheses. If findings do not support an investigator’s hypothesis or do not achieve statistical significance, it is often difficult to find the energy-or the journal willing-to publish it. Discussion and conclusion sections of papers that include statements that overstate or reinterpret what the findings show. Many of these issues are referred to in the following assessments. BREASTCANCER
Studies of the association of breast cancer with breastfeeding have fostered dialogue in the literature. In the 1920s, investigators found that breasts that never were used to breastfeed were more likely to become cancerous, but findings in the 1970s (when breastfeeding was at its lowest rate in the United States) associated age at first birth as the more important risk factor. The possibility of the association of breastfeeding and decreased breast-cancer risk resurfaced in the 1980s, and multiple controlled studies in the literature have been published in the past 10 years. Perhaps the primary issue that has complicated study of this issue is the apparent causal differences between premenopausal and postmenopausal breast cancers. The preponderance of the studies in the literature, including one large, population-based study,37concludes that no association exists between breastfeeding patterns and postmenopausal breast-cancer incidence; however, two other large, populationbased studiesl2,49 found a significant protective effect, continuing the controversy. Eleven* of 20 studies reviewed, however, showed a significant protective effect of breastfeeding against premenopausal breast cancer. The level of relative risk (RR) reported varied from approximately 0.54 to 0.85 for the first 3 to 6 months of breastfeeding, from 0.39 to 0.71 at 12 months of breastfeeding, 0.4 to 0.72 for more than 2 years, and 0.35 for more than 6 years. A protective effect is shown in these studies, and the effect generally increases with total months of lifetime breastfeeding. In these studies, in general, significant reductions in premenopausal breast cancer are associated with increasing durations of lifetime breastfeeding. Of the other nine studies and reviews that reported no significance in the association between breastfeeding and breast cancer, three issues are noted: (1) short durations of breastfeeding among several of the study populations, with little variability to allow for adequate biological effect to occur, (2) several were not sufficiently large to distinguish premenopausal from postmenopausal cases, and (3) the nearly consistent direction of the findings.t These nine studies include one review and two others that were different analyses of the same large data set.37,45 In *References 5, 11, 33, 41, 43, 50, 56, 60, and 76-78. tReferences 1, 4, 20, 37, 45, 62, 65, 69, 70, and 75.
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most of the studies, although the RRs or odds ratios presented are, for the most part, less than 1.0 and tend to show a trend of increasing protection with duration of total breastfeeding, the 95% confidence intervals (CI) on those ratios include 1.0. Each investigator, hence, concludes from this result that this individual finding lacks significance. If the entire set of studies is examined, however, even in a simple observational meta-analysis, statistical strength exists in the fact that so many of the findings were in the direction of protectiveness. Although not achieving significance, the trend of the association across nearly all published studies is consistent with the several studies in which the findings achieved statistical significance. Figure 1 illustrates this trend for the 12 data sets (13 studies) with RR or odds ratios as the manner of presentation of findings. Of all studies reviewed, only one study includes some analyses that reflect a nonsignificant increase in risk. The biological arguments for the association include exposure to 58 cellular and lack of maturation of the endcontaminant~,4~> organ. One study13raises the issue concerning whether the mother was breastfed as a possible factor in decreased risk for breast cancer, allowing speculation as to additional developmental biological arguments. Two subsequent studies and a meta-analysis found a protective effect against adult cancer of having been breastfed, but none achieved statistical significance.%,71, 74 A new, interesting finding is the inverse association of breastfeeding with certain breast-cancer biomarkers (e.g., HER-2 /new oncogene amplifi~ationl~); however, these findings, although provocative, have not been consistent. The issue of breastfeeding as a variable associated with decreased
Figure 1. Premenopausal breast cancer among women who breastfed. Thirteen studies that include odds ratio or relative risk data. ’Authors who conclude no protective effect of breastfeeding on premenopausal breast cancer incidence. “Authors who conclude no protective effect of breastfeeding on premenopausal breast cancer incidence using same data set. London figure for less than 7 months breastfeeding, Michels figure for “ever breastfeeding.”
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prevalence of premenopausal breast cancer no longer is controversial; rather, a clear and consistent protective effect is reflected in nearly all of the analyses of extant data sets.
OVARIAN CANCER Breastfeeding has long been considered a potential cancer-preventive behavior and, in the 1970s, Casagrande et a16 hypothesized the ”incessant ovulation” theory as a cause of ovarian cancer, linking the ”excess” ovulation and concomitant epithelial irritation caused by fewer pregnancies and lack of breastfeeding to the observed increase in ovarian cancer. In 1983, Risch et a157found a protective effect of lactation (RR, 0.79 per year of lactation) in a retrospective study of newly diagnosed patients with epithelial ovarian cancer, with a sample of women living in the same counties in Washington and Utah serving as contr01s.5~ The conclusion of that study, however, was that the magnitude of the decrease in risk is more than could be accounted for by the short-term inhibition of ovulation alone. In a study of 436 identified cases of women with ovarian cancer and 3833 geographically matched controls, Gwinn et all6 found a similar RR of 0.6 (95% CI, 0.5-0.8) for women who ever breastfed. In 1993, Rosenblatt and Thornas6Icompleted a multinational study of 393 cases of ovarian cancer and 2565 age-, hospital-, and year-ofinterview-matched controls. The researchers found a 20% to 25% decrease in risk for cancer among women who breastfed for at least 2 months, with little increased protection with increased durations. A review by Shoham@(1994) showed that although four studies did not find an association of breastfeeding and ovarian cancer, another found a 50% decrease in risk for ovarian cancer, and six additional studies found a significant protective effect of the early postpartum months of breastfeeding. The conclusion that might be drawn from this series of studies is that the initiation and physiologic completion of breastfeeding during the first 2 to 7 months postpartum is associated with a significant decrease in ovarian-cancer risk, with studies reporting protective levels that average 20%. Also, one study66 found no association of duration of more intensive, full lactation with ovarian-cancer risk. Although the findings clearly support the protective effect of breastfeeding against the occurrence of ovarian cancer (Fig. 2), the dose-response phenomenon is inconsistently supported by the data. Therefore, biological hypotheses alternative to that of Casagrande are warranted. OSTEOPOROSIS
Apparent conflict exists between the clinical studies that show bone loss during lactation and the later mixed findings among retrospective
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Figure 2. Breastfeeding and risk for ovarian cancer.
epidemiologic studies that assess bone status at men~pause.~, 25, 26, 35, 44, 72 Detractors often expand on these apparent conflicts without considering the biological basis and the interactions that may reveal a consensus. The better approach is to review all literature on a subject and to understand what mechanisms codd allow all the findings to be accurate and sound. In the case of osteoporosis, difficulties include the prospective study of women over long periods of time, especially when expensive testing is involved; short, or lack of variability in, durations of breastfeeding in the population; and age of women in study. Some studies find the positive effects of significantly longer periods of breastfeeding and less bone fracture, and a biologically plausible mechanism for this effect exists: the hormonal control of calcium and bone regulation in several systems in the body result in a short-term, somewhat negative effect, but a long-term, positive effect. Studies that have followed up women longer postpartum reveal rapid recovery during the period of sustained weaning.%These complex interactions are common in the field of reproductive health but are often difficult to study because of expense, length of time necessary, and lack of appropriate animal models. Carefully controlled studies in populations with variable breastfeeding patterns, controlling for socioeconomic statistics and other factors, might yield increased clarity on this issue. MATERNAL HUMAN IMMUNODEFICIENCY VIRUS AND BREASTFEEDING
Many health agencies, including the Centers for Disease Control and Prevention (CDC), now suggest that infected mothers should not breastfeed their infants to avoid the chance of mother-to-child viral transmission (MTCT) by this route. Where testing is available, replacement feeding is of high quality, and where good health care is accessible,
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the balance for the survival of the infant favors the use of replacement feeding. Although this may seem logical on first consideration, little is known about viral passage under various breastfeeding patterns. The data on the RRs of mortality for infants of HIV-positive women in various settings show wide variability, and even less is known about the effects of breastfeeding on the course of the disease in mothers. Breastfeeding supports the immune system, but little information in the literature sheds light on those issues among HIV-positive women. Arguments in favor of breastfeeding infants of HIV-positive mothers exist. One study from South Africa9 confirms the early postulation that exclusive breastfeeding seems to decrease the risk for transmission of the virus. Also, some studies seem to show that HIV-positive infants survive longer if breastfed; however, what are these conditions in the subpopulations with high levels of HIV infection? And what is the effect of this decision on maternal survival? One study of the effect of breastfeeding versus formula feeding on MTCT of HIV type 1in Kenya49 concluded that the prevalence of MTCT at 24 months was 36.7%among breastfed children and 20.5% among formula-fed infants; however, the study also reports that the mortality rate at 24 months was not significantly different, at 24.4% (95% CI, 18.2, 30.7) and 20.0% (95% CI, 14.4, 25.6), respectively. Much must be learned about the relative effects of this disease on the breastfeeding dyad. Clearly, a comprehensive approach to HIV prevention would better serve the interests mothers and infants than a lone concentration on reducing MTCT through decreased brea~tfeeding.~ BREASTFEEDING AND FERTILITY
Breastfeeding is associated with increased child spacing. Medical literature from Aristotle, the Renaissance, and occasionally thereafter noted that women who suckle are less likely to become pregnant. The phenomenon was forgotten or disbelieved in recent decades as infant feeding substitutes replaced breastfeeding behaviors. Scientific evidence compiled by the social sciences, demonstrating the population level effect of breastfeeding on fertility, and the medical sciences, which now have identified the biological basis of lactational infertility, has reinitiated interest in this area. One symposium'O has summarized the understanding of the physiologic basis of lactational infertility based on exploration of published and unpublished literature. Three stages were identified: (1) early postpartum, (2) continued lactational amenorrhea, and (3) early menses return. The early postpartum period, in this context, is the 6 to 8 weeks postpartum, during which the inhibitory mechanisms of pregnancy continue, with diminished pituitary response to the hypothalamic release of gonadotropin-releasing hormone (GnRH), which may be caused by decreased activity of the GnRH pulse generator; however, in the first
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month post partum, no luteinizing-hormone response to a GnRH bolus occurs. Luteinizing-hormone activity during this same period shows individual and behavior-based variation. By the second post partum month, luteinizing-hormone response to a GnRH bolus occurs, indicating a shift in the underlying mechanisms.79 The relative duration of continuing lactational amenorrhea also is not fully understood.42In addition to a diminished pituitary responsiveness and GnRH suppression, other possible mechanisms include enhanced or paradoxic negative feedback of ovarian secretions on the hypothalamic-pituitary axis, failure of positive feedback actions, lack of stimulation of the hypothalamus, decreased number or function of GnRH receptors, altered biological activity of the hormones of ovulation, and a variable role of prolactin. Redundance in these mechanisms may exist. Fertility is not immediately recovered with the return of regular vaginal bleeds. The first cycles frequently are associated with abnormal ovulatory activity and luteal-phase defects. One study15found, on average, a gradual return to normalcy over the first three cycles. The suckling stimulus is key in each of the three stages discussed earlier. In the early postpartum stage, suckling 10 to 12 times per day seems the minimum number necessary to establish full lactation and fertility suppression. During the second stage, frequency may be reduced, but increasing intervals between feeds and initiation or increase in supplementation are associated with hastened return of ovulation and menses.15,52 After menses, or regular bleeds, is restored, frequent suckling continues to be associated with decreased fertility. One analysis51 of survey data found that, in areas where breastfeeding is practiced physiologically, the continuation of breastfeeding after menses return is associated with a significant delay in fertility. In this study, for each additional month of breastfeeding after menses return, the likelihood of conception is decreased 7.4%. In 1988, the research findings of several centers worldwide was shared at a meeting at the Rockefeller Bellagio Conference Center, and the scientists agreed that three criteria (i.e., full breastfeeding, amenorrhea, first 6 months postpartum) would be sufficient to serve as a method. These findings became known as the Bellagio Consensus.22A few months later, this approach was presented to a group of family-planning service providers at a meeting at Georgetown University (Washington, DC),the lactational amenorrhea method (LAM) was developed as a clinical algorithm, and guidelines were prepared.31 LAM is a postpartum introductory method that includes three criteria for defining the period of lowest pregnancy risk and then advises immediate commencement of another method that complements the effects of breastfeeding thereafter. Clinically, the mother is asked whether menses has resumed, whether she is no longer fully or nearly fully breastfeeding, and whether her infant is 6 months of age or older. If the answer to any of these questions is yes, she is advised to begin another method of family planning, preferably one that will have no negative
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effects on lactation.31*73 This new method of family planning is highly effective (Table l),is now in use in more than 30 countries, and has been included in Family Planning and Maternal and Child Health policy in several countries. LAM use across these studies averaged approximately to 4 to 5 months. Duration of LAM in common use depends on ambient breastfeeding normal values, maternal commitment, and physiologic predisp~sition.'~, 27 Because LAM is behavior based, no organization in the United States mandates the review of its safety. For this reason, among others, the World Health Organization; Family Health International; and the Institute for Reproductive Health, Department of Obstetrics and Gynecology, Georgetown University assembled a second internationally recognized panel approved by the Rockefeller Foundation to meet in their conference center in Bellagio, Italy, to consider the safety and efficacy of the method. This panel concluded that? the Bellagio Consensus clearly has been confirmed. . . . The efficacy of LAM has now been well established in prospective studies, and programs should regard LAM as an additional method that increases the family planning choices for postpartum women. Lactational Amenorrhea Method should receive the programmatic and policy support necessary to become available worldwide. . .Programs should ensure that any LAM user is able to begin the new method in a manner th-at ensures continuity of protection from an unplanned pregnancy.
Studies of maternal nutritional recovery postpartum and of outcomes of subsequent pregnancies have shown that spacing of births is necessary Table 1. EFFICACY OF THE LACTATIONAL AMENORRHEA METHOD
Location
Chile Ecuador Philippines Pakistan Multicenter Study (10 sites) Multicenter Follow-up Study53
Study Type
Prospective study with control group Retrospective-prospective study of LAM acceptors in a family planning clinic Prospective clinical study among women with previous breastfeeding experience Prospective clinical study among women with previous breastfeeding experience Prospective study of L A M acceptors in various settings Postmarketing study
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Efficacy: Life Table Analysis
(%I 99.6 98.8
99.0 99.4 98.5 100
LAM = lactational amenorrhea method. From Labbok M, Perez A, Valdes V, et al: The lactational amenorrhea method: A new postpartum introductory family planning method with program and policy implications. Advances in Contraception 1093-109,1994;with permission.
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for improved outcomes.62Child spacing of approximately 3 years (more in developing countries) is recommended for maternal and infant health and infant survival.62Although breastfeeding alone can result in spacing of this duration, individual women are cautioned not to rely on breastfeeding alone if they wish to achieve this goal. Therefore, the introduction and use of family planning during breastfeeding is an important health intervention. The choice of method should be the woman’s, however, she should be given complete information with which to make an informed choice. In general, contraceptive technology texts emphasize efficacy as the major criterion for method acceptance. Child spacing and limitation options for breastfeeding women also might be viewed in a framework as first, second, or third choices for presentation as part of informed choice. The ranking is based on potential effects on breastfeeding, not on the efficacy of the method.3l The nonhormonal methods of family planning are considered firstchoice methods because they have no direct effects on breastfeeding. In addition to LAM, the choices include physical, chemical, and temporal barriers and male and female sterilization. The second method of choice is the progestin-only method that has been extensively tested and found safe in later breastfeeding; however, little information is available in the literature on the use of these methods during the first 6 to 8 weeks post partum among breastfeeding women. Assessment of the studies available, clinical reports, and preliminary guidance from the World Health Organization encourage caution and recommend additional reThe estrogenic methods are search concerning this specific considered the third method of choice because of their known negative effect on milk production. Breastfeeding can significantly affect menstrual loss and fertility but alone cannot provide reliable adequate child spacing for most women. Although additional research is needed to fully understand all of the neuroendocrine mechanisms underlying lactational infertility, clinical studies have outlined the parameters under which breastfeeding may be reliable. LAM should be considered an option in the complete picture of informed family planning for lactating women. NUTRITIONAL STATUS AND BREASTFEEDING Lactation demands maternal nutrient stores and intake. In regions where women are malnourished, a downward spiral from generation to generation may occur in which each new generation has a poor energy, protein, and micronutrient start on life that can never fully be replaced. Unfortunately, the approach in the past has been to try to supplement the infant. The result is shortened breastfeeding duration with concomitant increased disease and shortened interpregnancy interval, resulting in increased risk for the target child, the mother, and the new fetus. In the past decade, a panel to address this problem was assembled, and the results were published as a supplement to the Journal of Tropical Pediatr i c ~The . ~ ~only way to break this cycle of malnutrition is to ensure that
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adolescents enter their procreative years with good nutritional status that is maintained through supplementation to mothers while ensuring optimal breastfeeding, appropriate weaning, and active infant breastfeeding. Bottle-feeding has no role in this vital intervention strateu. To avoid maternal nutritional depletion while ensuring adequate stores for lactation, all women of reproductive age should maintain micronutrient (i.e., vitamin and mineral) stores. During pregnancy, sufficient protein and calories should be consumed so that the mother has stored approximately 2 kg to 4 kg that will be depleted by lactation. During lactation, consumption of an excess 900 calories per day is recommended; however, where a variety of foods is readily available and women eat to their level of hunger and drink to their level of thirst, there is little need to count calories. MENTAL HEALTH AND BONDING
The author finds the literature on mental health and mother-infant bonding sparse and unconvincing. Although much of the literature is scientifically sound, the questions asked rarely directly address the issue of breastfeeding, and when they do, proper definition and timing of pattern shifts in breastfeeding are lacking.*,46 Nonetheless, the biological plausibility that hormonal shifts might be associated with depression seems to be borne out in some studies,- and the sense of empowerment One associated with successful breastfeeding has been study from BarbadosI4 found an association between depressive symptoms at 7 weeks post partum with reduced breastfeeding preference at that time and thereafter. No similar associations were seen at 12 and 26 weeks post partum. Because the period of 6 to 8 weeks post partum is thought to be associated with changes in the hormonal mechanisms supporting breastfeeding,l"this finding invites additional inquiry. Another approach is to assess maternal reports of the reward versus the effort necessary to provide breastmilk for preterms infants.21Most mothers identified some efforts but indicated that breastfeeding rewards were greater. This perception of rewards outweighing efforts is also a reflection of mental attitude but may or may not relate to other aspects of mental health and parental satisfaction. Personal experience (e.g., in countries where breastfeeding is the norm, depression seems to peak at approximately 9 mo post partum, and in countries where breastfeeding is of short duration, depression seems to peak at approximately 3 mo post partum) gives the author the sense that more work is needed on biological and social influences on postpartum depression. SUMMARY
In the rush to find nutrient alternatives to breastfeeding, a theme that dominated research on infant feeding throughout the twentienth
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century, only recently have new findings that reconfirm the importance of breastfeeding for maternal and child health begun to influence medical texts and health policy. Approximately 30 years of increasingly rigorous and positive research findings have led to the rediscovery of breastfeeding as a valid and evidence-based health intervention for infants. Unfortunately, because much of the research was designed to assess human milk as a nutrient replacement for infant formula, the literature on the effects of breastfeeding on maternal health remain limited. Nonetheless, a clear pattern of positive physiologic changes that lead to improved short-term and long-term health sequelae are emerging. All patients and their families should be informed fully as to the positive preventive health effects of breastfeeding not only for infants but also for mothers. Women have many difficult choices to make; it behooves physicians to ensure that they receive all of the facts on which to base these decisions. References 1. Adami H, Adams G, Boyle P, et al: Breast cancer etiology. Int J Cancer 5(suppl):2239,1990 2. Auerbach KG, Jacobi AM: Postpartum depression in the breastfeeding mother. NAACOGS Clinical Issues in Perinatal and Womens Health Nursing 1:375-384,1990 3. Berer M Reducing perinatal HIV trarismission in developing countries through antenatal and delivery care, and breastfeeding: Supporting infant survival by supporting women’s survival. Bull World Health Organ 77%71477,1999 4. Brinton LA, Potischman NA, Swanson CA, et al: Breastfeeding and breast cancer risk. Cancer Causes Control 6:199-208, 1995 5. Byers T, Graham S, Rzepka T, et al: Lactation and breast cancer. Am J Epidemiol 12k664-674, 1985 6. Casagrande JT, Pike MC, Ross RK, et al: ’Incessant ovulation’ and ovarian cancer. Lancet ik170-173, 1979 7. Clark P, de la Pena F, Gomez Garcia F, et al: Risk factors for osteoporotic hip fractures in Mexicans. Arch Med Res 29253-257,1998 8. Kennedy K, Labbok M, Van Look P: Lactational Amernorrhea Method for family planning. Int J Gynaecol Obstet 54:55-57, 1996 9. Coutsoudis A, Pillay K, Spooner E, et ak Influence of infant-feeding patterns on early mother-to-child transmission of HIV-1 in Durban, South Africa: A prospective cohort study. Lancet 354471476,1999 10. Diaz S, Seron-Ferre M, Croxatto HB, et ak Neuroendocrine mechanisms of lactational infertility in women. Biol Res 28:155-163, 1995 11. Enger S, Ross R, Henderson B, et al: Breastfeeding history, pregnancy experience and risk of breast cancer. Br J Cancer 76:118-123, 1997 12. Enger S, Ross R, Paganini-Hill A, et al:Breastfeeding experience and breast cancer risk among postmenopausal women. Cancer Epidemiol Biomarkers Prev 7365-369, 1998 13. Freudenheim JL, Marshall JR, Graham S, et al: Exposure to breastmilk in infancy and the risk of breast cancer. Epidemiology 53324331,1994 14. Caller JR, Harrison RH, Biggs MA, et a1 Maternal moods predict breastfeeding in Barbados. J Dev Behav Pediatr 2080437,1999 15. Gray R, Apelo R, Campbell 0, et a1 The return of ovarian function during lactation: Results of studies from the US and the Philippines. In Gray R (ed): Biomedical and Demographic Determinantsof Reproduction. Oxford, Colorado Press, 1993, pp 45 16. Gwinn ML, Lee NC, Rhodes PH, et al: Pregnancy, breast feeding, and oral contraceptives and the risk of epithelial ovarian cancer. J Clin Epidemiol43559-568,1990
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17. Hight-Laukaran V, Labbok M, Peterson A, et al: Multicenter study of the lactational amenorrhea method (LAM): II. Acceptability, utility, and policy implications. Contraception 55:337-346, 1997 18. Hirose K, Tajima K, Hamajima N, et a1 A large-scale, hospital-based case-control study of risk factors of breast cancer according to menopausal status. Jpn J Cancer Res W146-154,1995 19. Huang W, Newman B, Millikan R, et al: Risk of breast cancer according to the status of HER-2/neu oncogene. Cancer Epidemiol Biomarkers Prev 9:65-71,2000 20. Katsouyanni K, Lipworth L, Trichopoulou A, et al: A Case-control study of lactation and cancer of the breast. Br J Cancer 73814418,1996 21. Kavanaugh K, Meier P, Zimmerman B, et al: The rewards outweigh the efforts: Breastfee-ling outcomes for mothers of preterm infants. Journal of H&an Lactation 13:15-21, 1997 22. Kennedy K: Effects of breastfeeding on women's health. Int J Gynecol Obstet 47(~~ppl):ll-22, 1994 23. Kennedy K, Rivera R, McNeilly A: Consensus statement on the use of breastfeeding as a family planning method. Contraception 39:477496, 1989 24. Krasovec K, Labbok M, Queenan J (eds): Breastfeeding and maternal malnutrition. J Trop Pediatr 37(suppl):1-24, 1991 25. Kreiger N, Kelsey J, Holford T, et al: An epidemiologic study of hip fracture in postmenopausal women. Am J Epidemiol 116:141-148,1982 26. Kritz-Silverstein D, Barrett-Connor E, Hollenbach K Pregnancy and lactation as determinants of bone mineral density in postmenopausal women. Am J Epidemiol13610521059, 1992 27. Labbok M. Hirrht-Laukaran V, Peterson A, et al: Multicenter studv of the lactational amenorrhea method (LAM). I.' Efficacy, duration, and implications ior clinical application. Contraception 55:327-336,1997 28. Labbok M, Laukaran VH. Breastfeeding and family planning. In Sciarra J (ed):Gynecology and Obstetrics, vol. 6. Philadelphia, JB Lippincott, 1992 29. Labbok M, Krasovec K Towards definition of breastfeeding. Stud Fam Plann 21:226240,1990 30. Labbok M, Hendershot G Does breastfeeding protect against malocclusion? An analysis of the 1981 child health supplement to the national health interview survey. Am J Prev Med 3927-232, 1987 31. Labbok M, Cooney K, Coly S Guidelines: Breastfeeding, Family Planning, and the Lactational Amenorrhea Method (LAM). Washington, DC,Institute for Reproductive Health, 1994 32. Labbok M, Perez A, Valdes V, et al: The lactational amenorrhea method: A new postpartum introductory family planning method with program and policy implications. Adv Contracept 1093-109,1994 33. Layde PM, Webster LA, Baughman AL, et a1 The independent associations of parity, age at first full term pregnancy, and duration of breastfeeding with the risk of breast cancer. Cancer and Steroid Hormone Study Group. J Clin Epidemiol42:963-973, 1989 34. Lazi A, Kennedy K, Visness CM, et al: Effectiveness of the lactational amenorrhea method in Pakistan. Fertil Steril M717-723, 1995 35. Lissner L, Bengtsson C, Hansson T: Bone mineral content in relation to lactation history in pre- and postmenopausal women, Calcif Tissue Int 48:319-325,1991 36. Locklin M, Naber S Does breastfeeding empower women? Insights from a select group of educated, low-income, minority women. Birth 2030-35,1993 37. London SJ, Colditz GA, Stampfer MJ, et al: Lactation and risk of breast cancer in a cohort of US women. Am J Epidemiol 132:17-26, 1990 38. Lopez J, Gonzalez G, Reyes V, et a1 One turnover and density in healthy women during breastfeeding and after weaning. Osteoporos Int 6:153-159, 1996 39. Magnusson CM, Persson I, Baron J, et a1 The role of reproductive factors and use of oral contraceptivesin the aetiology of breast cancer in women aged 50-74 years. Int J Cancer 80:231-236,1999 40. Mallmin H, Ljunghall S, Persson I, et a1 Risk factors for fractures of the distal forearm: A population-based case-control study. Osteoporos Int 4298-304, 1994
EFFECTS OF BREASTFEEDING ON THE MOTHER
157
41. McCredie M, Paul C, Skegg D, et al: Reproductive factors and breast cancer in New Zealand. Int J Can&r 76182-188, 1998 42. McNeilly AS, Glasier A, Howie PW Endocrine control of lactational infertility. In Dobbing J (ed): Maternal Nutrition and Lactational Infertility. New York, Vevey/Raven Press, 1985 43. McTiernan A, Thomas D Evidence for a protective effect of lactation on risk of breast cancer in young women. Am J Epidemiol124:353-358,1986 44. Melton LJ 111, Bryant SC, Wagner HW,et al: Influence of breastfeeding and other reproductive factors on bone mass in later life. Osteoporos Int 37643,1993 45. Michels K, Willett W, Rosner 8, et al: Prospective assessment of breasffeeding and breast cancer incidence among 89,887 women. Lancet 347431436, 1996 46. Misri S, Sinclair D, Kuan A Breast-feeding and postpartum depression: Is there a relationship? Can J Psychiatry 42:1061-1065,1997 47. Murrell TGC: Epidemiological and biochemical support for a theory on the cause and prevention of breast cancer. Med Hypotheses 39389-396, 1991 48. Nath DC,Land KC, Singh KK: The role of breast-feedingbeyond postpartum amenorrhea on the return of fertility in India: A life table and hazards model analysis. J Biosoc Sci 26191-206,1994 49. Nduati R, John G, Mbori-Ngacha D, et a1 Effect of breasffeeding and formula feeding on transmission of HnT-1: A randomized clinical trial. JAMA 283:1167-1174,2000 50. Newcomb PA, Storer BE, Longnecker MI', et al: Lactation and a reduced risk of premenopausal breast cancer. N Engl J Med 330:81-87, 1994 51. Newcomb PA, Egan Kh4, Titus-Ernstoff L, et al: Lactation in relation to postmenopausal breast cancer. Am J Epidemiol 150174-182,1999 52. Perez A, Vela P, Masnick GS, et a1 First ovulation after childbirth: The effect of breasffeeding. Am J Obstet Gynecol 114:1041-1047, 1972 53. Peterson A, Labbok M, Hight LV, et a1 Multicenter study of the lactational amenorrhea method (LAM):III. Study with only one follow-up visit. Contraception (in press) 54. Potischman N, Toisi R In-utero and early life exposure in relation to risk of breast cancer. Cancer Causes Control 10561-573,1999 55. Ramos R, Kennedy KI, Visness CM: Effectiveness of lactational amenorrhoea in prevention of pregnancy in Manila, the Philippines: Non-comparative prospective trail. BMJ 313909-912,1996 56. Reuter KL, Baker SP, Krolikowski FJ:Risk factors for breast cancer in women undergoing mammography. Am J Roentgen01 158:27%278,1992 57. Risch HA, Weiss NS, Lyon JL, et al: Events of reproductive life and the incidence of epithelial ovarian cancer. Am J Epidemiol 117:128-139, 1983 58. Rogan WJ, Ragan NB: Chemical contaminants, pharmohetics, and the lactating mother. Environ Health Perspect 102 (suppl 11):89-95, 1994 59. Rogers IS, Golding J, Emmet PM The effects of lactation on the mother. Early Hum Dev 49(suppl):191-203, 1997 60. Romieu I, Hernandez-Avila M, Lazcano E, et al: Breast cancer and lactation history in Mexican women. Am J Epidemioll43543-552,1996 61. Rosenblatt KA, Thomas DB: WHO Collaborative study of neoplasia and steroid contraceptives: Lactation and the risk of epithelial ovarian cancer. Int J Epidemiol 22:192197, 1993 62. Rosero-Bixby L, Oberle MW, Lee NC: Reproductive history and breast cancer in a population of high fertility, Costa Rica, 1984-5. Int J Cancer 40747-754,1987 63. Rutstein S Unpublished observations, 1999 64. Shoham Z Epidemiology, etiology, and fertility drugs in ovarian epithelial carcinoma: Where are we today? Fertil Steril62433-448, 1994 65. Siskind V, Schofield F, Rice D, et al: Breast cancer and breastfeeding: Results from an Australian case-control study. Am J Epidemiol 130229-239, 1989 66. Siskind V, Green A, Bain C, et al: Breasffeeding, menopause, and epithelial ovarian cancer. Epidemiology 8:188-191, 1997 67. Sowers M Pregnancy and lactation as risk factors for subsequent bone loss and osteoporosis. J Bone Miner Res 11:1052-1060, 1996
158
LABBOK
68. Susman V, Katz JL: Weaning and depression: Another postpartum complication. Am J Psychiatry 145498-501,1988 69. Tao SC,Yu MC, Ross RK, et ak Risk factors for breast cancer in Chinese women of Beijing. Int J Cancer 42495498,1988 70. Thomas DB, Noonan EA Breast cancer and prolonged lactation. Int J Epidemiol 2619426,1993 71. Titus-Emstoff L, Egan K, Newcomb P, et al: Exposure to breast miUc in infancy and adult breast cancer risk. J Natl Cancer Inst 90:921-924,1998 72. Tuppurainen M, Kroger H, Saarikoski S, et al: The effect of gynecological risk factors on lumbar and femoral bone mineral density in pen- and postmenopausal women. Maturita 21:137-145,1995 73. Vekemans M. Postpartum contraception: The lactational amenorrhea method. Eur J Contracept Reprod Health Care 2105-111, 1997 74. Weiss H, Potischman N, Brinton L, et al: Prenatal and perinatal risk factors for breast cancer in young women. Epidemiology 8181487,1997 75. Wu A, Ziegler R, Pike M, et ak Menstrual and reproductive factors and risk of breast cancer in Asian Americans. Br J Cancer 73580486,1996 76. Yang CP, Weiss NS, Band PR, et ak History of lactation and breast cancer risk. Am J Epidemiol 138:1050--1056,1993 77. Yo0 KY, Tajima K, Kuroishi T, et ak Independent protective effect of lactation against breast cancer: A case-control study in Japan. Am J Epidemiol 135726-733, 1992 78. Yuan JM, Yu MC, Ross RK, et al: Risk factors for breast cancer in Chinese women in Shanghai. Cancer Res 48:1949-1953,1988 79. Zinaman M, Cartledge T, Tomai T, et a1 Pulsatile GnRH stimulates normal cyclic ovarian function in amenorrheic lactating postpartum women. J Clin Endocrin Metab 80:208azo93,i995
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