Breastfeeding, Fertility, and Family Planning*
Miriam H. Labbok
Table Of Contents
Miriam H. Labbok, MD, MPH
ISSUES IN THE STUDY OF BREASTFEEDING AND FERTILITY
PHYSIOLOGY OF LACTATIONAL INFERTILITY
BREASTFEEDING AND FAMILY PLANNING
Breastfeeding is associated with an increased interval between births; this has been recorded for centuries. Medical literature from Aristotle to the Renaissance, and, occasionally, thereafter, noted that women who suckle are less likely to become pregnant. This phenomenon was forgotten or disbelieved in scientific circles of the 20th century as infant-feeding substitutes replaced breastfeeding behaviors. However, recent scientific evidence compiled by social sciences, demonstrating the population level impact of breastfeeding on fertility, and medical sciences, which now have identified the biologic basis of lactational infertility, has reinitiated interest in both breastfeeding and the mechanisms related to lactational amenorrhea.
Today, breastfeeding is being rediscovered and is slowly becoming normative behavior. Data from the National Survey of Family Growth confirm that about 60% of infants are now breastfed, and most of those infants are still being breastfed at 3 or more months.1 The goal for the nation is to increase this to at least 75%, with 50% continuation to 5 to 6 months. This means that, for an increasing number of postpartum women, the introduction of contraception postpartum occurs during breastfeeding. Physicians must increasingly have the knowledge and skills to support both lactation and appropriate family planning.
Several aspects of this issue may be relevant to clinical practice. These include the special problems in the study of breastfeeding and fertility, basic anatomy, and physiology as they apply to the fertility aspects of breastfeeding, the proper counseling and provision of contraception, and supporting conception during breastfeeding where warranted.
|ISSUES IN THE STUDY OF BREASTFEEDING AND FERTILITY|
There are both research design and analysis-based and conviction-based reasons for conflicting interpretation of the studies of breastfeeding and fertility.
Research Design-Based Issues
DIFFERENT DEFINITIONS OF CHARACTERISTICS UNDER STUDY.
The term breastfeeding is, unfortunately, used to describe a wide variety of behaviors and physiologic states of the mother and the child. The most generally used definition in the 1960s and 1970s was that of the formula industry, which defined breastfeeding in relation to a formula norm. Therefore, the term exclusive breastfeeding was used when breastfeeding was the only source of milk; other foods could thus be given under this definition of exclusive breastfeeding. This definition, which has no relationship to the mother's physiology, continues to be used occasionally, confusing the casual reader of the literature. More recently, the Women, Infants and Children program (WIC) defined a mother-infant pair as breastfeeding if they ever breastfed at all, or breastfed during a specified time period. This has now been modified to be more reflective of nonformula feeding, similar to the definition in previous use.
Several journals have now accepted a definition that allows specification of the pattern of feeding in relation to both maternal and infant action and physiology.2 This schema
*Calls for age of child, feeding frequency and intervals, use of bottle, cup, spoon; pacifier use, and feeding of expressed milk be recorded for each definition where available.
The schema also suggests that researchers and program planners note frequency, timing and length of intervals, age of the child, use of expressed milk, how other milks are given, whether pacifier use allowed, and, where applicable, the type, timing, and amount of other feeds. If used, such a schema would allow differentiating between the specific behaviors and the physiologic consequences.
Another widely used set of definitions was developed subsequently by the World Health Organization (WHO). This definition was modified from that just given in this chapter but changed to apply only to infant nutritional intake.4 This newer set of definitions does not take into account the impact on maternal physiology and potential milk maintenance, the potential differences in behaviors within the definitions used, nor the differences between direct breastfeeding and indirect breast-milk feeding in terms of immunologic and other factors.
These two sets of definitions are contrasted in Table 1.
SAMPLING FRAME AND SAMPLE SIZE.
Immense differences in lactational behaviors indicate that large samples would be necessary to control for this variable alone. However, the relatively short durations of lactation and the prevalence and use of contraceptives that mask or interfere with physiologic changes limit study in industrialized countries. Therefore, much of what we understand is derived from limited clinical studies, some of which have little control over sucking stimulus or age of infant or that information is inferred from larger prospective studies with limited neuroendocrinologic elements.
SELECTION BIAS IN SELECTION OF CASES AND CONTROLS.
Breastfeeding patterns are skewed, with more breastfeeding occurring among those earlier postpartum. With or without breastfeeding, normal maternal physiology undergoes changes postpartum. Therefore, the choice of infant age group/time postpartum studied can significantly influence physiologic outcomes. This is further complicated by the difficulty in random assignment of these breastfeeding and complementary feeding behaviors. It is not ethically possible, nor probable that women would agree, to assign groups of women to breastfeed or not breastfeed. It is even more unlikely that infants will cooperate with the timing of their hunger or the intensity of their suck at any particular time. This may lead to confounding associated with the factors that may influence self-selection into one pattern of feeding or another.
ANALYTIC PLAN AND TECHNIQUES USED.
Proper selection of statistical approach is vital. There are many textbooks designed for the clinician or occasional researcher. The analysis plan should be designed before data are gathered, because it may dictate to some extent the sample frame and size. However, it remains important to reassess the plan after data are collected. The data set may have insufficient numbers in proposed subgroups due to limited variability within the sample or may not reflect other assumption used in planning. For example, if all women in the sample breastfeed for about the same length of time, there will be insufficient variability in the data set to assess the biologic impacts of varying durations of breastfeeding.
SELECTIVE PRESENTATION OF FINDINGS DUE TO JOURNAL SPACE LIMITS.
Because journals frequently limit the length of articles, important facts in the interpretation of the findings may be inadvertently omitted. Also, negative results are rarely accepted for publication.
MISINTERPRETATION OR CONFUSED CONCLUSIONS, AND CONVICTION-BASED BIAS IN PRESENTATION.
In statistics, terms such as association or determinant may be misinterpreted as meaning causation. Two things may be statistically significantly associated but have no biologically meaningful relationship. Although we like to think that scientists are unbiased, each works from personal understanding of the issue in question. This may affect how the hypothesis is stated and tested, and which data are presented. If findings do not support the author's hypothesis or do not achieve statistical significance, it is often difficult to find the energy—or the journal willing—to publish it. Finally, discussion and conclusion sections of papers may include statements that overstate or reinterpret what the findings show.
These difficulties compound the problems of data collection and analysis this already complex area of study.
|PHYSIOLOGY OF LACTATIONAL INFERTILITY|
The anatomy of the breast and the hypothalamic-pituitary axis for release of prolactin and the production of breast milk may be found elsewhere in this text. These same structures are integral to the mammary-hypothalamic-pituitary-ovarian axis that mediates lactational infertility. The current understanding of the physiology of this feedback system is derived from studies of the different systems under conditions of lactation and nonlactation. Because of the difficulties in studying of these phenomena, as previously outlined, this section summarizes current understanding and presents also a summary of studies that confirm the underlying conclusions presented here.
Suckling at the breast, especially with active stimulation of the nipple and areola and the structures that underlie them, stimulates a modification in gonadotropin-releasing hormone (GnRH) release from the hypothalamus, which in turn, disorganizes the pulsatility and levels of follicle-stimulating hormone (FSH) and luteinizing hormone (LH). The result of the disruption of the levels of LH, and the sometimes reduced levels of FSH, is suppression of the development and release of a viable follicle and ovum. If there is some follicular development and estradiol levels rise, there is a paradoxical resuppression of fertility, rather than the stimulation of ovulation seen in nonbreastfeeding women.5 Oxytocin release from the posterior pituitary, which stimulates the let-down reflex, allowing milk to flow through the capillary-like mammary tubules, has not as yet been linked to suppression of fertility; however, its establishment is necessary for successful lactation, and, as such, is a necessary part of the lactational infertility.6 Prolactin plays little role in this feedback system, and maternal nutritional status is much less important than the pattern of infant breastfeeding. Although much remains to be elucidated, the basic parameters of this feedback system may be seen in Figure 1.
Discussion of Research
A recent symposium attempted to bring together scientists to discuss the current understanding and gaps in the knowledge concerning the physiologic basis of lactational infertility. Based on exploration of published and unpublished literature, three stages were identified7: early postpartum lactational amenorrhea, continued lactational amenorrhea, and menses return.
The early postpartum period, in this context, is the 6 to 8 weeks postpartum during which the inhibitory mechanisms of pregnancy continue to produce an impact, with diminished pituitary response to the hypothalamic release of GnRH. This is possibly due to reduced activity of the GnRH pulse generator; however, in the first month postpartum there is no LH response to a GnRH bolus. Studies of LH activity during this same period have yielded variable findings, indicating that there may be individual or behavior-based variation. Another study shows that the LH pulse frequency is not significantly different from that found in the early follicular phase; the peak levels, however, are significantly reduced.8 By the second postpartum month, LH response to a GnRH bolus may be seen, indicating a shift in the underlying mechanisms.9 This would imply decreased end-organ receptivity, in this case the pituitary. Opiates do not seem to mediate this shift in humans as they do in some nonhuman animal models.10 The timing of this shift may be dictated by intensity and pattern of feeding or by individual physiologic differences.
Those factors that influence the duration of continuing lactational amenorrhea, in relation to the duration of lactation, are not fully understood. At the same time, ongoing diminished GnRH and pituitary responsiveness continue in relationship to the intensity of the suckling stimulus. However, quantifying this phenomenon is difficult. Other mechanisms are thought to contribute, creating a complex of sometimes-conflicting feedback loops. These include enhanced or paradoxical 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 biologic activity of the hormones of ovulation; and a variable role of prolactin. It was concluded that there is a possibility of redundancy in these mechanisms.6
Attempts to elucidate the role of prolactin have found little direct involvement in the suppression of fertility. One important study included 20 women, with 24-hour blood sampling every 10 minutes, at either 4 or 8 weeks postpartum, at either time of introduction of supplements, at first menses while continuing breastfeeding, and in the follicular phase of the first cycle after weaning. Results included that the pattern of prolactin levels was responsive to breastfeeding pattern, but that there was no relationship between the plasma concentrations, day or night, and the duration of amenorrhea. There was, however, a strong and statistically significant correlation between the timing of introduction of supplements and the duration of amenorrhea.11 Another study of 10 women in Chile found that women who returned to fertility earlier exhibited a smaller prolactin response to suckling as early as the first month postpartum than was found among those with a delayed return of fertility.12 Although prolactin levels clearly are responsive to suckling, and there is an association of prolactin response and earlier return of menses, the pattern of prolactin release is not predictive of fertility return for the individual.
Another long-held hypothesis was that maternal fat stores dictated the duration of lactational infertility. To investigate the extent to which better maternal nutrition is associated with a reduction in the duration of lactational amenorrhea, data on 339 mother-infant pairs were analyzed.13 Maternal triceps skinfold was negatively associated with the length of amenorrhea; once controlled for infant feeding pattern, the effect was small; only a 0.5-month difference was seen when the 25th and 75th percentiles were compared. Improved maternal nutritional status by supplementation was not associated with change in length of amenorrhea when infant supplemental feeding was controlled for. This suggests that infant, not maternal, supplementation influences the duration of lactational amenorrhea, and that maternal nutritional status has modest influence. In a recent review of the physiology of lactation, Neville raises the possibility that another hormone associated with nutritional status, such as the appetite-suppressing hormone leptin, may play a role.14 Clearly, although the impact of nutritional status on lactational amenorrhea is less significant than earlier believed, the factors that mediate this association remain to be elucidated.
The return of menses during lactation is highly variable, among individuals and among cultural groupings.15,16 There are many behavioral and physiologic parameters that may have some impact on the timing of the return of fertility during lactation. Clearly, the sucking stimulus is a major variable and accounts for much of the variation seen. Frequency, with recovery time during the interval between feeds, intensity of the child's suckling, and hence breast stimulation, and the sensitivity of the nipple and areola of the breast, may all play a role. There appears to be increased pituitary responsiveness to GnRH over time; however, the presumed mediation by β-endorphins or opiates, has not been substantiated in humans. Whether it is dictated by individual variation in neuroendocrine response to the stimuli, variation in bioactivity of specific hormones and end organ, including ovarian, response to the changes remains to be assessed.
Fertility does not necessarily return immediately with the return of regular vaginal bleeds. The first cycles during breastfeeding frequently are associated with abnormal ovulatory activity and luteal phase defects. Studies have found, on average, a gradual return to normality over the first three cycles. An analysis of survey data found that, in areas where breastfeeding is practiced physiologically, that is, frequently day and night with little to no supplementation given, the continuation of breastfeeding after menses return is associated with significant continuing delay in fertility. In this study, for each addition month of breastfeeding after menses return there is about 7.4% reduction in risk of conception.17 This is thought to be primarily due to ongoing luteal phase defects.18
Differentiation of the first hormonally induced bleed from continued lochia or perceived end-of puerperium bleeding episodes may present an issue for some women, especially those interested in charting their cycles or predicting the next bleed. A multicenter multinational study of the return of a hormonally induced bleed, retrospectively defined as a bleed followed by another bleed within 21 to 70 days. This study found that duration of lochia varied significantly and concluded that among intensively breastfeeding women, about 11% experienced such a bleed in the first 2 months postpartum.19
The suckling stimulus is key throughout the duration of the feedback; however, the specific attributes of the suckling that contribute to the suppression of fertility are not readily elucidated. Clearly, frequency of the suckling episodes is vital. In the very early postpartum stage, suckling of 10 to 12 times a day appears 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 of or increase in supplementation are associated with hastened return of both ovulation and return of menses.17,20 After menses, or regular bleeds, recurs, frequent suckling continues to be associated with decreased fertility. Other parameters of the suck stimulus have been harder to study. In an effort to assess the impact of sucking intensity, a pressure transducer was attached to the nipple of exclusively breastfeeding women (n = 62) at 2 and 5 months postpartum. Although the efficiency and duration of the suckling, per se, were not correlated with duration of amenorrhea, the time at the breast in nonsuckling pauses was positively associated with a delay in menses return.21 This may indicate that sensory stimulation other than suckling alone may have a vital role in the feedback to the hypothalamus. Possible areas for further exploration include the importance of olfaction in early mother-infant bonding22 and cosleeping. These areas remain to be studied in relation to the duration of lactational infertility, and the physiologic impact of behaviors and sensory stimuli.
|BREASTFEEDING AND FAMILY PLANNING|
Contraceptive Use During Lactation
Studies of maternal nutritional recovery postpartum and of outcomes of subsequent pregnancies have shown that spacing of births is necessary for improved outcomes. Child spacing of about 28 months is suggested as healthiest for pregnancy outcomes in a U.S.-based population.23,24 In developing country settings, spacing of this length or longer is recommended.25 Although breastfeeding alone can result in spacing of this duration, the individual woman is cautioned not to rely on breastfeeding alone if she wishes to achieve this goal. Therefore, the introduction and use of family planning during breastfeeding are important health interventions.
The choice of method should be the woman's, based on complete information on which to make an informed choice. Counseling is generally necessary to ensure that this fully informed choice can occur. Generally, contraceptive technology texts emphasize efficacy as the major criterion for method selection. In fact, women's choices are generally based on various other factors, including personal experience, a desire to delay or permanently cease childbearing, lifestyle, and religious influences. She might also be influenced by the other health impacts of the method on her or her child, in addition to those directly associated with breastfeeding and contraceptive efficacy. Some of these are presented in Table 2.
*Hormonal methods may have long-term health benefits for women including decreased rates of reproductive tract cancers; methods that reduce menstrual blood loss would contribute to anemia reduction.
(Hatcher R, Rhinehart W, Blackburn R et al: The Essentials of Contraceptive Technology pp 4---19. Baltimore: Johns Hopkins School of Public Health, Population Information Program, 1997.)
Table 3 presents the method options categorized by potential impact on breastfeeding, not on efficacy of the method or the other issues that may be of interest to the individual patient. (The American College of Obstetrics and Gynecology issued guidelines on aspects of breastfeeding. The guidelines support Table 3 while allowing earlier initiation of hormonal methods when appropriate.)
*Most pregnancy, or failure, rates as presented are from life-table analyses in studies of women who are not breastfeeding. These rates would be expected to be lower when used during breastfeeding due the additive impact of to its fertility suppressive effects. Pregnancy rates presented are based on studies of use during lactation.
(Modified from Hatcher R, Rhinehart W, Blackburn R et al: The Essentials of Contraceptive Technology, pp 4---19. Baltimore: Johns Hopkins School of Public Health, 1997; and Labbock M, Cooney K, Coly S: Guidelines: Breastfeeding, Family Planning and the Lactational Amenorrhea Method. 2nd ed. Washington, DC: Institute for Reproductive Health, 1994)
Nonhormonal methods are considered the first choice because they have no direct impact on breastfeeding. The lactational amenorrhea method (LAM), described later in this chapter, may be used as in introduction to other method selection, or as the primary method in the early months. In addition to LAM, the choices include physical, chemical, and temporal barriers, as well as male and female sterilization.
Second choice is the progestin-only methods that have been extensively tested and found safe in later breastfeeding.30 In the last decade, possible association with maternal bone loss became an issue. A prospective study of levonorgestrel (Norplant), progesterone vaginal rings, and CuT380 intrauterine devices (IUDs) found no difference in bone status among the three groups at months 1 and 12 postpartum, and at 6 and 12 months after cessation of lactation.31 There are many studies of vaginal rings, a method not as yet approved for use in the United States, that show this to be a safe and efficacious method for lactating women, however, there remain issues of user satisfaction.
The timing of introduction of progestin-only methods continues to be debated. There is little in the literature on the use of these methods during the first 4 to 6 weeks postpartum among fully breastfeeding women. Assessment of the studies available, clinical reports, and preliminary guidance from the WHO would encourage caution, recommending delay of use for at least 6 weeks postpartum, and calling for further research concerning this specific situation.
The estrogenic methods, despite their higher efficacy, are considered third choice because of their known negative effect on milk production. Other concerns, such as changes in micronutrients, including iron, calcium, copper and phosphorus, seem unfounded.32,33 Consideration has been given to whether a woman should switch from the less efficacious progesterone-only methods to the estrogenic methods at some point during lactation. An opinion poll of 20 providers considered to be expert in the field concluded that there is no reason to switch during early lactation but that there is no problem with doing so after 6 months postpartum.34
Breastfeeding can significantly reduce menstrual loss and fertility, but alone, cannot provide reliable adequate child spacing for most women. Although further research is needed to understand all the neuroendocrine mechanisms underlying lactational infertility fully, clinical studies have outlined the parameters under which breastfeeding can be reliable. LAM should be considered an option in the complete picture of informed family planning choice for the lactating woman.
Family Planning Based on the Physiology of Lactation
There has been interest in building on lactational infertility to create a reliable, efficacious form of family planning for more than 25 years. In the 1970s, researchers began to publish studies showing that under clinical conditions of full breastfeeding and amenorrhea, fertility would be a rare event.20 At the same time, Tyson and others pursued the pituitary-gonadotrophin route, assessing the impact of thyrotropin-releasing hormone (TRH) and other related hormonal releasing hormones on fertility.35,36 More recently, it has been suggested that GnRH agonists might enhance the impact and duration of lactational infertility.37 These approaches that enhance or suppress the hormonal feedback system have been associated with acceptable side effects. Although there is a high correlation of the timing postpartum of fertility return with previous breastfeeding experience when measured in a population of women, this is not a reliable indicator for the individual.
Stimulated by early publications, many researchers began to explore the relationship between breastfeeding patterns, menses return, and fertility suppression to see whether a noninvasive approach based on an improved understanding of the physiology might be possible. In 1988, the research findings of several centers around the world were 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.38 A few months later, this approach was presented to a group of family planning service providers at a meeting at Georgetown, in the District of Columbia, and LAM was developed as a clinical algorithm, and guidelines were prepared.39
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 would be asked whether her menses have resumed, whether she is no longer fully or nearly fully breastfeeding, and whether the infant is 6 months of age or older. If the answer to any of these is affirmative, she is advised to begin another method of family planning, preferably one that will have no negative effects on lactation (Fig. 2). Counseling includes timely switch to another method compatible with lactation, and the encouragement of healthy birth spacing of about 2.5 to 3 years, allowing for maternal recovery postpartum and postlactation before another pregnancy commences.
Because this method is based on behavior, there is no organization in the United States with the mandate to review its safety. For this reason among others, the WHO, Family Health International, and the Institute for Reproductive Health/Department of Obstetrics and Gynecology/Georgetown University assembled a second international recognized panel. The Rockefeller Foundation approved a second Bellagio conference that was held to consider the safety and efficacy of the method. Based on LAM clinical trials and WHO multicenter studies that had confirmed that fully lactating amenorrheic women have about a 1% chance of pregnancy, this panel concluded the following:
This new method of family planning has been found to be highly effective (Table 4), 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.49 Duration of LAM use, which contributes to effectiveness of the method, varied across these studies, averaging about 4 to 5 months. Duration of the method in common usage has been shown to depend on ambient breastfeeding norms and maternal commitment, in addition to physiologic predisposition. Although this is important to the individual, it may not have a significant impact on lifetime fertility. Therefore, the recommendation to switch to another method in a timely manner is best accompanied by counseling for at least 3-year intervals between children. At least one study has shown that LAM provision is associated with a lengthened birth interval.50
*Significant loss to follow-up.
LAM, lactational amenorrhea method.
Success in the provision of this method is enhanced when there is adequate breastfeeding support available to the mother and when she is properly counseled in those breastfeeding behaviors associated with fertility suppression. Based on the physiologic responses, LAM counseling should include discussion of optimal breastfeeding behaviors for both lactation maintenance and fertility suppression, and the importance of birth spacing and the timely switch to another method of family planning. Studies indicate that the frequency of the breast stimulation and the maintenance of short intervals between feeds (no longer than 4 hours during the day or 6 at night) seem to be associated with lactation maintenance.
For the longest use of the method, 6 months of exclusive breastfeeding is required. Although international guidance has called for 4 to 6 months of exclusive breastfeeding since the expansion of growth charting in the 1970s, many studies now indicate that less than 6 months exclusive breastfeeding may carry excess health risks.51,52 Work by Dewey and colleagues with random assignment at 4 months to continue exclusive breastfeeding or to begin a high-quality, clean supplement provided free of charge, two important findings were noted: there was a significant decrease in the breast milk intake and amenorrhea at 6 months was decreased by 20%.53,54 Clearly, the use of this method, and the practice of optimal breastfeeding in general, are linked to lifestyle choices for the mother.
In the diagnosis of infertility, breastfeeding and lactational amenorrhea status should be one of the first aspects of the medical history addressed. Other factors that should be considered include the possibility of subclinical infection associated with secondary infertility, and, where appropriate, extreme altitudes.14,55 This normal fertility delay may not be welcome among women who wish to plan a subsequent pregnancy and are not concerned with the public health guidance concerning spacing of births.
It is not always necessary to advise cessation of breastfeeding in these cases; adjustment of feeding pattern to favor return of ovulation is a possible alternative. Because hormonal responses are thought to be greater at night, it is suggested that night feedings be limited, and that total 24-hour frequency of breast stimulation be reduced. This should not be recommended unless the infant is independent of the need for breastfeeding for nutrition, health, and immune system development. Lactational infertility may continue even after menses appear to be normal, so counseling should include the possibility of an extended time line, and assurances that optimal maternal nutritional recovery occurs with cessation of breastfeeding when mother and baby decide, followed by about 6 months of nonlactation, nonpregnant status.
3. Zinaman MJ, Hughes V, Queenan JT et al: Acute prolactin and oxytocin responses and milk yield to infant suckling and artificial methods of expression in lactating women. Pediatrics 89: 437– 440, 1992
10. Kremer JA, Borm G, Schellekens LA et al: Pulsatile secretion of luteinizing hormone and prolactin in lactating and nonlactating women and the response to naltrexone. J Clin Endocrinol Metab 72: 294– 300, 1991
11. Tay CC, Glasier AF, McNeilly AS: Twenty-four hour patterns of prolactin secretion during lactation and the relationship to suckling and the resumption of fertility in breast-feeding women. Hum Reprod 11: 950– 955, 1996
13. Kurz K, Habicht JP, Rasmussen KM et al: Effects of maternal nutritional status and maternal energy supplementation on length of postpartum amenorrhea among Guatemalan women. Am J Clin Nutr 58: 636– 642, 1993
15. WHO Task Force on Methods for the Natural Regulation of Fertility: The WHO Multinational Study of Breast-feeding and Lactational Amenorrhea: I. Description of infant feeding patterns and of the return of menses. Fertil Steril 70:448–460, 1998
16. WHO Task Force on Methods for the Natural Regulation of Fertility. The WHO Multinational Study of Breast-feeding and Lactational Amenorrhea: II. Factors associated with the length of amenorrhea Fertil Steril 70:461–471, 1998
17. Gray R, Apelo R, Campbell O et al: The return of ovarian function during lactation: results of studies from the U.S. and the Philippines. In Gray R (ed): Biomedical and Demographic Determinants of Reproduction, pp 428–445. Oxford: Colorado Press, 1993
18. Diaz S, Cardenas H, Brandeis A et al: Relative contributions of anovulation and luteal phase defect to the reduced pregnancy rate of breastfeeding women. Fertil Steril September 58: 498– 503, 1992
19. WHO Task Force on Methods for the Natural Regulation of Fertility. The WHO Multinational Study of Breast-feeding and Lactational Amenorrhea: IV. Postpartum bleeding and lochia in breastfeeding women. 72:441–447, 1999
26. Farr G, Rivers R: Interactions between intrauterine contraceptive device use and breastfeeding status at time of insertion: analysis of Tcu-380A acceptors in developing countries. Am J Obstet Gynecol 167: 144, 1992
29. Shaaban M, Olind V, Salem H et al. Levonorgestrel concentration in maternal and infant serum during use of subnormal levonorgestrel contraceptive implant, Norplant, by nursing mothers. Contraception 1986, 33:357
30. Diaz S, Zepeda A, Maturana X et al: Fertility regulation in nursing women. IX. Contraceptive performance, duration of lactation, infant growth, and bleeding patterns during use of progesterone vaginal rings, progestin-only pills, Norplant implants, and copper T 380-A intrauterine devices. Contraception 56: 223– 232, 1997
31. Diaz S, Reyes MV, Zepeda A et al: Norplant implants and progesterone vaginal rings do not affect maternal bone turnover and density during lactation and after weaning. Hum Reprod 14: 2499– 2505, 1999
45. Labbok M, Hight-Laukaran V, Peterson A et al: Multicenter study of the lactational amenorrhea method (LAM): I. Efficacy, duration, and implications for clinical application. Contraception 55: 327– 336, 1997
47. WHO Task Force on Methods for the Natural Regulation of Fertility: The WHO Multinational Study of Breast-feeding and Lactational Amenorrhea. III. Pregnancy during breastfeeding. Fertil Steril 72:431–440, 1999
53. Cohen R, Brown KH, Canahuati J et al: Effects of age of introduction of complementary foods on infant breast milk intake, total energy intake, and growth: a randomised intervention study in Honduras. Lancet 344: 288– 293, 1994
54. Dewey KG, Cohen RJ, Rivera LL et al: Effects of age at introduction of complementary foods to breast-fed infants on duration of lactational amenorrhea in Honduran women. Am J Clin Nutr 65: 1403– 1409, 1997