Relative contributions of anovulation and luteal phase defect to the reduced pregnancy rate of breastfeeding women*

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1 - FERTILITY AND STERILITY Copyright c() 1992 The American Fertility Society Printed on acid-free paper in U.S.A. Relative contributions of anovulation and luteal phase defect to the reduced pregnancy rate of breastfeeding women* Soledad Diaz, M.D.t:j: Hugo Cardenas, Ph.D.t Astrid Brandeis, B.A.t Patricia Miranda, R.N. II Ana M. Salvatierra, R.N.II Horacio B. Croxatto, M.D.t Ponti/icia Universidad Cat6lica de Chile and Instituto Chileno de Medicina Reproductiva, Santiago, Chile Objective: To evaluate the contribution of anovulation and luteal phase defects to lactational infertility. Design: Prospective longitudinal follow-up. Setting: Outpatient clinic. Subjects: Forty-nine women fully nursing and amenorrheic on day 75 postpartum and 25 cycling, interval non-nursing women. Interventions: Plasma prolactin, luteinizing hormone, estradiol (E 2), and progesterone (P) levels twice a week up to the second postpartum menses. Main Outcome Measures: Ovulation rate and endocrine profile of the menstrual cycles. Results: Ovulation rates were 37% and 97% at 6 and 12 months postpartum; 67% of ovulations occurred in amenorrhea. The luteal phase was shorter, and E2 and P levels were lower in lactating women than in non-nursing women. These parameters were closer to normal in the second cycle than the first, in spite of active nursing. The risk of ovulation and pregnancy in amenorrhea was 27.7% and 0.9% at month 6 postpartum. After the first menses, these risks were 93% and 7%, respectively. Conclusion: The abnormal endocrine profile of the first luteal phase offers effective protection to women who ovulate during lactational amenorrhea within the first 6 months after delivery. Later luteal phases are improved and women are at risk of pregnancy. Fertil Steril 1992;58: Key Words: Breastfeeding, anovulation, luteal phase defect, ovarian function, lactational infertility Lactational amenorrhea is associated with extremely low pregnancy rates (PRs) and the first postpartum cycles of nursing women (1-4) are also Received October 14, 1991; revised and accepted May 5, * Supported by grant from the World Health Organization, Special Programme of Research Development and Research Training in Human Reproduction, Geneva, Switzerland, by grant CB 87.10A/ICCR from the Population Council, and by grant from the Rockefeller Foundation, New York, New York. t Laboratorio de Endocrinologia, Facultad de Ciencias Biologicas. :\: Reprint requests: Soledad Diaz, M.D., Facultad de Ciencias Biologicas, Laboratorio de Endocrinologia, Pontificia Universidad Catolica de Chile, Casilla 114-D, Santiago, Chile. Technician. II Consultorio de Planificacion Familiar, Instituto Chileno de Medicina Reproductiva. associated with decreased fertility. This can be explained by a low incidence of ovulation during the amenorrheic period and the occurrence of anovulatory bleedings or abnormal cycles later on (5-9). Compared with other groups (6,9,10), urban Chilean nursing women experience a relatively high risk of menstruation and ovulation even when they are fully breastfeeding (3). Their risk of pregnancy during amenorrhea is low, but the PR increases rapidly after the recovery of menses (11, 12). This suggests a high incidence of normal ovulatory cycles in spite of nursing. To test this possibility, a longitudinal study was performed to assess the risk of ovulation during the 1st postpartum year before and after the end of amenorrhea, the characteristics of the first postpartum cycles, and their contribution to the pattern of fertility observed during breastfeeding. 498 Diaz et al. Ovarian function and lactational infertility Fertility and Sterility

2 MATERIALS AND METHODS A detailed description of the admission criteria, follow-up procedures, and breastfeeding management has been published (3). The aspects relevant to this report are summarized in the following paragraphs. Characteristics of the Subjects Nursing cases were selected from urban postpartum women who wanted to breastfeed their child for as long as possible. None had a previous history of infertility, irregular menstrual cycles, or endocrine or gynecological pathology before pregnancy. Other criteria for selection were: ages 18 to 38 years, parity 1 to 5, normal pregnancy, vaginal term delivery of a healthy child of normal birth weight, no chronic disease or condition requiring continuous drug therapy, choosing an intrauterine device (IUD) for contraception, * willing to participate in the blood sampiing protocol, and being fully breastfeeding and amenorrheic at day 75 postpartum. Forty-nine of the 96 subjects enrolled during the first postpartum month met these final admission requirements. A contemporary control group was established with 25 non-nursing healthy women of proven fertility, who had not delivered recently, who were within the same age and parity range as the nursing group, and who were using nonhormonal contraceptives (IUDs or sterilization). To compare the risk of ovulation and pregnancy, we used the data obtained in a comparable population of unprotected nursing women who participated in a contemporary study on the contraceptive efficacy of breast feeding (11, 12). These women were selected according to the same biomedical criteria as the study group. They also had a similar socioeconomic status and were followed in the same clinic using comparable follow-up procedures and breastfeeding management. We assumed a similar endocrine profile in the protected and unprotected groups. The data were reanalyzed including only the subsample of women who were also amenorrheic and fully nursing at day 75 postpartum. Follow-up Follow-up took place at the Consultorio de Planificaci6n Familiar, affiliated with the Instituto Chileno de Medicina Reproductiva (ICMER). Women * The Catholic University was not involved in the clinical fol low-up or contraceptive administration done at the Consultorio de Planificacion Familiar (rcmer). were given an appointment at days 7, 20, and 30 postpartum for clinical evaluation, reinforcement of instructions for breastfeeding on demand, and information on the choices available to avoid a new pregnancy. A monthly calendar was provided to record the number of nursing episodes each day and night and all bleeding or spotting days. On days 30 to 35 postpartum, a general physical, pelvic and breast examination, Papanicolaou smear, and hemoglobin (Hb) were performed. Only healthy women with an adequate nutritional status and Hb values > 120 gil were admitted. Thereafter, follow-up visits were scheduled fortnightly up to the end of the 1st year or the occurrence of the second postpartum bleeding, whichever came last. At each visit, the daily breastfeeding chart and the bleeding record were reviewed. Mothers and infant underwent a physical examination. All intercurrent diseases were recorded. Breastfeeding Management The women were instructed to give their infants no liquid or solid food or water and to use the breast as the only source of water and nutrients during the first 6 months postpartum, except for the administration of vitamin drops. These instructions were reinforced at each visit. However, milk supplements were indicated when inadequate milk output was diagnosed. Infant weight gain was considered the most sensitive indicator of the adequacy of milk output. Milk supplements were prescribed when the infant's average weight increase was <20 gld, with the exception of those infants who continued in their weight percentile curve ± 1 SD or those whose absolute weight was higher than expected for their age and length. The Boston percentile weight curve for male infants was used as the reference standard (13). A single nondairy meal was recommended routinely to full nursing infants after the 6th postpartum month, and a second meal was introduced at the 9th month. Blood Sampling Protocol Samples were scheduled at approximately 10 A.M. every 15 or 30 days during the first 3 months postpartum and twice a week thereafter. In a few cases, blood sampling was started later (month 2, n = 6; month 3, n = 7; month 6, n = 1). Additional samples were drawn 10 minutes after the initiation of suckling at 15 to 30-day intervals. Control women were sampled twice a week during one menstrual cycle. Prolactin (PRL) and estradiol (E 2) were measured in all samples available. Luteinizing hormone (LH) Diaz et al. Ovarian function and lactational infertility 499

3 and progesterone (P) were measured once a week up to 30 days before the first menses and in all samples thereafter. Samples for this study were obtained during 1980 and 1981 and were assayed from 1982 through Hormone Assays Determinations of PRL, LH, E2, and P were made using the reagents and methodology of the World Health Organization, Programme for the Provision of Matched Assay Reagents for the Radioimmunoassay (RIA) of Hormones in Reproductive Physiology. Assays of each hormone were done simultaneously for all samples collected from an individual case. Intra-assay and interassay coefficients of variation (CVs) for LH were 5%,10%, and 15% and 14%, 11%, and 29% for high (53.6 ± 6.2 lull), medium (26.5 ± 2.9 lull), and low (5.3 ± 1.5 lull) pools, respectively. Intra-assay and interassay CVs for PRL were 10%, 15%, and 9% and 18%, 17%, and 22% for high (4,559 ± 825 mull), medium (1,445 ± 253 mull), and low (312 ± 69 mull) pools, respectively. Intra-assay and interassay CVs for E2 were 6, 7, and 21 and 13, 15, and 17 for high (1,554 ± 194 pmol/l), medium (922 ± 140 pmol/l), and low (257 ± 23 pmol/l) pools, respectively. Intra-assay and interassay CVs for P were 10, 12, and 18 and 18, 17, and 25 for high (32.1 ± 6.0 nmol/l), medium (16.8 ± 3.0 nmol/l), and low (1.4 ± 0.3 nmol/l) pools, respectively. Pool values are shown as means ± SD. Data Presentation and Analysis First Postpartum Ovulation The occurrence of ovulation was indirectly assessed by P and LH levels. Progesterone values> 10 nmol/l were considered compatible with ovulation. This level is achieved within 3 to 4 days after the LH peak in normal women in whom the occurrence of ovulation has been confirmed by the recovery of an oocyte from the fallopian tube (14). Levels above this threshold have never been observed in the follicular phase of the menstrual cycle in our control population. Luteinizing hormone values > 39 lull were considered as preovulatory surge values. The date of ovulation was determined retrospectively for each subject. The day after the LH surge, if detected, or the intermediate day between the last P level < 6 nmol/l and the first P level> 10 nmol/l were considered to be the day of ovulation. First Postpartum Bleeding The first bleeding consisting of at least 1 day of normal bleeding or 3 consecutive days of spotting was recorded 10 or more days after the end of the puerperal bleeding. Bleeding induced by the insertion of an IUD was not considered in the analysis. First Cycle The events before and after the first ovulation after delivery up to the day before the following menses constituted the first cycle. Nonovulatory intervals between bleedings were not considered cycles. Exclusive Breastfeeding or Full Nursing Women were classified in this category while the breast was the only source of water and nutrients for the infant during the first 6 months and if the child had a normal growth rate according to the Boston reference (13) standard. In this analysis, cases were kept in this category after 6 months if only nondairy food was introduced. Probabilities of first bleeding and first ovulation and pregnancy were calculated by life table analysis. Characteristics of the subjects at the time of first and second ovulation, suckling frequency, and the mean hormonal levels were compared using Student's t-test. The area under the curve (AUC) was calculated for E2 and P, and the values were compared using Student's t-test. Distributions according to nursing categories and highest P level were analyzed by contingency table analysis. The SAS statistics software (SAS Institute Inc., Cary, NC) was used for data analysis. Probability values < 0.05 were considered significant. RESULTS Of the 49 women enrolled in the study group, 43 (88%) ovulated while breastfeeding during the 1st postpartum year. Four of the other 6 women left the study, one completed the year still in amenorrhea, and one had not ovulated when she weaned at month 8. Cumulative probabilities of experiencing the first ovulation and the first bleeding during the 1st postpartum year are shown in Table 1. The risks were nil for the first 2 postpartum months because the study protocol required that all subjects should be amenorrheic and fully nursing at day 75 postpartum. The probability increased with time for both events. Ovulation occurred before the first postpartum bleeding in 12 (67%) of the 18 women who ovulated within months 3 to 6 and in 17 (68%) of the 25 women who ovulated within months 7 to 12. Eleven women ovulated after one bleeding, and three did so after two or more bleedings. In this sample, the 500 Diaz et al. Ovarian function and lactational infertility Fertility and Sterility

4 Table 1 Cumulative Probability of Experiencing the First Bleeding and the First Ovulation During Breastfeeding Table 2 Breastfeeding Status at the Time of the First and Second Postpartum Ovulation First bleeding First ovulation Postpartum length N* CPt N CP rno Breastfeeding (%) Fully Nondairy supplements Milk supplements Suckling frequency (means ± SD) 24 h Night * P = First (n = 43) ± ± 0.2 Ovulation Second (n = 33) ± 0.4* 1.9 ± 0.2 * Number of women entering the month without having experienced the first bleeding or the first ovulation. t Cumulative probability X 100. first menses was a good indicator of the recovery of ovulation. Twenty-eight (57%) women remained fully nursing, and 21 (43%) introduced milk supplements within postpartum months 3 to 6. The first ovulation occurred in this interval in 10 (35.7%) ofthe 28 fully nursing women and in 18 (85.7%) of the women who introduced bottle feeding, showing a significant influence (P < 0.001) of milk supplementation on the risk of ovulation during breastfeeding. In another 15 women, the first ovulation was observed within months 7 to 12 postpartum after the introduction of nondairy food (n = 12) or milk supplements (n = 3). The first and second postpartum ovulatory cycles were studied in 43 and 33 cases, respectively. The breastfeeding status at the time of each ovulation is shown in Table 2. The total suckling frequency per 24 hours decreased significantly from the first to the second cycle but not the suckling frequency at night. Estradiol and P levels observed in the first and second postpartum cycle and in control cycles are shown in Figure 1. Progesterone levels (AVC) were lower in the first (P < ) and second (P = 0.001) cycle during breastfeeding than in control cycles and also in the first postpartum cycle in comparison with the second cycle (P = 0.02). Estradiol levels (AVC) were significantly lower (P < ) in the first and in the second (P = 0.002) postpartum cycle in comparison with the control cycles but did not differ between the first and second cycle. Table 3 shows selected parameters of the first and second cycle during breastfeeding and in control cycles. The length of the first cycle and of the first follicular phase was calculated only for those cases whose first ovulation followed the first menses, excluding one woman who got pregnant in that cycle. The length of the cycle and of the follicular phase were significantly longer in nursing than in nonnursing women. The first luteal phase and its highest P value were significantly shorter and lower than the second or those of the control group. The highest E2 level of the luteal phase was lower in nursing than in non-nursing women. No significant differences were found in PRL basal levels, the length ofthe luteal phase, the highest E2 levels in the follicular and luteal phase, and I II C... '::I! ~ '" w ':J '::I 60 J 40 J4~~ ~~~...,,, iii 0,,,,,,, w z 0 w... '" U> W g '" lo ~lo 0 lo -lo 0 lo III\VS N = 43 N = 33 N = 25 Figure 1 Estradiol and progesterone levels (means ± SE) during the first (I) and second (II) postpartum cycle in nursing women and in interval non-nursing women (C); day 0 = day of ovulation. E2 I < E2 C (P < ); E2 II < E2 C (P = 0.002); P I < P II (P = 0.02); P I < PC (P < ); P II < PC (P = 0.001). Differences calculated for the AVC using Student's t-test. Diaz et ai. Ovarian function and lactational infertility 501

5 == Table 3 Selected Parameters of the First Two Ovulatory Cycles in Lactating Women and Cycles in Nonlactating Women* Parameter Length (d) Cyclet Follicular phaset Luteal phaset:j: Basal PRL OUjL)t Highest E2 (pmol/ L) First cycle (n = 43) 36.1 ± ± ± ± 82 Breastfeeding status Lactating Second cycle (n = 33) 36.6 ± ± ± ± 80 Follicular phase 793 ± ± 53 Luteal phaset 558 ± ± 45 Highest P (nmol/ L) Nonlactating (n = 25) 26.6 ± ± ± ± ± ± 70 Luteal phaset 23.8 ± ± ± 3.1 * Values are means ± SE. t Cycles occurring before first menses (n = 29) excluded from mean length of the first cycle and first follicular phase. Lactating women significantly different (P < 0.05) from nonlactating women. t First cycle significantly different (P < 0.05) from second cycle. the highest P level when comparisons were done between the first ovulatory cycles that occurred before the first bleeding versus those occurring after the first bleeding, those occurring in exclusive breastfeeding versus those occurring in supplemented nursing, and those occurring before or after day 180 postpartum (data not shown). The first postpartum cycle had all P levels < 15 nmoljl in a significantly higher proportion of cases (28%) in comparison with the second (4%) or with the control cycles (0%). The second postpartum cycle and the control cycles were similar in this respect. Luteal phases> 10 days with P levels> 30 nmoljl were found only in 2 of 12 and 3 of 17 cases who ovulated in amenorrhea before and after 6 months postpartum, respectively. The risk of ovulation during lactational amenorrhea described here was compared with the risk of pregnancy during amenorrhea in unprotected nursing women who met the same requirements at admission and had a similar clinical management and breastfeeding behavior. The analysis included only the subjects who were fully nursing and amenorrheic at day 75. Approximately 60% ofthe women of both groups remained fully nursing and in amenorrhea at 6 months. During the period of lactational amenorrhea, the risk of pregnancy was extremely low in comparison with the risk of ovulation, particularly during the first 6 postpartum months (Table 4). In the cycle that followed the first postpartum menses, ovulation was detected in 93 % of the women, which contrasts with the 7% PR observed in the 1st month after the end of amenorrhea in the comparative group of unprotected nursing women. DISCUSSION In this study, the probability of ovulating during breastfeeding was nearly 37% before the 6th month and nearly 100% before the end of the year. In 67% of the women, ovulation occurred before the first menses, and 93 % of the cases had an ovulatory cycle after the first bleeding. The risk of ovulating was high even for fully nursing women, 36% of whom had ovulated in the first 6 months. It should be noted that all women were fully nursing and amenorrheic at day 75 postpartum. Therefore, the risks described here cannot be applied to the general population who experience an even higher probability of bleeding (3) and presumably of ovulating during breastfeeding. The first ovulatory cycle was clearly abnormal in comparison with the control cycles. It showed a prolonged follicular phase, a short luteal phase, and low estrogen and P levels during the luteal phase. This was observed regardless if ovulation occurred before or after the first menses or during exclusive or supplemented breastfeeding. The second cycle also exhibited a prolonged follicular phase, but the luteal phase approached a normal profile with a significantly longer duration and higher E2 and P levels in comparison with the first luteal phase. These differences between the first and second cycle occurred in the presence of similar PRL levels and only minor differences in the nursing frequency during day hours. The second luteal phase showed only minor differences in comparison with the control cycles, Table 4 Comparative Risk of Ovulation and Pregnancy During Lactational Amenorrhea First ovulation Postpartum length N* cpt mo * Number of women in amenorrhea. t Cumulative probability X 100. All women fully nursing at day 75 postpartum. N Pregnancy CP Diaz et a1. Ovarian function and lactational infertility Fertility and Sterility

6 suggesting that the sensitivity of the hypothalamicpituitary-ovarian axis to the suckling stimulus decreases once the hormonal events of the first cycle have occurred. The risk of ovulating in amenorrhea was much higher than the corresponding risk of pregnancy at any given time during the 1st postpartum year (Table 4). The ratio for the risks ofpregnancyjovulation observed in amenorrheic women increased from 1 to 28 at 6 months to 1 to 5 at 12 months. Approximately one fourth of non-nursing control women of similar characteristics become pregnant during the first exposure cycle (12). Therefore, anovulation does not account for all the contraceptive efficacy of lactational amenorrhea. The second luteal phase was normal in a high proportion of cycles, and this probably explains the prompt recovery of fertility in lactating women after the first postpartum bleeding (12). Nevertheless, breastfeeding still retained some effect on the second luteal phase, and this may explain why the PR observed after the first postpartum cycle was lower than that observed in comparable cycles of exposure in control women (12). For a short interval at the end of amenorrhea, breastfeeding prevented pregnancy in ovulatory cycles. Interference with implantation associated with luteal phase defects seems the most plausible explanation, considering the characteristics of the first luteal phase, the small inhibitory influence of breastfeeding on sperm penetration (15), and the coital frequency reported by the women of this study during the postpartum period (11). These results confirm that lactational amenorrhea is associated with a strong inhibition of fertility during the 1st postpartum months (4). Nursing women who ovulate before the end of amenorrhea are protected by the abnormal endocrine profile associated with the first ovulation (7). In contrast, the endocrine pattern of the second cycle does not warrant effective protection against pregnancy. Accordingly, lactating women who want to postpone a new pregnancy should initiate contraceptive measures no later than the first postpartum menses. Acknowledgments. The authors are grateful to the volunteers who participated in the studies, to Mrs. Elizabeth Nunez and Ms. Griselda Bravo for their commitment in doing the RIA and to Mrs. Emma Munoz for secretarial assistance. REFERENCES 1. Van Ginneken JK. The chance of conception during lactation. J Biosoc Sci SuppI1977;4: McCann MF, Liskin LS, Piotrow PT, Rinehart W, Fox G. Breastfeeding, fertility, and family planning. Popul Rep [J) 1984; Diaz S, Rodriguez G, Peralta 0, Miranda P, Casado ME, Salvatierra AM, et al. Lactational amenorrhea and the recovery of ovulation and fertility in fully nursing chilean women. Contraception 1989;38: Kennedy KI, Rivera R, McNeilly AS. Consensus statement on the use of breastfeeding as a family planning method. Contraception 1989;39: Perez A. Lactational amenorrhea and natural family planning. In: Hafez ESE, editor. Human ovulation. New York: Elsevier/ North-Holland Biomedical Press, 1979: Howie PW, McNeilly AS, Houston MJ, Cook A, Boyle H. Fertility after childbirth: post-partum ovulation and menstruation in bottle and breast feeding mothers. Clin Endocrinol (Oxf) 1982;17: McNeilly AS, Howie PW, Houston MJ, Cook A, Boyle H. Fertility after childbirth: adequacy of post-partum luteal phases. Clin Endocrinol (Oxf) 1982;17: Rivera R, Kennedy KI, Ortiz E, Barrera M, Bhiwandiwala PP. Breast-feeding and the return to ovulation in Durango, Mexico. Fertil SteriI1988;49: Shaaban MM, Kennedy KI, Sayed GH, Ghaneimah SA, Abdel-Aleem AM. The recovery of fertility during breast-feeding in Assiut, Egypt. J Biosoc Sci 1990;22: Howie PW, McNeilly AS, Houston MJ, Cook A, Boyle H. Effect of supplementary food on suckling patterns and ovarian activity during lactation. Br Med J 1981;283: Diaz S, Peralta 0, Juez G, Salvatierra AM, Casado ME, Durfm E, et al. Fertility regulation in nursing women. I. The probability of conception in full nursing women living in an urban setting. J Biosoc Sci 1982;14: Diaz S, Aravena R, Cardenas H, Casado ME, Miranda P, Schiappacasse V, et al. Contraceptive efficacy of lactational amenorrhea in urban chilean women. Contraception 1991;43: Nelson WE. Textbook of pediatrics. 8th ed. Philadelphia: Saunders Co., 1964: Croxatto HB, Ortiz ME, Diaz S, Hess R, Balmaceda JP, Croxatto H-D. Studies on the duration of egg transport by the human oviduct. II. Ovum location at various intervals following LH peak. Am J Obstet GynecoI1981;132: Vigil P, Perez A, Neira J, Morales P. Post-partum cervical mucus: biological and rheological properties. Hum Reprod 1991;6: Diaz et al. Ovarian function and lactational infertility 503

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