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Postpartum Consequences of an Overlap of Breastfeeding and : Reduced Intake and Growth During Early Infancy

Grace S. Marquis, PhD*; Mary E. Penny, MBChB, MRCP‡; Judith M. Diaz, BS‡; and R. Margot Marı´n, BS‡

ABSTRACT. Objective. Despite cultural pressure to cultural taboos against continuing to breastfeed.1,2 wean when a new pregnancy occurs, some women choose The practice of continuing to breastfeed during preg- to continue breastfeeding. We determined the effect of an nancy has been reported among US women but overlap of and late pregnancy on breastfeeding might not be discussed with health professionals and growth in early infancy. because of anticipated criticism of the practice.3–5 Methods. We studied 133 Peruvian pregnant women Breastfeeding during pregnancy is more common in who were >18 years of age, had a child <4 years old, and who then had a vaginal birth with a healthy, normal some low-income countries than in the weight . Of the 133 women, 68 breastfed during the because shorter birth intervals increase the likeli- last trimester of pregnancy (BFP), and 65 had not breast- hood of a pregnancy-lactation overlap. fed during pregnancy (NBFP). On day 2 and at 1-month It has been suggested that an overlap could pro- postpartum, 24-hour intake of and other liq- duce suboptimal outcomes for both pregnancy and uids was measured. Twice weekly home surveillance subsequent lactation.6–8 research has demon- documented infant morbidity and dietary intakes. An- strated that a complete overlap of lactation during thropometry was taken at birth and at 1 month. Maternal pregnancy dramatically compromises the total pro- anthropometric, health, and socioeconomic status data duction of mature milk during the next lactation were collected pre- and postpartum. period.9–14 A dry (nonmilking) period of approxi- Results. Pregnant BFP breastfed 5.3 ؎ 4.3 times/day. BFP and NBFP did not differ in breast- mately 2 months before calving is usual in the dairy feeding behavior or in intake on day 2. BFP industry. This is the first human study to provide infants breastfed longer per feed and per 24 hours (35.2 data on the association between the practice of lac- minutes/24 hours) than did NBFP infants; however, tating through late pregnancy and breastfeeding and 1-month intakes per feed tended to be lower among the growth outcomes of young infants. BFP infants. After controlling for confounders, BFP in- fants gained 125 g less than did NBFP infants (about 15% of mean weight gain). A sustained decline would result METHODS in a ؊0.7 z score change in weight-for-age by 6 months. Participants Conclusions. A lactation-pregnancy overlap had a The study was conducted in a poor periurban community of negative effect on early infant outcomes. Additional approximately 800 000 on the outskirts of Lima, Peru. The inclu- studies are needed to determine whether the effect con- sion criteria for mothers were: 1) pregnant; 2) Ն18 years of age; 3) tinues past 1 month of age. 2002;109(4). URL: multiparous and living with her child Ͻ4 years old; 4) without http://www.pediatrics.org/cgi/content/full/109/4/e56; apparent indicators for elective cesarean section; and 5) either breastfeeding, pregnancy, overlap, breast milk volume, continuing to breastfeed into the third trimester or never breastfed weight gain, infant feeding, Peru. during this pregnancy. Routes to identify possible participants were community census, local prenatal health service registers, and referrals. Between July 1998 and January 2000, 3417 pregnant ABBREVIATIONS. BFP, breastfed during pregnancy; NBFP, did women were identified. Of these, 601 women were not located at not breastfeed during pregnancy; BMI, body mass index; SES, home, and 27 women declined to participate in a screening inter- socioeconomic status; CI, confidence interval; OR, odds ratio. view. Field workers screened 2789 pregnant women, and 727 met all of the inclusion criteria: 170 women breastfed their older chil- dren during the third trimester of pregnancy (BFP) and 557 any women throughout the world breast- women had not breastfed at all during the present pregnancy (NBFP). Breastfeeding was confirmed by direct observation; date feed for as long as possible to give their of was obtained from those mothers who had weaned Mchildren the nutritional, immunologic, and during the third trimester and before enrollment. emotional benefits of breastfeeding. When lactation Postpartum follow-up was confined to women who gave birth overlaps a new pregnancy, some women choose not to an infant who was a vaginal delivery, full-term (Ͼ37 weeks’ ), healthy (Ͼ2500 g), and with no birth to wean their toddlers, although there may be strong defects or complications that would hinder breastfeeding. Of the 170 enrolled BFP women, 70 -infant pairs were followed after birth. Reasons for no postpartum follow-up included refusal From the *Department of Food Science and , Iowa State (N ϭ 40), moved or worked (N ϭ 12), mother not available within University, Ames, Iowa; and ‡Instituto de Investigacio´n Nutricional, Lima, 48 hours of birth (N ϭ 13), birth problems (N ϭ 19), and other (eg, Peru. twins, older child with problems; N ϭ 16). Received for publication Jun 11, 2000; accepted Nov 28, 2000. Of the 557 NBFP women enrolled during pregnancy, 67 were Address correspondence to Grace S. Marquis, PhD, 1127 Human Nutri- followed up. Probable data of delivery was recorded for all NBFP tional Sciences Building, Department of Food Science and Human Nutri- mothers. For each BFP infant born, a NBFP was selected at tion, Iowa State University, Ames, IA 50011. E-mail: [email protected] random from the pool of women scheduled to give birth that PEDIATRICS (ISSN 0031 4005). Copyright © 2002 by the American Acad- month. The first selected NBFP woman who met the postpartum emy of Pediatrics. criteria was included. The reasons for no follow-up were refusal http://www.pediatrics.org/cgi/content/full/109/4/Downloaded from www.aappublications.org/newse56 by guestPEDIATRICS on September Vol. 29, 2021 109 No. 4 April 2002 1of8 (N ϭ 174), moved or worked (N ϭ 40), not randomly selected (N ϭ Morbidity N ϭ 71), not available within 48 hours of birth ( 99), birth problems Maternal reports of daily symptoms of infants and any treat- N ϭ N ϭ ( 54), and other ( 52). Of the 137 infants who were studied ment were recorded twice weekly for the first month. Stool char- on day 2 postpartum, 133 infants had a repeated study at 1 month acter and frequency as well as general and respiratory symptoms of age. Two BFP and 2 NBFP infants had no repeat study because were recorded along with maternal illness and treatment. A diar- N ϭ N ϭ of refusal ( 2) and moving ( 2). This analysis is based on rheal day was a day with 3 or more liquid/semiliquid stools in 24 the 133 infants with observations for both days. hours. A dichotomous variable of ever having was de- veloped. Prevalence of diarrhea and cough in the infant and any Comparison of Included and Excluded maternal illness was calculated. Other symptoms were infrequent The included BFP families had some indicators of a better (Ͻ6% of days observed) and, therefore, not considered here. economic status (eg, housing quality) than the excluded BFP fam- ilies. The included NBFP mothers were significantly more likely to be younger, born in the mountains, and live with fewer adults as Socioeconomic Data compared with excluded NBFP families. Other demo- Socioeconomic data on the quality of housing, hygiene, posses- graphic, socioeconomic, and obstetric data that were collected sions owned, and education and employment of family members during pregnancy did not differ. were collected at the screening interview and day 2 postpartum.

Data Collection Data Analysis Obstetric History and Birth Mean group differences for continuous variables were tested At screening, all pregnant women were interviewed about their with the Student t test and analysis of variance; Kruskal-Wallis obstetric history and previous breastfeeding experience. Morbid- 1-way analysis of variance was used for variables with nonnormal ity data were gathered twice monthly for all enrolled women. distribution. Frequency differences were tested with the ␹2 good- Relevant delivery and birth information was collected from clini- ness-of-fit test. Multiple linear regression models were used to cal records when available and from mothers. For deliveries at estimate the effect of breastfeeding late in pregnancy on day 2 and health facilities, dystocia (abnormal duration of labor) was defined 1-month breast milk intake and 1-month growth. Logistic regres- by practitioners, using the World Health Organization’s parto- sion was used to estimate the effect of an overlap on the risk of graph to monitor cervical dilatation and fetal descent.15 All home very low (Ͻ25th percentile) milk intake and growth. Both models births were assumed to have involved normal labor. controlled for confounding factors including sex, age, first weight, feeding behaviors (duration and frequency of feeds, breastfed by Breastfeeding Behavior another woman, hours postpartum), and maternal characteristics (age, parity, pregnancy complication, anthropometric measure- Once a month during pregnancy, BFP mothers recorded their ments). With birth weight or length in an equation predicting toddlers’ feeding frequency or the date of weaning. After birth at 1-month weight or length, the other coefficients reflected their twice-weekly home visits, mothers recalled their breastfeeding effects on the corresponding increment from birth. Morbidity (eg, practices of the previous days, including whether the infant was prevalence of diarrhea and cough) and socioeconomic status (SES) breastfed by another woman and whether the mother breastfed variables were not significant predictors of the milk and growth another child. outcomes. The effects of BFP on milk intake and growth outcomes Twenty-four-hour breast milk intakes and duration of feeds of in the models discussed here were unchanged when analyses Ϯ all infants were measured twice: day 2 (41.7 5.7 hour) and 1 were rerun without 10 children who received breast milk from Ϯ month (33 3 days). Milk intake was measured by the test other mothers. 16 weighing method, weighing the infant before and after each All analyses were conducted with SYSTAT version 10.19 Data feed, using an electronic digital balance sensitive to 1 g (Mettler are presented as the mean Ϯ standard deviation and significance Toledo Model SB/16 000, Columbus, OH). Total milk intake was for all 2-tailed probability tests was set at P Ͻ .05, unless otherwise 17 corrected for a 3% insensible loss. On both days, only 0.1% indicated. This study was approved by the Human Subjects Re- of feeds were not weighed because the mother was not at home at search Office at Iowa State University, University of Alabama at the time of the feed. The missed values were imputed using Birmingham, and the Ethics Committee at the Instituto de Inves- separate multiple regression equations that estimated intake per tigacio´n Nutricional; written informed consent was obtained. feed by time since last feed, duration of the missed feed, and child identifier. Milk intake was expressed as g/feeding and g/24 hours. RESULTS Family Baseline Characteristics Intake of Other Liquids/Foods NBFP families appeared poorer than BFP house- Nonbreast milk liquids that were consumed during the 24-hour observation period were weighed. Information on reported intake holds (Table 1). NBFP houses were made of lower for all other days was collected at twice-weekly visits. quality materials and were less likely to have piped water and a functioning sewage system. Field work- Anthropometry ers observed human fecal matter on the floor in 3 Birth weights and lengths were collected from health facilities times more NBFP than BFP homes; however, this did when available. A similar number of BFP and NBFP mothers gave not reach significance. birth at home, and their infants were weighed and measured by the study staff within 3 days. For clarity, both of these measure- ments are referred to as the first weight or length. At 1 month of Maternal and Infant Characteristics age, infants were measured in triplicate without clothes in the field office. Weight was measured on a digital electronic infant Baseline scale (Soehnle-Waagen GMbH and Co, KG, Murrhardt, Germany) BFP and NBFP mothers were similar in age and sensitive to 10 g. Length was measured to the nearest 0.1 cm with education (Table 2). Only 2 women (1 BFP and 1 a locally made rigid length board. Head circumference was mea- NBFP) worked in the formal sector. Compared with sured to 1 mm with nonstretchable tape measures (Lasso, Child Growth Foundation, London, ). NBFP mothers, twice as many BFP mothers were Maternal mid-arm and calf circumferences were measured pre- born on the coast and lived about 3 years longer in and postnatally to a precision of 1 mm with the same nonstretch- Lima. Although there were no differences between able tape measurer mentioned above. Weight and height were groups in parity, the last interbirth interval was measured at 1-month postnatally, using a Seca adult beam balance with a precision of 100 g and a locally-made stadiometer with a longer for NBFP mothers than BFP mothers, as dem- precision of a 0.1 cm. Body mass index (BMI) (weight/height2) onstrated by the 10-month difference in the age of the was calculated. Field workers were standardized.18 last child.

2of8 BREASTFEEDINGDownloaded WHILE PREGNANTfrom www.aappublications.org/news AFFECTS GROWTH by guest on September 29, 2021 TABLE 1. Baseline Family Socioeconomic and Demographic tions, or smoking during pregnancy (2 BFP and 2 Characteristics by Practice of Breastfeeding During Pregnancy Ϯ ϭ NBFP). BFP mothers breastfed their toddlers 5.3 (n 133) 4.3 (median: 4) times per day. Fourteen mothers Breastfeeding Practice breastfed Ͼ5 times during the daytime; the maxi- BFP NBFP mum frequency reported was 17 feeds/day. (n ϭ 68) (n ϭ 65) Of those who gave birth in a health facility, abnor- N (%) N (%) mally prolonged labor (dystocia) tended to occur House characteristics and indicators more often among the BFP than the NBFP mothers of wealth (Table 3). Other birth and newborn characteristics Cement floor** 41 (60.3) 27 (41.5) were not different between groups. Brick/cement wall* 43 (63.2) 31 (47.7) There were no differences in postpartum anthro- Electricity 58 (85.3) 55 (84.6) Ϯ Ϯ pometry or prevalence of maternal illness in the first Daily food expenditures (S/.)† 13.3 5.3‡ 12.8 4.5‡ Ͻ Home environmental health month postpartum. Mothers reported being ill 10% Piped water*** 50 (73.5) 32 (49.2) of the first 30 days postpartum. Sewage**** 43 (63.2) 16 (24.6) Human fecal material visible on 2 (2.9) 7 (10.8) floor Breastfeeding Characteristics Family member smokes*** 33 (48.5) 15 (23.1) Breast Milk Intake Family member smokes in house 18 (26.5) 8 (12.3) Family composition There was a wide range of 24-hour intake of co- Number of members in home 5.4 Ϯ 2.7‡ 5.0 Ϯ 2.2‡ lostrum (2g–570 g; Fig 1). When intake was adjusted Extended family 27 (39.7) 20 (30.8) for time after birth of initiation of study, the higher Paternal intake of BFP infants than NBFP infants (195.3 Ϯ Lived with family** 59 (86.8) 64 (98.5) Ϯ ϭ Completed primary school 57 (83.8) 60 (92.3) 110.7 vs 175.1 110.7 g/24 hour, P .13; respec- Had a stable income 20 (29.4) 28 (43.1) tively) did not reach significance. There were also no group differences in frequency or total duration of Significant difference by breastfeeding practice: * P Ͻ .10; ** P Ͻ .05; *** P Ͻ .01; **** P Ͻ .001. breastfeeding over the 24 hours. Mothers breastfed a † Peruvian currency (S/. ϭ Nuevos Soles). mean of 20.7 Ϯ 5.1 times for a total of 305.8 Ϯ 116.9 ‡ Mean Ϯ standard deviation. minutes. At 1 month of age, the number of feeds per 24 TABLE 2. Baseline, Prenatal, and Postpartum Maternal Char- hours decreased to 16.9 Ϯ 3.4. In contrast with the acteristics by Practice of Breastfeeding During Pregnancy (n ϭ observation shortly after birth, BFP mothers breast- 133) fed for 35.2 minutes (95% confidence interval [CI]: Breastfeeding Practice 11.5–58.9 minutes) longer than NBFP mothers, for a mean total time of 213.8 Ϯ 80.0 versus 178.6 Ϯ 56.4 BFP NBFP Ͻ (n ϭ 68) (n ϭ 65) minutes (P .01), respectively. The average duration of a feed was significantly longer among the BFP Baseline than the NBFP mothers (12.4 Ϯ 3.9 vs 10.9 Ϯ 2.9 Age (y) 25.9 Ϯ 5.5† 25.9 Ϯ 4.7 ϭ Born on the coast** 37 (54.4)‡ 16 (24.6) minutes, respectively; P .01). This increased time Lived in Lima (y)* 16.6 Ϯ 8.8 13.9 Ϯ 8.3 did not translate into higher milk intakes (Figs 1 and Completed primary school 60 (88.2) 54 (83.1) 2). BFP as compared with NBFP infants had about a Number of live births 2.1 Ϯ 1.3 2.1 Ϯ 1.1 Ϯ Ϯ 9% decline in intake per feed that tended to be sig- (Age of last child (y)** 1.9 0.6 2.7 0.7 nificant (46.2 ؎ 14.6 vs 50.4 ؎ 11.2 g/feed; P ϭ .06 Prenatal§ Ϯ Attended prenatal care at least 51 (75.0) 52 (80.0) and about an 8% lower total milk intake (765.5 once 212.3 vs 810.5 Ϯ 161.9 g/24 hour; P ϭ .17). Mid-arm circumference (mm) 26.9 Ϯ 3.1 26.5 Ϯ 2.9 Calf circumference (mm) 33.6 Ϯ 2.3 33.5 Ϯ 2.6 Postpartum (1 mo)§ Breast Milk From Other Mothers Height (cm) 149.1 Ϯ 5.2 150.0 Ϯ 7.1 Ten infants were observed also to be breastfed by Mid-arm circumference (mm) 27.3 Ϯ 3.1 26.9 Ϯ 2.6 another woman, 6 on day 2 (4 BFP and 2 NBFP) and Calf circumference (mm) 33.0 Ϯ 2.5 32.6 Ϯ 2.8 BMI 26.2 Ϯ 3.8 25.9 Ϯ 3.6 4 (all BFP) at 1 month. The odds ratio (OR) of a BFP infant receiving milk from another mother at either Ͻ Ͻ * P .10; ** P .001. observation point was 4.2 (P ϭ .06). During both † Data in this format indicate mean Ϯ standard deviation. ‡ Data in this format indicate n [%]. observation days, the range of milk consumed from § Sample for anthropometric measurements was at least n ϭ 64 other mothers was wide:1gto105g(median: 30.4 g) BFP and 64 NBFP. on day 2 and 14 g to 209.1 g (median: 54.6 g) at 1 month. When intakes of breast milk from the infant’s mother and other women were summed, the differ- Prenatal, Birth, and Postpartum Characteristics ence in milk intake at 1 month between BFP and About three fourths of all women attended a NBFP infants was attenuated slightly (770.4 Ϯ 208.4 health facility for prenatal care (Table 2). NBFP vs 810.5 Ϯ 161.9 g/24 hour; P ϭ .22). The results mothers were more likely than BFP mothers to seek (regression coefficients and significance levels for prenatal care at the governmental health centers breastfeeding during pregnancy) for breast milk in- rather than private facilities (75.8% vs 55.9%). There take and growth discussed below were similar with were no group differences in prepartum anthropo- and without the data from these 10 children who metric measurements, reported pregnancy complica- received milk from another woman.

Downloaded from www.aappublications.org/newshttp://www.pediatrics.org/cgi/content/full/109/4/ by guest on September 29, 2021 e56 3of8 TABLE 3. Birth Events and Newborn Characteristics by Practice of Breastfeeding During Preg- nancy Breastfeeding Practice BFP (n ϭ 68) NBFP (n ϭ 65) Birth event Born in health facility 54 (79.4)* 50 (76.9) Prolonged labor (dystocia)†‡ 7 (13.0) 2 (4.0) Mother received medicine during labor 18 (26.5) 15 (23.1) Mother received medicine after birth 51 (75.0) 53 (81.5) Newborn characteristics Female sex 33 (48.5) 32 (49.2) First weight (kg)§ 3.4 Ϯ 0.4࿣ 3.4 Ϯ 0.4 First length (cm)§ 50.0 Ϯ 1.7 50.0 Ϯ 1.6 Gestational age (wk)§ 39.6 Ϯ 1.0 39.6 Ϯ 1.1 Time after birth started breastfeeding (h) 1.7 Ϯ 2.6 2.4 Ϯ 6.0 Did not receive liquids in first 24 h 61 (89.7) 61 (93.8) * Data in this format indicate n (%). † P Ͻ .10. ‡ Extracted from clinic records; reflects inadequate progress of cervical dilation and fetal descent, as defined by the World Health Organization’s partogram.15 All births at home were assumed to be normal. § Samples for anthropometric and gestational age measurements were at least n ϭ 59 BFP and 60 NBFP. ࿣ Data in this format indicate mean Ϯ standard deviation.

Fig 2. Infants’ mean intake per feed of their mothers’ breast milk at 1 month by presence of a breastfeeding-pregnancy overlap. Fig 1. Infants’ 24-hour intake of their mothers’ breast milk by Upper and lower limits of the box represent the 25th and 75th presence of a breastfeeding-pregnancy overlap and day of obser- percentile values; the horizontal line within the box represents the vation. Upper and lower limits of the box represent the 25th and median. Bars represent the standard deviation. 75th percentile values; the horizontal line within the box repre- sents the median. Bars represent the standard deviation. Use of Other Liquids Exclusive breastfeeding was short-lived in this community. Ten percent (10.3%) of the BFP infants Tandem Breastfeeding and 6.2% of the NBFP infants received nonbreast About one third of the BFP mothers breastfed an- milk liquids during the first 24 hours of life, includ- other child in addition to the newborn on day 2 (N ϭ ing sugar water, other , and teas. By 1 month, 24; 35.3%) and at 1 month (N ϭ 27; 39.7%) postpar- 31.6% of all infants had been given other liquids (32% tum. On day 2, only 1 NBFP mother breastfed an- of liquids were teas or water; 68% were other milks), other infant (total ϭ 10.3 g). Milk intakes of the other with no group difference in use. However, the BFP as child ranged from 0 to 384.2 g on day 2 and 0 to 405.8 compared with the NBFP infants had a higher total g at 1 month. When milk intake of the other child number of days when other liquids were offered Ϯ Ϯ Ͻ was considered as part of total milk production, the (9.4 7.5 days vs 4.4 3.0 days; P .001) and higher Ϯ difference between BFP and NBFP mothers was re- total 30-day intake of teas and water (3.5 9.4 vs Ϯ duced. The mean 1-month intakes of infants in- 0.7 2.0 fl oz). creased progressively from BFP/no tandem breast- feeding (762.5 Ϯ 232.4 g/24 hour), BFP/tandem One-Month Infant Characteristics breastfeeding (768.6 Ϯ 192.3 g/24 hour), to NBFP Morbidity (813.0 Ϯ 161.8 g/24 hour), demonstrating that tan- There was little diarrheal morbidity during the dem feeding did not account for the low milk intakes first 30 days of life; 25 mothers reported that their of BFP infants. infants had at least 1 day of diarrhea (about 20% in

4of8 BREASTFEEDINGDownloaded WHILE PREGNANTfrom www.aappublications.org/news AFFECTS GROWTH by guest on September 29, 2021 both groups). Significantly more BFP than NBFP in- duration. The first weight, an indicator of child re- fants had a cough for Ͼ7 days (35.3% vs 20.0%). quirements, was the primary determinant of milk intake; a 1-kilo increase was associated with a 152-g Growth Outcomes increase in intake. Finally, maternal report of com- Complete weight data were available for 66 BFP plications during pregnancy was positively associ- and 64 NBFP infants; length data were available for ated with milk intake; the explanation of this rela- 63 BFP and 57 NBFP infants. The infants had similar tionship is not clear. Tandem breastfeeding, first weights. BFP infants gained 170 g less (95% CI: receiving milk from another mother, and intake of Ϫ0.308 to Ϫ0.031) than NBFP infants over the first nonbreast milk liquids did not explain any addi- month of life (Fig 3), a 14% difference in weight gain. tional variance. By 1 month of age, there was a nonsignificant mean The risk of a very low breast milk intake (Ͻ25th difference of Ϫ118 g (95% CI: Ϫ313 to Ϫ77) in at- percentile of the study population) at 1 month was tained weight of BFP as compared with NBFP in- fivefold higher among those infants who were fants. There was no group difference in length gain breastfed also by another women (OR: 5.3; P ϭ .01). (BFP gained 4.6 Ϯ 1.4 and NBFP gained 4.7 Ϯ 1.5 These data do not indicate if this practice negatively cm), attained length, or head circumference at 1 affected maternal production or was in response to a month. previous low production.

Models to Estimate Breast Milk Intakes From Infant’s Models to Explain 1-Month Infant Weight Gain Mother After controlling for other factors, the practice of Day 2 breastfeeding throughout pregnancy was associated Day 2 breast milk intakes were associated with with a decrease in 1-month weight gain (Table 5). several factors (Table 4). Milk intake decreased about Holding the continuous explanatory variables at 25 g for each 5-year increment of maternal age and their mean, a BFP infant gained 125 g less (95% CI: 3 g per 10 additional minutes of breastfeeding. Intake 8–241) than NBFP infants, or about 15% of National 20 increased 6.5 g per 100-g increase in the first weight. Center for Health Statistics mean weight gain. A Receiving breast milk from another woman was sustained decline of this magnitude would result in a Ϫ strongly associated with a lower intake (Ϫ96 g) from 0.7 z score change in weight-for-age by 6 months of the infant’s own mother. BFP was not associated life. with day 2 intake when controlling for these above The negative effect of BFP on weight gain was factors and time of initiation of the study. amplified by an increase in maternal calf circumfer- ence (an additional Ϫ53 g/mm increase in calf cir- One Month cumference among only BFP infants). For example, Parity significantly modified the effect of a breast- for a mother with a calf circumference equivalent to feeding-pregnancy overlap on 1-month milk intake the 75th percentile (34.4 mm), the weight gain in a (Table 4). Holding the other explanatory variables BFP infant was 175 g less than that of an equivalent constant, for each increase of 1 birth, there was an NBFP infant, almost 20% of National Center for additional 116-g reduction in milk intake among BFP Health Statistics mean weight gain. Maternal calf infants but only a 17-g reduction among NBFP in- circumference had a significant positive correlation ϭ fants (interaction term; P ϭ .01). with maternal age and BMI at 1 month (r 0.25 and Milk intake was positively associated with the 0.75, respectively) and may be functioning as a proxy number of feeds but was negatively associated with of nutritional stress, age, or other related biological factors. Intake of bovine milk had a negative effect on weight gain. Lower weight gain was also associated with being female, higher parity, and younger infant age. Controlling for infant’s age, the risk of a very low weight gain (Ͻ25th percentile value of the study population; Ͻ0.9 kg) tended to double for BFP in- fants (OR ϭ 2.193; P ϭ .077) and was threefold higher for females (OR ϭ 2.8; P ϭ .03). Other feeding prac- tices, such as tandem feeding, breastfeeding from another woman, or use of nonbreast milk liquids, did not affect the total weight gain or the risk of a very low weight gain.

Models to Explain 1-Month Infant Length Gain Similar models were developed for length gain (Table 5). Length gain was positively associated with Fig 3. One-month weight (solid) and length (hatched) gain of infant’s age and tended to increase with increased study infants by presence of a breastfeeding-pregnancy overlap. Upper and lower limits of the box represent the 25th and 75th breast milk intake on day 2. BFP as well as other percentile values; the horizontal line within the box represents the breastfeeding practices did not explain any addi- median. Bars represent the standard deviation. tional variance in length gain.

Downloaded from www.aappublications.org/newshttp://www.pediatrics.org/cgi/content/full/109/4/ by guest on September 29, 2021 e56 5of8 TABLE 4. Multiple Linear Regression Models for 24-Hour Breast Milk Intake on Day 2 and at 1-Month Postpartum* Day 2 (Adjusted R ϭ 0.339) 1 Month (Adjusted R ϭ 0.366) Variable Coefficient SE P Value Variable Coefficient SE P Value Constant Ϫ98.681 99.855 .325 Constant 183.796 126.886 .150 First weight (kg) 64.986 21.927 .004 First weight (kg) 152.094 33.624 .000 BF duration (min) Ϫ0.341 0.085 .000 BF duration (min) Ϫ0.770 0.236 .001 Initiate study (h) 168.958 35.359 .000 Parity (number)† Ϫ17.116 17.792 .338 BF other mother on day 2 Ϫ95.881 41.193 .022 Pregnancy complication 55.092 27.280 .046 Mother’s age (y) Ϫ4.971 1.719 .005 Breastfeeds (number) 14.039 4.904 .005 BFP (1 ϭ yes) Ϫ40.714 27.665 .144 Parity BFP† Ϫ57.778 22.805 .013 BF indicates breastfeeding; SE, standard error. * n ϭ 132; data for 1 birth weight was missing. Intake was adjusted for 3% insensible water loss. † Variable was centered for analysis.

TABLE 5. Multiple Linear Regression Models for 1-Month Weight (kg) and Length (cm) Gain Weight (n ϭ 128; Adjusted R ϭ 0.995) Length (n ϭ 120; Adjusted R ϭ 0.999) Variable b SE P Value Variable b SE P Value First weight (kg) 1.000 0.052 .000 First length (cm) 0.993 0.022 .000 Infant’s age (d) 0.048 0.006 .000 Infant’s age (d) 0.137 0.033 .000 30-d total bovine milk (fl oz) Ϫ0.001 0.000 .002 Day 2 intake (g) 0.002 0.001 .052 BFP (1 ϭ yes) Ϫ0.125 0.059 .036 30-d total bovine milk (fl oz) Ϫ0.003 0.001 .086 Maternal calf circumference (mm)* 0.005 0.017 .783 Maternal calf circumference (mm)* 0.114 0.054 .038 Sex (1 ϭ female) Ϫ0.174 0.058 .003 Parity (number) Ϫ0.069 0.026 .009 BFP calf circumference* Ϫ0.058 0.023 .013 SE indicates standard error. * Variable was centered for analysis.

No variables were significant explanatory factors the range of overweight) do not support this mech- for the risk of very low (Ͻ25th percentile value of the anism. In addition, there were no group differences study population; Ͻ3.55 cm) length gain. in maternal anthropometric indicators pre- or post- natally. It is possible that BFP is a proxy for other DISCUSSION maternal psychosocial factors, not measured, that Lactation during pregnancy is known to have ad- influenced successful mothering and, ultimately, verse effects on milk production in cows.9–14 The growth. present study is the first human study to document a Butcher (cited in reference 11) estimated a reduc- negative effect of an overlap of lactation and late tion of 585 kg of milk over the course of the lactation pregnancy on the breastfeeding and growth success in cows that were milked up to 5 to 20 days before of the subsequent infant. The magnitude of the effect parturition. The mechanism of reduction of milk pro- on weight gain is cause for concern. A sustained 15% duction in cows is not well understood; possibly, decline in expected weight gain would move an in- with an inadequate nonmilking period before birth- fant born at the 50th percentile to under the 25th ing, there is insufficient and subsequent percentile weight-for-age by 6 months of age. rejuvenation of the mammary secretory cells. Species The primary limitation of the study is group self- vary in the amount of involution that naturally oc- selection. That is, mothers chose whether they were curs; those with longer cycles and a functional luteal BFP or NBFP; they were not randomly assigned to a phase normally retain some of the alveolar struc- feeding group. Without the benefit of randomization, ture.11,14 The importance of this mechanism in hu- it is possible that other confounding factors explain mans is not well understood. our results. For example, if SES were a confounder Healthy infants self-regulate intake to meet their and the true determinant of poor growth among the needs.25 Generally, a reduced milk intake in BFP BFP children, then one would expect the BFP fami- infants could have 3 causes: 1) maternal behaviors lies to be poorer than the NBFP families. However, a that reduce infant access to milk, 2) limited maternal number of indicators suggested that the SES was production, and/or 3) reduced infant demand. The lower in the NBFP families. It is not clear how the similar feeding frequency and increased duration group differences in maternal characteristics, such as among BFP infants are inconsistent with the first place of birth, would affect breastfeeding success explanation. However, the data were collected at 1 unless they reflect breastfeeding support networks. time point and may not reflect feeding behaviors Shorter interbirth intervals among BFP mothers may over the entire month. Also, although access was reflect decreased recuperation of maternal stores.21,22 similar, BFP infants may have been less successful at Milk production may be reduced when maternal diet extracting milk or expending more energy doing so. is extremely limited23,24; however, observed social Studies on feeding mechanisms are needed. conditions and maternal BMI levels (mean value in Second, dairy research would suggest that the

6of8 BREASTFEEDINGDownloaded WHILE PREGNANTfrom www.aappublications.org/news AFFECTS GROWTH by guest on September 29, 2021 lower intakes were related to lower milk production. mothers adjust their feeding behavior and are able to However, when total milk production was calcu- exclusively breastfeed for 6 months with adequate lated, those BFP mothers who had additional stimu- growth, there is no reason to wean a toddler before a lation because of tandem breastfeeding were able to mother wishes to do so. With these additional re- produce an equal amount of milk as NBFP mothers, sults, health professionals will be able to provide suggesting that milk production was not a limitation. advice that will lead to optimal health for the infant, The selection bias for tandem breastfeeding is not toddler, and mother. known. Women who perceived inadequate milk pro- duction may have chosen not to tandem breastfeed. ACKNOWLEDGMENTS Finally, there are no data to assume a lower de- This work was funded by National Institutes of Health R03 mand for milk from the BFP infants. No infant was grant HD35183–03. We thank the field staff of the Instituto de Investigacio´n Nutri- low birth weight or premature, or had any condi- cional for their outstanding work; the staff at the Instituto Materno tions that would hinder breastfeeding. BFP infants Perinatal, the Hospital Materno-infantil, Huascar, and the Minis- had slightly higher rates of symptoms of upper re- try of Health facilities in San Juan de Lurigancho in the study spiratory tract infections. Difficulty in breathing as- community for facilitating access to mothers who gave birth in sociated with illness could hinder infants breastfeed- their units; and the Iowa State University Community Nutrition Research group for their critical review of the manuscript. ing; however, previous studies have demonstrated only a minor effect of respiratory illness (without REFERENCES fever) on breast milk intakes.26,27 Our regression 1. Oliveros C, Marquis GS, Ormsby G, Rudatsikira E. Maternal lactation: analysis failed to find any association with upper a qualitative analysis of the breastfeeding habits and beliefs of pregnant infections and milk intake; it is not women living in Lima, Peru. Int Q Community Health Educ. 1998–99;18: clear whether this was because our variable was an 415–434 insensitive marker of illness. 2. Dettwyler KA. Breastfeeding and weaning in Mali: cultural context and hard data. Soc Sci Med. 1987;24:633–644 BFP mothers may perceive feeding difficulties and 3. 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Downloaded from www.aappublications.org/news by guest on September 29, 2021 Postpartum Consequences of an Overlap of Breastfeeding and Pregnancy: Reduced Breast Milk Intake and Growth During Early Infancy Grace S. Marquis, Mary E. Penny, Judith M. Diaz and R. Margot Marín Pediatrics 2002;109;e56 DOI: 10.1542/peds.109.4.e56

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