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Bpeast-feeding educes maternal lowep-body fat IFMA
TI&W MMMWEI2PhD ALBERT J STUNK4RD, MD, KAT11LEENA. MARSE4LL, SHORTE MCKWVEY, Phl, RD, 14AE LIEBSCHUTZ
ABMIIICT: The effect of breast-feeding on maternal anthropometric measures during the first 6 postpartum months was studied in 24 women. Mothers, who were seen in the hospital shortly after delivery and at monthly intervals thereafter, kept a record of their infant-feeding practices and provided three 24-hour dietary recalls per month. The women were placed in one of three groups according to their infant-feeding practices: breast-feeding exclusively, combination of breast- and formula-feeding, and formulafeeding only. Changes in anthropometric variables at 6 months postpartum were similar in the three groups, but mothers who breast-fed exclusively or partially had significantly larger reductions in hip circumference measurements (3.6% and 3.1%, respectively) and were less above their prepregnancy weights at month postpartum (7.8%/ and 8.5% above prepregnancy weight, respectively) than mothers who fed formula exclusively (0.68% reduction in hip circumference and 13.7% above prepregnancy weight). Our findings indicate that a womarfs choice of infant-feeding practice influences postpartum anthropometric changes, but these effects may be temporary.JAm Diet Assoc. 1993, 93:429-433.
During
regnancy is frequently cited as a cause of long-term weight gain. Epiden-dological studies have shown a positive relationship between parity and weight gain adulthood (1-3), and women frequently report a net weight gain as a result of pregnancy (4-5). Data from several studies indicate a net weight gain of approximately 1 kg per birth, after adjustment for the effect of normal aging (6). Such results raise the question of what factors influence changes in body fat and weight after the birth of a child. Results of studies examining loss of body weight and fat after delivery are inconsistent (7). Studies that examined women who breast-fed exclusively typically found steady weight loss (7-12), whereas studies that compared the effect of different infant-feeding practices reported inconsistent results (3,13-21). Five studies (15,17,18,20,21) found no evidence that breast-feeding was associated with greater postpartum weight or fat loss than was formula-feeding, four (3,13,14,16) found that breast-feeding resulted in postpartum weight or fat loss, and one (19) found that breast-feeding led to postpartum weight gain. The inconsistency among results may be due largely to methodological differences among the studies, such as the type of study population, definition of breast-feeding, number and types of infant-feeding practices studied, maternal postpartum energy intake, anthropometric measures taken, and times of measurement. The present study was undertaken to clarify the effect of a woman's infant-feeding practice on postpartum anthropometrics and, particularly, on postpartum changes in lower-body fat. Pregnancy enhances fat deposition, especially in the lower body (22), but during lactation, lipids are preferentially diverted to the breast for milk production, and changes in hormonal and enzymatic conditions enhance mobilization of lower-body fat (23). We hypothesized that breast-feeding would be associated with greater weight loss and reduction in body fat, particularly in the lower body. F. Kramer(correspondingauthor) is a research psychologistat the USArmy Natick Researc/4 Development, and Engineering Center,Natick, MA 01 7605020 A. J Stunkard is a professor and K A. Marshalland J. Liebschutz are researchassistantsin the Department of Psychiatry at the University ofPennsylvania, Philadelphia,PA 19104. S. McKinney is an associate professorin the Departmentofl~utritionandFbod Sciences at Dreel University, PhiladelphiaPA 19104. JOURNAL OF THE AMERICAN DIETETIC ASSOCIATION / 429
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purpose of the study was to learn about changes in body weight and other body measurements after pregnancy The study was approved by the Committee on Studies Involving Human Beings of the University of Pennsylvania. All subjects signed informed consent forms.
FIG 1. Change in maternal body weight over 6 postpartummonths expressed as a percentage above self-reported prepregnancyweight adjustedfor pregnancyweight gain. Vertical bars are standard errors.At I month postpartum, women in both the breast-feeding and combined-feeding groups were significantly (P<.05) above their prepregnancyweight compared with women in theformula-feedinggroup.
Table Mean ± standard deviation body weight measures recorded before pregnancy through 6 months postpartum for 24 women grouped by infant-feeding practice, Time of measurement
Innfant-eeding practice Breast-feed (n=7)
Prepregnancy Delivery Postdelivery
,(~ 61.8 ± 7.3 78.9-8.7 72.3±8.8
1 Month postpartum 3 Months postpartum 6 Months postpartum
66.3±8.0 64.3 ± 7.3 63.0 ± 8.0
~
Combination (n = 12)
Formula (n=5)
Kg 58.0 + 7.4 73.5±9.0 67.5 -+9.3
61.0 + 6.8 81.0±+8.4 76.1 ±8.7
62.4- 8.6 61.2 ± 9.6 60.8-+10.4
71.0±7.4 67.5 ± 6.4 66.6± 7.5
'Women were grouped by infant-feeding practice: breast-feeding only, com-
bination of breast- and formula-feeding, or formula-feeding only
METHODS Subjects This report is based on data for 24 women who were studied for 6 months postpartum. Sixty women initially agreed to participate: 23 dropped out within the first month and 13 dropped out later. Analysis of variance and X2 tests of parity and demographic and anthropometric variables found no significant differences as a function of dropout status. Attrition was similar (approximately 60%) regardless of whether a mother breast- or formula-fed her child. Potential subjects were approached 1 to 3 days after giving birth at a suburban hospital. The women were told that the 430 / APRIL 1993 VOLUME 93 NUMBER 4
Procedures and Measures After a subject was recruited in the hospital, she was immediately interviewed, initial anthropometric measurements were taken, and she was given forms for reporting how and when she fed her child. Follow-up anthropometric measurements as well as measures of dietary intake and physical activity were scheduled at 1-month intervals over the next 6 months. In the hospital interview, each subject was asked about demographic variables, previous pregnancies, weight history, prepregnancy weight, plans for feeding her new child, and how any previous children had been fed. Weight gain during pregnancy was determined by subtracting prepregnancy weight from the delivery weight obtained from medical charts. Anthropometric measures included measured height and weight, five skinfold thicknesses (triceps, biceps, subscapular, suprailiac, and midthigh), and four circumferences (midarm, waist, hips, and midthigh). Measurements were performed by two trained research assistants (K. A. M. and J. L.) according to current recommendations (24). Lange calipers (Beta Technology Incorporated, Cambridge, Md) were used to obtain the skinfold thickness measures and a steel tape measure was used to obtain the circumference measures, except for the midarm measure, which was measured using a specially designed device. Each skinfold and circumference measure was taken twice, and the two values were averaged. If the two values differed, two additional measurements were taken. Reliability of the anthropometric measurements, as determined by intra-examiner and inter-examiner measurement errors, were comparable to or smaller than those reported in the National Health and Nutrition Examination Survey (25,26) for 10 of the 12 possible comparisons. Subjects were given stamped, addressed postcards on which to record their method and schedule of infant feeding. The postcards had a 7-day, 24-hour grid on which the women entered the time of day and length of each feeding. This reporting form was reviewed at the initial meeting, and subjects were given a completed example. Postcards were reviewed as received, and any questionable data were discussed with the subject. Women who were breast-feeding recorded the time of day and duration of each feeding for each week during the 6month study. Mothers who were not breast-feeding recorded the type and quantity of formula given and time of day of each feeding for 1 week each month. Skinfold, circumference, weight, and physical activity assessments were obtained at monthly meetings. A trained dietitian conducted a 24-hour dietary recall with each subject at the 1-month meeting using food models and typical utensils for portion estimation. The 1-month meeting served as a training session to enhance reporting accuracy for the three dietary recalls conducted by telephone each month (2 weekdays and 1 weekend day per month). Dietary recall data were analyzed using an interactive nutrient analysis program, MacDiet Professional (version 1, 1986, Drexel University, Philadelphia, Pa) (27). The Minnesota Leisure Time Physical Activity questionnaire (Minnesota LTPA) (28) was administered at each monthly meeting;.an interview format was used to obtain frequency of and time spent on activities such as walking, exercising, sports, gardening, and work in the home. Each activity was weighted by an intensity code (28) to derive an estimate of energy expended daily in voluntary physical activity.
Data Analysis The primary analyses compared the three feeding methods: breast-feeding for the entire 6 months, formula-feeding only, and combined breast- and formula-feeding. Weight changes from delivery to 1, 3, and 6 months postpartum were reported in two ways: as the percentage change from the measured hospital weight taken 1 to 3 days after delivery and as the percentage above self-reported prepregnancy weight. To account for individual differences in weight gain during pregnancy, all weight-related analyses used pregnancy weight gain as a covariate. Particular attention was given to changes in upper- and lower-body fat. The measure of upper-body fat was the sum of triceps, biceps, subscapular, and suprailiac skinfold thicknesses (29). The measures of lower-body fat were hip circumference alone and a composite measure of the sum of the hip and thigh circumferences and the thigh skinfold thickness. Changes in anthropometric measures were reported as a percentage of the values obtained in the hospital shortly after delivery. The SAS general linear model procedure (Statistical Analysis System, version 6, 1985, SAS Institute, Cary NC) (30) was used to conduct multivariate repeated-measures analysis of variance to test whether changes over the 6 months differed as a function of feeding method. Planned comparisons (Dunnett's t test) were also conducted to determine whether changes at each assessment differed for the breast-feeding and combined-feeding groups compared with the formulafeeding group. RESULTS Demographic and other baseline variables did not differ for the three groups, other than, as expected, women in the breastfeeding and combined-feeding groups were more likely to state that they planned to breast-feed their child. For all 24 subjects, mean age was 28.1 years, mean height was 1.65 m, mean years of education was 14.1, and mean household income was $37.5 thousand. All subjects were married and Caucasian, 12 had other children, and 11 of those 12 had breast-fed previously Body Weight and Anthropometric Measures Repeated-measures analysis of covariance was used to determine changes in weight over the 6-month study (ie, percentage above prepregnancy weight and percentage change in body weight from the hospital measurement obtained after delivery). Changes in weight over time were not significant for the three feeding groups separately, but the feeding method by time interactions were significant (P<.05 and P<.03, for percentage above prepregnancy weight and percentage change in body weight, respectively, for Wilks' lambda) when the breastfeeding and combined-feeding groups were collapsed and compared with the formula-feeding group. Women in the breast-feeding and combined-feeding groups lost weight at a faster rate during the first postpartum month than women in and the Table). At 1 the formula-feeding group (Figure month postpartum, the weights of both breast-feeding and combined-feeding mothers were significantly (P<.05) less above prepregnancy weights than were the weights of the formula-feeding mothers. Differences in body weight between the three groups decreased over time and were not significant at 3 or 6 months. However, at 6 months, mothers in the breastfeeding group did riot weigh significantly more than they did before pregnancy, whereas women in the combined-feeding and formula-feeding groups did. The pattern of weight loss expressed as a percentage of the measured hospital weight at delivery was similar. Women in the breast-feeding and combined-feeding groups lost more weight than did mothers in the
FIG 2. Change in maternal hip circumference over 6 postpartum months expressed as a percentage of the hip circumference measure obtained in the hospital after delivery. Vertical bars are standarderrors. At 1 month postpartum, women in both the breast-feeding and combined-feeding groups had significantly (P<.05) larger reductionsin hip circumference than did women in theformula-feeding group. (Hip circumference datawere not collectedfor two subjects.)
formula-feeding group during the first postpartum month; the difference in weight loss between breast-feeding and formulafeeding mothers was significant (P<.05). Changes in hip circumference paralleled those for weight. The repeated-measures analysis indicated that the feeding method by time interaction for the three groups separately was not significant (P<.07), but the interaction of feeding method and time was significant (P<.03) when women in the formula-feeding group were compared with women in both the breast-feeding and combined-feeding groups. The significant interaction again reflects a more rapid, early reduction in hip circumference in women who breast-fed (Figure 2). Follow-up tests of the change at 1 month indicated that women in the breast-feeding and combined-feeding groups lost significantly (P<.05) more than mothers in the formula-feeding group during the first month, but changes in hip circumference were not significantly different thereafter. Changes in the lower-body composite measure were similar to those for hip circumferences, but no group differences were found. The three groups did not show significant differences in change for either the upper-body composite measure or any individual upper-body site. Percentage changes in the upperbody composite were - 2.9% and - 16.7% at 1 and 6 months, respectively, for mothers who breast-fed and were 2.9% and - 16%, respectively, for mothers who fed their infants formula only Interestingly, upper-body changes were more variable than lower-body changes (eg, at 6 months postpartum, the standard deviation in percent change was 3.1 for hip circumference, 3.7 for the lower-body composite, and 35.4 for the JOURNAL OF THE AMERICAN DIETETIC ASSOCIATION / 431
RESEARCH upper-body composite). Changes in the ratio of upper-body and lower-body composite measures reflected the larger initial losses in lower-body fat among women in the breast-feeding and combined-feeding groups but were not significantly different across the three groups. Energy Intake and Expenditure Mean daily energy intake in the breast-feeding and combined feeding groups was 462 kcal more per day than in the formulafeeding group during the entire 6 months. Physical activity, as assessed by the Minnesota LTPA questionnaire, did not vary significantly by time of assessment or by feeding method. Mean energy expenditure in voluntary physical activities was 190.1, 179.1, and 173.1 kcal/day for the breast-feeding, combinedfeeding, and formula-feeding groups, respectively. DISCUSSION The present study suggests that although feeding method may not have an enduring impact, during the initial postpartum weeks, breast-feeding leads to significantly faster loss of body weight and reduction in hip circumference than does formulafeeding. These findings help explain the conflicting results of previous studies that breast-feeding enhances (3,13,14,16), inhibits (19), or has no impact (15,17,18,20,21) on postpartum weight and fat loss relative to formula-feeding. The effect of breast-feeding may depend, in part, on when and at which body sites measurements are obtained. Our results suggest that breast-feeding enhances loss during the first month, that there are no apparent significant effects thereafter, and that the losses primarily affect the lower body. These results are consistent with those of the one study (13) that compared weight and fat changes during the first postpartum month in women who breast-fed or formula-fed their infants. Our results support recent reports on the relationship between breast-feeding, hormonal and enzymatic conditions during lactation, and loss of body fat, particularly in the lower body. In nonpregnant women and, even more so, in pregnant women, lipoprotein lipase activity is higher in lower-body than in upper-body adipose tissue (22). As a result, triglycerides tend to be deposited in lower-body sites, where they are not easily mobilized (22). More frequent feedings increase prolactin (31-33), which enhances lipoprotein lipase activity in mammary tissue and inhibits it in adipose tissue (34-35). A previous study (10) found that fat loss was linked to more frequent feeding. If lactation is infrequent or does not occur, prolactin levels fall rapidly, resulting in a return to the prepregnancy pattern of adipose tissue deposition (33,35-36) and a greater likelihood that adipose tissue will be maintained (37-39). The lack of group differences at 6 months is consistent with the decline over time in both breast-feeding frequency and the prolactin response to feeding (40-41). These studies suggest that feeding method affects fat loss and that the primary effects occur in the lower body during the initial postpartum weeks. Whether this early effect of breast-feeding has long-term consequences, as appears to be the case in animals (7,37-39), remains to be determined. Given that the mean energy intake of the women in the breast-feeding and the combined-feeding groups was 462 kcal more per day than that of women in the formula-feeding group and that breast-feeding may enhance metabolic efficiency and reduce energy expenditure (42), the differences in weight and fat loss between women who breast-fed and women who formula-fed in the present study are probably not due solely to the caloric demands of lactation. Instead, they are consistent with studies that show breast-feeding affects fat storage and mobilization. 432 / APRIL 1993 VOLUME 93 NUMBER 4
APPLICATIONS The present study shows that breast-feeding enhances fat loss in the early postpartum weeks, particularly in the lower body. Further research with larger samples and more frequent measurements during the early phases of lactation is needed to determine the reliability of these findings and their clinical and theoretical relevance. Although these data do not indicate that breast-feeding will eliminate the weight gain often associated with childbearing, the results provide further support for the overall positive effects of breast-feeding for both the infant and the mother. ·
This researchwas supported,in part, by National Institutes of Health grants 5-T32-DK07452 (F M. Kramer), 5-R01-MH31050 (A. J. Stunkard), a Research Scientist Award (A. J Stunkard), and a grantfrom the MacArthur Foundationon Determinationand Consequences of Health Promotingand Health DamagingBehavior (A. J Stunkard). The authors thank James Connauthton,MD; James Kolter, MD, Michael Lemert, MD; Gilbert Liss, MD; and Alan Silverberg, MD, of the Valley Forge Obstetricaland GynecologicalAssociates and the staff of the Phoenixville (Pa) Hospital. We also thank Marlo Baird, Helen Mazuryk, Sheli Tinkleman, and Sharon Whitefor their assistance with data collection. References 1. Beazley JM, Swinhoe JR. Body weight in parous women: is there any alteration between successive pregnancies? Acta Obstet Gynecol Scand. 1979; 58:45-47. 2. Heliovaara M, Aromaa A. Parity and obesity. J Epidemiol Community Health. 1981; 35:179-199. 3. Ohlin A, Rossner S. Maternal body weight development after pregnancy. Int J Obes. 1990; 14:159-173. 4. Bradley PJ. Conditions recalled to have been associated with weight gain in adulthood. Appetite. 1985; 6:235-241. 5. Rossner S. Pregnancy, weight cycling, and weight gain in obesity. Int J Obes. 1992; 16:145-147. 6. Institute of Medicine. Nutrition During Pregnancy:Weight Gain and Nutrient Supplements. Washington, DC: National Academy Press; 1990. 7. Institute of Medicine. Nutrition During Lactation. Washington, DC: National Academy Press; 1991. 8. Adair LS, Pollitt E, Mueller WH. Maternal anthropometric changes during pregnancy and lactation in a rural Taiwanese population. Hum Biol. 1983; 55:771-787. 9. Butte NF, Garza C, Stuff JE, Smith EO, Nichols BL. Effect of maternal diet and body composition on lactational performance. Am J Clin Nutr 1984; 39:296-306. 10. Quandt SA. Changes in maternal adiposity and infant feeding patterns. Am JPhysAnthropol,1983; 60:455-461. 11. Sadurskis A, Kabir N, Wager J, Forsumr E. Energy metabolism, body composition, and milk production in healthy Swedish women during lactation. Am J Clin Nutr 1988; 48:44-49. 12. Nommsen LA, Lovelady CA, Heinig MJ, Lonnerdal B, Dewey KG. Determinants of energy, protein, lipid, and lactose concentrations in human milk during the first 12 mo of lactation: The DARLING Study. Am J Clin Nutr. 1991; 53:457-465. 13. Bradshaw MK, Pfeiffer S. Feeding mode and anthropometric changes in primiparas. Hum Biol. 1988; 60:251-261. 14. Brewer MM, Bates MR, Vannoy LP. Postpartum changes in maternal weight and body fat depots in lactating vs nonlactating women. Am J Clin Nutr. 1989; 49:259-265. 15. Dugdale AE, Eaton-Evans J. The effect of lactation and other factors on post-partum changes in body-weight and triceps skinfold thickness. Br J Nutr 1989; 61:149-153.
16. English RM, Hitchcock NE. Nutrient intakes during pregnancy, lactation and after the cessation of lactation in a group of Australian women. Br JNutr 1968; 22:615-624. 17. Manning-Dalton C, Allen LH. The effects of lactation on energy and protein consumption, postpartum weight change and body composition of well nourished North American women. Nutr Res. 1983; 3: 293-308. 18. Naismith DJ, Ritchie CD. The effect of breast-feeding and artificial feeding on body-weights, skinfold measurements and food intakes of forty-two primiparous women. ProcNutr Soc. 1975; 34:116A- 117A. 19. Rookus MA, Rokebrand P, Burema J, Deurenberg P. The effect of pregnancy on the body mass index 9 months postpartum in 49 women. IntJObes. 1987; 11:609-618. 20. Thomson AM, Hytten FE, Billewicz WZ. The energy cost of human lactation. Br J Nutr 1970; 24:565-572. 21. Potter S, Hannum S, McFarlin B, Essex-Sorlie D, Campbell E, Trupin S. Does infant, feeding method influence maternal postpartum weight loss? JAm Diet Assoc. 1991; 91:441-446. 22. Rebuffe-Scrive M, Enk L, Crona N, Lonnroth P, Abrahamsson L, Smith U, Bjorntorp P. Fat cell metabolism in different regions in women: effect of menstrual cycle, pregnancy and lactation. J Clin Invest. 1985; 75:1973-1976. 23. Greenwood MRC, Savard R, West DB, Kava R. Energy metabolism and nutrient 'gating' in pregnancy and lactation. In: Berry E, Blondheim SH, Eliahou HE, Shafrir E, eds. RecentAdvances in Obesity Research: V London, England: John Libbey and Co; 1987:258-263. 24. Lohman TG, Roche AF, Martorell R. Anthropometric Standardization Reference Manual. Champaign, Ill: Human Kinetics Books; 1988. 25. Johnston FE, Hamill PVVW, Lemeshow S. Skinfold thickness of youths 12-17 years. United States. Rockville Md: National Center for Health Statistics; 1974. US Dept of Health, Education and Welfare publication (HRA) 74-1614. 26. Malina RM, Hamill PW, Lemeshow S. Selected body measurements of children 6-11 years. United States. Rockville MD: National Center for Health Statistics; 1973. US Dept of Health, Education, and Welfare publication HSM 73-1605. 27. McKinney S. MacDiet Professional: interactive nutrient analysis and energy balance program. JDietSoftware. 1989;30-35. 28. Taylor HL, Jacobs DR, Schucker B, Knudsen J, Leon AS, Debacker G. A questionnaire for the assessment of leisure time physical activity.
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97. 30. SAS/STAT User's Guide for Personal Computers, Version 6 Edition. Cary, NC: SAS Institute Inc; 1985. 31. Delvoye P, Demaegd M, Delogne-Desnoeck J. The influence of the frequency of nursing and of previous lactation experience on serum prolactin in lactating mothers. JBiosoc Sci. 1977; 9:447-451. 32. Glasier A, McNeilly AS, Howie PW The prolactin response to suckling. Clin Endocrinol. 1984; 21:109-116. 33. Hamosh M, Clary TR, Chernick SS, Scow RO. Lipoprotein lipase activity of adipose and mammary tissue and plasma triglyceride in pregnant and lactating rats. Biochim Biophys Acta. 1970; 210:473482. 34. Scow RO, Chernick SS, Fleck TR. Lipoprotein lipase and uptake of triacylglycerol, cholesterol and phosphatidylcholine from chylomicrons by mammary and adipose tissue of lactating rats in vivo. Biochim Biophys Acta. 1977; 487:297-306. 35. Steingrimsdottir L, Brasel JA, Greenwood MRC. Diet, pregnancy, and lactation: effects on adipose tissue, lipoprotein lipase, and fat cell size. Metabolism. 1980; 29:837-841. 36. Radcliffe MA, Colville C. Effect of litter removal and prolactin on lipolysis in parametrial white fat cells of lactating rats. Proc Nutr Soc. 1988; 47:110A. Abstract. 37. Jen K-LC, Juuhl N, Lin PKH. Repeated pregnancy without lactation: effects on carcass composition and adipose tissue cellularity in rats. J Nutr. 1988; 118:93-98. 38. Moore BJ, Brasel JA. One cycle of reproduction consisting of pregnancy, lactation or no lactation, and recovery: effects on carcass composition in ad libitum-fed and food-restricted rats. J Nutr 1984; 114:1548-1559. 39. Moore BJ, Brasel JA. One cycle of reproduction consisting of pregnancy, lactation or no lactation, and recovery: effects on fat pad cellularity in ad libitum-fed and food-restricted rats. J Nutr 1984; 114: 1560-1565. 40. Johnston JM, Amico JA. A prospective longitudinal study of the release of oxytocin and prolactin in response to infant suckling in long term lactation. J Clin EndocrinolMetab. 1986; 62:653-657. 41. Yuen BH. Prolactin in human milk: the influence of nursing and the duration of postpartum lactation. Am J Obstet GyJnecol. 1988; 158: 583-586. 42. Prentice AM, Prentice A. Energy costs of lactation. Annu Rev Nutr. 1988; 8:63-79.
OF HWTT TO YO
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JOURNAL OF THE AMERICAN DIETETIC ASSOCIATION / 433