ARTICLES

The Journal of Nutrition, FEB. 2009 (link)

Duration of Breast-feeding and Adiposity in Adult Life

^{1 Presented at the conference “Infant Feeding and the Development of Obesity: What Does the Science Tell Us?” held in San Diego, CA, April 9, 2008 during the American Society for Nutrition’s annual meeting at Experimental Biology. The conference was sponsored by The International Formula Council (IFC), Atlanta, GA. The contents are the sole responsibility of the authors. The papers comprising this supplement were developed independently, and the conclusions drawn do not represent the official views of IFC. The mention of trade names, commercial products, or organizations does not imply endorsement by IFC. Supplement Coordinator for the supplement publication was Heather Gorby, Life Sciences Research Office, Bethesda, MD., 2 Supported by the British Heart Foundation, the Academy of Finland, the Paivikki and Sakari Sohlberg Foundation, the Finnish Diabetes Research Foundation, the Finnish Foundation for Cardiovascular Research, the Finnish Medical Society Duodecim, Yrjo Jahnsson Foundation, and Finska Lakaresällskapet. This substudy was funded by the International Formula Council., 3 Author disclosures: P. O’Tierney received compensation from the Infant Formula Council for speaking at the symposium; D. J. P. Barker and E. Kajantie received funding for this research from the International Formula Council; C. Osmond and J. G. Eriksson, no conflicts of interest. Heart Research Center, Oregon Health and Science University, Portland, OR 97239}

Perrie F. O’Tierney,^{3 Author disclosures: P. O’Tierney received compensation from the Infant Formula Council for speaking at the symposium; D. J. P. Barker and E. Kajantie received funding for this research from the International Formula Council; C. Osmond and J. G. Eriksson, no conflicts of interest. Heart Research Center, Oregon Health and Science University, Portland, OR 97239} David J. P. Barker,^{3 Author disclosures: P. O’Tierney received compensation from the Infant Formula Council for speaking at the symposium; D. J. P. Barker and E. Kajantie received funding for this research from the International Formula Council; C. Osmond and J. G. Eriksson, no conflicts of interest. Heart Research Center, Oregon Health and Science University, Portland, OR 97239, 4 MRC Epidemiology Resource Center, University of Southampton, SO16 6YD Southampton, UK} Clive Osmond,^{4 MRC Epidemiology Resource Center, University of Southampton, SO16 6YD Southampton, UK} Eero Kajantie,^{5 National Public Health Institute, FIN 00300 Helsinki, Finland} and Johan G. Eriksson^{5 National Public Health Institute, FIN 00300 Helsinki, Finland, 6 University of Helsinki, FIN-00014 Helsinki, Finland}

Abstract

Few studies have examined whether the duration of breast-feeding is associated with BMI in adult life. In the past, the heights and weights of infants and the duration of breast-feeding were routinely recorded at infant welfare clinics in Helsinki, Finland. Most infants in the city were taken to these free clinics. The Helsinki Birth Cohort comprises 13,345 people born in the city during 1934–1944; 84% were breast-fed. In 2001, a questionnaire was sent to members of the cohort asking about their weight and height. A random sample of 2003 men and women attended a clinic at which height, weight, and body composition were measured. We studied sibships that included 2 or more people from the cohort. There were 1823 subjects: 831 had completed the questionnaire; 129 had attended the clinic. Wegrouped the subjects according to duration of breast-feeding: 0–2 mo, 3–4 mo, 5–7 mo, and 8 mo or more. We compared siblings who were discordant for duration of breast-feeding. We found that a longer period of breast-feeding was associated with lower BMI at 1 y of age (P = 0.04 for a linear trend). This relation disappeared by the age of 7 y. People breast-fed for 5–7 mo had the lowest reported BMI at age 60 y, although this was not statistically significant; 8.8% more people breast-fed for 8 mo or more had reported BMIs that were overweight (25 to 30 kg/m2) compared with those breast-fed for shorter periods (P 0.06). Breast-feeding for <2 mo or 8 mo or more was associated with an increased BMI and percentage body fat in later life, measured at the clinic (P = 0.08 and P = 0.03 for quadratic trends). We conclude that breast-feeding for <2 mo may be deleterious, possibly because of lack of exposure to protective factors in breast milk. Breast-feeding beyond 8 mo may be deleterious because mother’s hormones in breast milk reset the infant’s hypothalamic-pituitary-thyroid axis. J. Nutr. 139: 422S–425S, 2009.

Breast-Feeding and Obesity

There is evidence that increased intensity and exclusivity of breastfeeding is associated with decreased incidence of obesity and overweight in childhood and adolescence ^{(1 Weyermann M, Rothenbacher D, Brenner H. Duration of breastfeeding and risk of overweight in childhood: a prospective birth cohort study from Germany. Int J Obes (Lond). 2006; 30:1281–7., 2 Gillman MW, Rifas-Shiman SL, Camargo CA Jr, Berkey CS, Frazier AL, Rockett HR, Field AE, Colditz GA. Risk of overweight among adolescents who were breastfed as infants. JAMA. 2001; 285:2461–7., 3 Grummer-Strawn LM, Mei Z. Does breastfeeding protect against pediatric overweight? Analysis of longitudinal data from the Centers for Disease Control and Prevention Pediatric Nutrition Surveillance Sytem. Pediatrics. 2004; 113: e81–6., 4 Mayer-Davis EJ, Rifas-Shiman SL, Zhou L, Hu FB, Colditz GA, Gillman MW. Breast-feeding and risk for childhood obesity: does maternal diabetes or obesity status matter? Diabetes Care. 2006; 29:2231–7.)}. These associations, however, are difficult to interpret because mothers who elect to breast-feed for prolonged periods may differ inmany ways from those who do not. A recent meta-analysis, after adjusting for possible confounds, reported no strong association between breast-feeding and risk of obesity in adolescence ^{(5 Owen CG, MartinRM, Whincup PH, Davey SmithG, CookDG. Effect of infant feeding on the risk of obesity across the life course: a quantitative review of published evidence. Pediatrics. 2005; 115:1367–77.)}.

Different types of analyses have been done to avoid confounding variables. One example is sibling analysis ^{(2 Gillman MW, Rifas-Shiman SL, Camargo CA Jr, Berkey CS, Frazier AL, Rockett HR, Field AE, Colditz GA. Risk of overweight among adolescents who were breastfed as infants. JAMA. 2001; 285:2461–7., 6 Nelson MC, Gordon-Larsen P, Adair LS. Are adolescents who were breast-fed less likely to be overweight? Analyses of sibling pairs to reduce confounding. Epidemiology. 2005; 16:247–53.)}. Gillman et al. ^{(2 Gillman MW, Rifas-Shiman SL, Camargo CA Jr, Berkey CS, Frazier AL, Rockett HR, Field AE, Colditz GA. Risk of overweight among adolescents who were breastfed as infants. JAMA. 2001; 285:2461–7.)} reported that observations on siblings discordant for duration of breast-feeding supported the hypothesis that breastfeeding was protective against overweight in adolescence. Sibling analysis controls for many maternal variables, but the issue remains unresolved. Kramer et al. ^{(7 Kramer MS, Matush L, Vanilovich I, Platt RW, Bogdanovich N, Sevkovskaya Z, Dzikovich I, Shishko G, Collet JP, et al. Effects of prolonged and exclusive breastfeeding on child height, weight, adiposity, and blood pressure at age 6.5 y: evidence from a large randomized trial. Am J Clin Nutr. 2007; 86:1717–21.)} presented results in this symposium showing that, in an interventional trial, prolonged and exclusive breast-feeding was unrelated to BMI in childhood. There are few data linking the duration of breast-feeding with body composition in adult life.

In Hertfordshire, UK, in the 1920s and 1930s, a health visitor routinely visited each baby and collected information on breastfeeding, infant weights, and growth ^{(8 Syddall HE, Aihie SA, Dennison EM, Martin HJ, Barker DJ, Cooper C. Cohort profile: the Hertfordshire cohort study. Int J Epidemiol. 2005; 34:1234–42.)}. A sample of men born in Hertfordshire was examined at the mean age of 70 y. There was no difference in the BMI of those who had been bottle-fed, breast- and bottle-fed, or exclusively breast-fed, and neither was there a difference in the BMI of those exclusively breast-fed for <1 y or >1 y ^{(9 Fall CH, Barker DJ, Osmond C, Winter PD, Clark PM, Hales CN. Relation of infant feeding to adult serum cholesterol concentration and death from ischaemic heart disease. BMJ. 1992; 304:801–5.)}. Compared with men who were weaned off breast milk before 1 y of age, those who were not weaned had higher total cholesterol, low-density lipoprotein cholesterol, and apolipoprotein B concentrations and higher death rates from coronary heart disease. Here we present data from the Helsinki Birth Cohort, in which we examined the association between duration of breast-feeding and later BMI and adiposity by comparing people with their siblings breast-fed for different lengths of time.

Methods

The Helsinki Birth Cohort comprises 13,345 men and women who were born in Helsinki, Finland from 1934 to 1944 ^{(10 Eriksson J, Forsen T, Osmond C, Barker D. Obesity from cradle to grave. Int J Obes Relat Metab Disord. 2003; 27:722–7., 11 Eriksson J, Forsen T, Tuomilehto J, Osmond C, Barker D. Size at birth, childhood growth and obesity in adult life. Int J Obes Relat Metab Disord. 2001; 25:735–40.)}. As children, they attended child-welfare clinics. These clinics were free, and nearly all children attended, with an average of 8 visits per child between birth and 2 y of age. The clinics measured the child’s height and weight and recorded infant feeding and the father’s occupation. All members of the cohort were still living in Finland in 1971, when a personal identification number was assigned to each resident of Finland. This number has been used to trace the cohort and record illnesses and mortality up to the present day. In 2000, a questionnaire was sent to each person in the cohort, asking her/him to record her/his heights and weights. A random sample of 2003 people attended a clinic at an average age of 62 y. At the clinic, their heights and weights were recorded and percent body fat was measured by electrical impedance ^{(10 Eriksson J, Forsen T, Osmond C, Barker D. Obesity from cradle to grave. Int J Obes Relat Metab Disord. 2003; 27:722–7., 11 Eriksson J, Forsen T, Tuomilehto J, Osmond C, Barker D. Size at birth, childhood growth and obesity in adult life. Int J Obes Relat Metab Disord. 2001; 25:735–40.)}. The Ethical Committee of Epidemiology and Public Health at the Helsinki and Uusimaa Hospital District approved this project, and all participants in the clinical study signed an informed consent.

Eighty-four percent of sibling pairs in the full cohort had been breastfed. We excluded anyone who had not been breast-fed from further analysis. This resulted in 1823 breast-fed individuals belonging to sibships. Of those participants that responded to the questionnaire, 831 had been breast-fed and belonging to sibships. When only 1 individual of a sibling pair responded, neither sibling was included in the questionnaire analysis. Similar criteria were employed for the clinic visit data, resulting in the analysis of 129 clinic attendees in sibships.

Statistical analysis

We divided individuals into 4 categories based on the duration of breastfeeding; <2 mo, 3 to 4 mo, 5 to 7 mo, or >8 mo. We compared siblings who were discordant for the duration of breast-feeding using a linear mixed model that allowed for the correlation of BMI and percentage body fat among members of the same sibship. Indicator variables for breast-feeding groups were included as fixed effects in the linear mixed model, with the 5- to 7-mo group as the baseline for comparison. A P-value of <0.05 was considered significant for a linear or quadratic trend. All data were adjusted for sex, year of birth and sibship size.

Results

Within the cohort, the median duration of breast-feeding was 171 d. Infants born into the families of manual workers were breast-fed for longer (180 d) than those born into lower (165 d) and upper (150 d) middle-class families.

We investigated the relation between the duration of breastfeeding and BMI during childhood (Table 1). At age 1 y, there was a progressive fall in BMI with increasing length of breastfeeding (P < 0.05 for linear trend). This association had disappeared by age 7 (P = 0.50). Breast-feeding had no effect on height in childhood (data not shown).

Current adult BMI was calculated from self-reported questionnaire data. People breast-fed for 5-7 mo had the lowest mean BMI, although this was not statistically significant as either a linear (P = 0.80) or quadratic trend (P = 0.90) (Table 2).

We divided the subjects according to whether their reported BMI was in the category of overweight (25–30 kg/m2) or obese (>30 kg/m2): 8.8% more people who had been breast-fed for 8 mo or more were overweight at age 60 y compared with those breast-fed for shorter periods (P = 0.06) (Table 2).

Among those subjects who had attended clinics where BMI and percentage body fat had been recorded, a U-shaped association was found between duration of breast-feeding and current BMI (Table 3). The highest BMIs were observed in those siblings breast-fed for the shortest period, <2 mo, or for the longest, 8 mo or more (P = 0.08 for quadratic trend). There is a significant U-shaped association between duration of breast-feeding and percentage body fat (P = 0.03 for quadratic trend).

TABLE 1    Association between duration of breast-feeding and sibling differences in childhood BMI
Duration of		BMI at 1 y, kg/m2			BMI at 7 y, kg/m2
breast-feeding, mo	n1	Mean ± SD	Difference1 (95% CI)	n1	Mean ± SD	Difference1 (95% CI)
<2	415	17.88 ± 1.46	0.08 (–0.10, 0.25)	415	15.45 ± 1.15	0.05 (–0.10, 0.19)
3–4	369	17.82 ± 1.44	0.02 (–0.02, 0.15)	369	15.47 ± 1.22	0.08 (–0.06, 0.22)
5–7	523	17.77 ± 1.37	0 reference	525	15.43 ± 1.15	0 reference
≥8	514	17.71 ± 1.32	–0.14 (–0.3, 0.02)	514	15.46 ± 1.17	0.02 (–0.11, 0.16)
P–linear trend			0.04			0.50
P–linear trend			1.00			0.70
1 Difference, the differences in BMI are calculated relative to the 5– to 7–mo group and are adjusted for sex, year of birth, and sibship size.

TABLE 2    Sibling differences in reported adult BMI and percentage of people who were overweight according to duration of breast-feeding
Duration of		BMI, kg/m2			Overweight, % (BMI 25–30 kg/m2)
breast-feeding, mo	n1	Mean ± SD	Difference1 (95% CI)		%	Difference1 (95% CI)
<2	206	26.6 ± 4.3	0.03 (–0.05, 1.1)		42.7	1.6 (–7.7, 11.0)
3–4	168	26.3 ± 4.3	0.03 (–0.05, 1.1)		42.9	1.9 (–8.0, 11.8)
5–7	233	26.2 ± 4.2	0 reference		41.2	0 reference
≥8	224	26.5 ± 4.0	0.2 (–0.5, 1.0)		50.0	8.8 (–0.3, 18.0)
P–linear trend			0.80			0.08
P–linear trend			0.90			0.50
1 Mean, average BMI of subjects in each group; %, percentage of overweight (BMI = 25–30) subjects within each group; difference, the differences in BMI or percentage overweight are calculated relative to the 5– to 7–mo group and are adjusted for sex, year of birth, and sibship size; CI, confidence interval.

TABLE 3    Sibling differences in adult body mass index and percent body fat measured at clinic according to duration of breast-feeding
Duration of		BMI, kg/m2			Body fat, %
breast-feeding, mo	n1	Mean ± SD	Difference1 (95% CI)	n	Mean ± SD	Difference1 (95% CI)
<2	22	29.5 ± 4.3	2.3 (–0.1, 4.7)	21	32.6 ± 9.7	3.9 (0.3, 07.4)
3–4	30	26.8 ± 5.2	–0.4 (–02.7, 1.8)	26	27.6 ± 8.5	0.3 (–03.1, 03.7)
5–7	38	26.9 ± 4.2	0 reference	36	28.4 ± 6.6	0 reference
≥8	39	28.2 ± 4.9	1.2 (–0.9, 3.2)	38	30.8 ± 8.0	1.3 (–1.7, 4.3)
P–linear trend			0.80			0.50
P–linear trend			0.08			0.03
1 Mean, average body mass index or percentage body fat in each group; difference, the differences in BMI or percentage body fat are calculated relative to the 5– to 7–mo group and are adjusted for sex, year of birth, and sibship size; CI, confidence interval.

Discussion

We have analyzed adult BMI and adiposity within sibling pairs whose duration of breast-feeding had been recorded at the time. The siblings were part of the Helsinki Birth Cohort, 84% of whom were breast-fed for an average duration of nearly 6 mo. We divided the siblings into 4 groups according to the length of breast-feeding. We found that longer periods of breast-feeding were associated with lower BMI at 1 y of age; however, this effect on BMI had disappeared by the age of 7 y. More siblings breast-fed for 8 mo or longer reported that they were overweight at age 60 y compared with those breast-fed for shorter periods, although this was of borderline statistical significance (P = 0.06). Among siblings who had attended a clinic, and therefore had accurate measurements of height and weight at that time, those who had been breast-fed for <2 mo or >8 mo had the highest BMI and percentage body fat. The findings for percentage body fat, measured by electrical impedance, were stronger than those for BMI, presumably because BMI can reflect either muscularity or adiposity.

Consistent with other studies of babies born 60 and more years ago, we found that those in poorer families tended to be breast-fed for longer ^{(9 Fall CH, Barker DJ, Osmond C, Winter PD, Clark PM, Hales CN. Relation of infant feeding to adult serum cholesterol concentration and death from ischaemic heart disease. BMJ. 1992; 304:801–5.)}. One reason for this is that breastfeeding was used as a method of contraception ^{(9 Fall CH, Barker DJ, Osmond C, Winter PD, Clark PM, Hales CN. Relation of infant feeding to adult serum cholesterol concentration and death from ischaemic heart disease. BMJ. 1992; 304:801–5.)}. In those days women who breast-fed their babies for different periods of time differed in many respects. Reported associations between length of breast-feeding and BMI in childhood and adolescence could therefore be the result of confounding variables including diet and physical activity in childhood. Sibling analysis controls for many potential confounding variables. The limitation of our analyses is that only siblings who are discordant for the length of breast-feeding contribute information.

Breast-feeding for 2 mo or less could have been deleterious because the alternative feeding was harmful. We have no information on what foods other than breast milk were given to the infants in our study. The infants were born before modern formulas became available and at a time when there were food shortages in Finland. Another possible explanation for the association between short duration of breast-feeding and high BMI and fat mass is that there are growth factors or hormones in breast milk that program the baby in ways that protect against excessive fat deposition in later life.

An explanation for the association between prolonged breastfeeding and high body fat is that prolonged exposure to maternal hormones in breast milk may permanently reset lipid metabolism. In the Hertfordshire cohort, prolonged breast-feeding is associated with high serum cholesterol concentrations in later life ^{(9 Fall CH, Barker DJ, Osmond C, Winter PD, Clark PM, Hales CN. Relation of infant feeding to adult serum cholesterol concentration and death from ischaemic heart disease. BMJ. 1992; 304:801–5.)}. Hertfordshire women breast-fed for longer than 1 y had increased free thyroxine concentrations ^{(12 Phillips DI, Barker DJ, Osmond C. Infant feeding, fetal growth and adult thyroid function. Acta Endocrinol (Copenh). 1993; 129: 134–8.)}. Thyroid hormones have been implicated in the regulation of circulating lipoprotein concentrations ^{(13 Heimberg M, Olubadewo JO, Wilcox HG. Plasma lipoproteins and regulation of hepatic metabolism of fatty acids in altered thyroid states. Endocr Rev. 1985; 6:590–607.)}. Studies in baboons have shown that, 1 y after weaning, those who were breast-fed had higher thyroxine concentrations than those who were bottle-fed ^{(14 Mott GE, Lewis DS, Jackson EM, McMahan CA. Preweaning diet programs postweaning plasma thyroxine concentrations in baboons. Proc Soc Exp Biol Med. 1996; 212:342–8.)}. When given a high-cholesterol diet, these breast-fed baboons had alterations in cholesterol metabolism that were more atherogenic than those in baboons that had been formula-fed ^{(15 Lewis DS, Mott GE, McMahan CA, Masoro EJ, Carey KD, McGill HC Jr. Deferred effects of preweaning diet on atherosclerosis in adolescent baboons. Arteriosclerosis. 1988; 8:274–80.)}. We speculate that the association between prolonged breast-feeding, beyond the usually recommended period, is associated with persisting alterations in lipid metabolism, which become evident as a high fat mass and atherogenic lipid profile in later life.

Other articles in this supplement include references ^{(16 Butte NF. Impact of infant feeding practices on childhood obesity. J Nutr. 2009; 139:412–6., 17 Adair LS. Methods appropriate for studying the relationship of breastfeeding to obesity. J Nutr. 2009; 139:408–11., 18 Kramer MS, Matush L, Vanilovich I, Platt RW, Bogdanovich N, Sevkovskaya Z, Dzikovich I, Shishko G, Collet J-P, et al. A randomized breast-feeding promotion intervention did not reduce child obesity in Belarus. J Nutr. 2009; 139:417–21.)}.

The Journal of Nutrition
Infant Feeding and the Development of Obesity: What Does the Science Tell Us?
© 2009 American Society for Nutrition.
First published online December 23, 2008; doi:10.3945/jn.108.097089.