Published online before print March 1, 2004, doi: 10.1161/01.CIR.0000118468.76447.CE
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(Circulation. 2004;109:1259-1266.)
© 2004 American Heart Association, Inc.
Clinical Investigation and Reports |
Does Breast-Feeding in Infancy Lower Blood Pressure in Childhood?
The Avon Longitudinal Study of Parents and Children (ALSPAC)
From the Department of Social Medicine (R.M.M., D.G., G.D.S.) and the Unit of Paediatric and Perinatal Epidemiology, Division of Child Health, University of Bristol, Bristol, UK (A.R.N., P.E.).
Correspondence to Richard M. Martin, MSc, MFPH, Department of Social Medicine, University of Bristol, Canynge Hall, Whiteladies Road, Bristol, UK, BS8 2PR. E-mail richard.martin{at}bristol.ac.uk
Received August 5, 2003; revision received November 11, 2003; accepted December 5, 2003.
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Abstract |
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Background— Breast-feeding in infancy has been associated with decreased coronary heart disease mortality, but the underlying mechanisms are unclear. We investigated the association of breast-feeding with blood pressure in a contemporary cohort.
Methods and Results— In a prospective cohort study (ALSPAC, United Kingdom), a total of 7276 singleton, term infants born in 1991 and 1992 were examined at 7.5 years. Complete data were available for 4763 children. The systolic and diastolic blood pressures of breast-fed children were 1.2 mm Hg lower (95% CI, 0.5 to 1.9) and 0.9 mm Hg lower (0.3 to 1.4), respectively, compared with children who were never breast-fed (models controlled for age, sex, room temperature, and field observer). Blood pressure differences were attenuated but remained statistically significant in fully adjusted models controlling for social, economic, maternal, and anthropometric variables (reduction in systolic blood pressure: 0.8 mm Hg [0.1 to 1.5]; reduction in diastolic blood pressure: 0.6 mm Hg [0.1 to 1.0]). Blood pressure differences were similar whether breast-feeding was partial or exclusive. We examined the effect of breast-feeding duration. In fully adjusted models, there was a 0.2-mm Hg reduction (0.0 to 0.3) in systolic pressure for each 3 months of breast-feeding.
Conclusions— Breast-feeding is associated with a lowering of later blood pressure in children born at term. If the association is causal, the wider promotion of breast-feeding is a potential component of the public health strategy to reduce population levels of blood pressure.
Key Words: pediatrics • breast feeding • blood pressure • nutrition
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Introduction |
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Breast-feeding is linked with a number of health benefits in childhood, but it may have longer-term effects, including protection against coronary heart disease mortality.1 There is inconsistent evidence, however, on the association between breast-feeding and coronary heart disease risk factors.2–13
Conflicting evidence may have arisen for several reasons. First, studies have included infants born at different times throughout the 20th century,4,9,10 during which the composition of artificial feeds changed markedly. Associations with particular components of these feeds may explain differences in results. Second, different definitions of breast-feeding may lead to inconsistent results.5,10 Third, breast-feeding duration may be misclassified in studies based on retrospective recall.14 Fourth, the strength of the relation may depend on the age at outcome measurement.2,15 Finally, control for confounding in some studies may have been inadequate.8,16
Two experimental studies support an influence of infant nutrition on blood pressure. In one, preterm infants assigned donor human milk had lower adolescent blood pressures than infants fed preterm formula.2 In another, sodium restriction was associated with a 2-mm Hg reduction in systolic blood pressure in infancy,17 an effect that persisted into adolescence.18
We investigated the association of breast-feeding with childhood blood pressure in a large, contemporary cohort, with prospective recording of infant feeding method and measures of a wide range of potential confounding factors.19
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Methods |
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ALSPAC is a prospective cohort study investigating the health and development of children. Details of methods have been published in full.19 Briefly, 14 541 pregnant women resident in 3 Bristol-based health districts with an expected date of delivery between April 1991 and December 1992 were enrolled on entry to the antenatal care system. In total, 7276 term (gestation: 36 to 44 weeks) singleton children were examined at age 7 years (Figure). Informed consent was obtained from the mothers, ethical approval was granted by local research ethics committees, and the procedures conformed to institutional guidelines.
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Infant Feeding
Data on method of infant feeding were obtained from questionnaires sent to mothers when the child was 6 and 15 months of age. We derived variables for (1) whether any breast-feeding occurred, coded as "ever" or "never" breast-fed; (2) the exclusivity of breast-feeding, coded as "exclusive breast-feeding beyond 2 months of age," "partial breast-feeding" (ie, breast-feeding had been stopped or was nonexclusive by 2 months), and "never breast-fed"; and (3) the duration of any breast-feeding, coded as "never," "<3 months," "3 to 6 months," and ">6 months." Exclusive breast-feeding was defined as no solids, milk formulas, or other drinks (except vitamins, minerals, medicines, and/or water). At 32 weeks of gestation, mothers were asked whether they intended to breast-feed or bottle-feed their child for the first 3 months.
Confounding Factors
Infant sex, ethnic background, health status, birth weight, gestational age, familial factors (overcrowding, number of older siblings, family income), and several maternal factors (socioeconomic position, education, smoking during pregnancy, alcohol consumption, self-reported height, self-reported prepregnancy weight, history of hypertension, and age at the birth of the child) were identified as potential confounding factors. Socioeconomic position was coded as manual (blue-collar, semiskilled, and unskilled socioeconomic background) or non-manual (professional, managerial, and white-collar socioeconomic background).
Measurements
Weight (in kilograms) at ages 6 weeks and 9 months was available from routine health visitor records. At the 7-year follow-up, blood pressure was measured with a Dinamap 9301 Vital Signs Monitor by 1 of 13 observers; height was measured to the nearest 0.1 cm with a Leicester stadiometer, and weight in underwear was measured to the nearest 0.1 kg with SECA scales. Our measure of maternal and childhood adiposity was body mass index (BMI, kg/m2).
Statistical Analysis
Blood pressure values are based on the mean of 2 readings. Associations of breast-feeding with potential confounding factors were investigated by use of 
2 or t tests as appropriate. Associations of breast-feeding and potential confounding factors with blood pressure were examined by linear regression. Multivariable linear regression controlled for social factors, maternal factors, and maternal, infant, and childhood anthropometry. Those factors that altered effect estimates by at least 5% were included in the final models. To standardize conditions of measurement, all models controlled for room temperature and field observer. All models were based on 4763 children with complete data. Likelihood ratio tests were used to test for interaction by sex,5 resting heart rate,18 and current BMI.20
Infants self-regulate food intake and weight gain,21 and accelerated postnatal growth is associated with later blood pressure.22,23 To investigate the importance of postnatal growth, we developed models controlling separately and in combination for weight at 6 weeks and at 9 months and for rate of weight gain between 6 weeks and 9 months (rate calculated as 9-month minus 6-week weight, divided by the time in weeks between examinations and multiplied by 4.36 to express weight gain in kilograms per month). Associations adjusted for weight gain were based on 4538 subjects.
To determine whether breast-feeding is a marker for other factors associated with both the decision to breast-feed and blood pressure, we investigated the breast-feeding–blood pressure association among mothers who, when questioned antenatally, intended to breast-feed their newborn child and compared those who actually breast-fed with those who did not. Analyses were performed by use of Stata software.24
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Results |
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The median age of the 7276 children attending the physical examination was 7.5 years (interquartile range, 7.4 to 7.6 years; range, 6.6 to 9.3 years); 51% were male. Of all mothers, 83% reported ever having breast-fed and 34% reported exclusively breast-feeding beyond 2 months (Table 1). Of those who breast-fed, 49% did so for 6 months.
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Representativeness
Participants in the 7-year follow-up were similar to nonparticipants with regard to infant sex, timing of introduction of solids, ethnicity, number of older siblings, maternal hypertension, infant health status, gestational age, and maternal BMI, but they were more likely to have been breast-fed and to have been breast-fed for longer and to come from more affluent social and economic categories, and were heavier at birth (Table 1). Participants’ mothers were slightly taller and older and were less likely to have smoked during pregnancy than nonparticipants’ mothers.
Factors Associated With Breast-Feeding
Breast-feeding was positively associated with increasing age at introduction of solids, greater affluence, having fewer older siblings, absence of maternal hypertension and smoking, greater maternal height and age, and child’s height (Table 2). Breast-feeding was inversely associated with maternal and child BMI.
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Factors Associated With Blood Pressure
Mean systolic blood pressure levels were similar in boys (98.7 mm Hg) and girls (98.9 mm Hg) (P=0.4), but boys had slightly lower mean diastolic blood pressures (56.1 mm Hg) than girls (56.9 mm Hg) (P<0.001). Blood pressure levels were lower with greater family income, higher birth weight, a number of maternal factors (nonmanual maternal social class, higher maternal educational achievement, absence of maternal hypertension or smoking during pregnancy, increased maternal age, and reduced maternal height and prepregnancy BMI), lower weight gain in infancy, lower current height, and lower BMI (Table 2).
Breast-Feeding and Blood Pressure
Blood pressure was lower among breast-fed than formula-fed children (Tables 3 and 4
). In simple models controlling for age, sex, room temperature, and field observer, systolic and diastolic pressures were, respectively, 1.2 mm Hg lower (95% CI, 0.5 to 1.9) and 0.9 mm Hg lower (0.3 to 1.4) among breast-fed than formula-fed children (Table 4). In fully adjusted models, the reduction in systolic pressure associated with any breast-feeding was 0.8 mm Hg (0.1 to 1.5), and the reduction in diastolic pressure was 0.6 mm Hg (0.1 to 1.0). The main confounding factor responsible for attenuating the associations was maternal education. The effect sizes were reduced from the simple models to 0.9 mm Hg and 0.7 mm Hg for systolic and diastolic blood pressure, respectively, after control for this variable alone. Controlling for childhood BMI hardly altered effect estimates. The associations between breast-feeding and blood pressure did not vary by sex, BMI, or pulse (P for interaction all 
0.2).
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The inverse association between breast-feeding and blood pressure was seen in an analysis confined to mothers of manual socioeconomic background: the fully adjusted mean difference in systolic pressure was -1.3 mm Hg (-2.9 to 0.3), and the difference in diastolic pressure was -1.1 mm Hg (-2.3 to 0.1). There was no evidence of interaction by social status on systolic (P=0.7) or diastolic (P=0.4) blood pressure.
Breast-feeding was associated with lowered blood pressure when the analysis was restricted to mothers who either originally intended to breast-feed for the first 3 months (regression coefficient for breast-feeding minus formula-feeding, simple model: -2.5 mm Hg; 95% CI, -5.3 to 0.3; n=3044) or to formula-feed for the first 3 months (-1.6 mm Hg; -2.7 to -0.4; n=1194).
The association of breast-feeding with blood pressure was similar whether breast-feeding was partial or exclusive at 2 months of age but was greater among those who had been breast-fed for at least 6 months (Table 3). In fully adjusted models, there was a 0.2-mm Hg reduction (95% CI, 0.0 to 0.3; P=0.05) in systolic pressure for each 3 months of any breast-feeding. Breast-feeding duration was not associated with diastolic pressure (P for trend, 0.3).
The pattern and size of the relationships between breast-feeding and blood pressure were the same after additional adjustment for overcrowding, family income, number of older siblings, maternal alcohol consumption, child’s health, or child’s ethnicity (data not shown). These factors were therefore not included in the final model. In simple models, associations between breast-feeding and blood pressure were similar among those excluded from the main analysis because they lacked complete data (data not shown).
Influence of Postnatal Growth
Although weight gain between 6 weeks and 9 months of age was associated with later blood pressure in fully adjusted models (coefficient, 3.2 mm Hg per kg/mo; 95% CI, 1.0 to 5.5), there was no evidence that weight gain in infancy attenuated the association between breast-feeding and blood pressure. Among the 4538 subjects with data on infant weights, the difference in systolic blood pressure associated with breast-feeding was -0.7 mm Hg (95% CI, -1.5 to 0.0) in models controlling for social, economic, and maternal variables, birth weight, and childhood height. When weight gain in infancy was included in the model, the blood pressure difference was not altered (-0.7 mm Hg; 95% CI, -1.5 to 0.0).
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Discussion |
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Breast-feeding was associated with lower blood pressure at age 7 years in this contemporary cohort. The results are of current relevance because the comparison was with modern formula milks, which more closely reflect the composition of breast milk than earlier formulas, for example, with regard to sodium content.25
Limitations
Selection bias is possible, because the 59% (7276/12 289) of eligible children who were examined at age 7 years differed from nonparticipants with regard to breast-feeding rates, birth weight, and socioeconomic and maternal factors. This would affect our results only if the association differed between those who did and did not take part in the study, which seems unlikely. Some reassurance against selection bias among the final analytical sample, compared with all children with breast-feeding and blood pressure data, is provided by the similarity of the inverse breast-feeding–blood pressure association seen in those subjects without complete data who were excluded from the full analysis.
Breast-feeding mothers differed from those who formula-fed in various ways. A number of lines of evidence, however, argue against residual or unmeasured confounding. First, control for several socioeconomic factors or factors potentially on the biological pathway between social class and later blood pressure (such as maternal prepregnancy BMI) made only a modest difference to effect estimates, which remained statistically significant. Second, the association was observed when we restricted our analysis to only those mothers who were initially intending to breast-feed, strengthening the possibility that the breast-feeding effect is biological rather than being related to factors influencing both breast-feeding intent and later blood pressure. Third, we observed a protective effect of breast-feeding in analysis stratified by socioeconomic background.
Comparison With Other Studies
Our results in term infants concur with a randomized controlled trial in preterm infants. Compared with preterm formula, banked breast milk was associated with a 2.7-mm Hg reduction in systolic and a 3.2-mm Hg reduction in diastolic blood pressure in adolescence.2 At earlier follow-ups of the same trial, there was no evidence of a breast milk effect on blood pressure,15 suggesting that the influence of breast-feeding may increase with greater age.
Partial as well as exclusive breast-feeding lowered blood pressure, as in another prospective study.4 Our results are consistent with a retrospective cohort showing a decrease in blood pressure with increased breast-feeding duration.5 No relation between breast-feeding and blood pressure was observed in other studies, although these had some limitations, including small sample size,26 retrospective recall of infant feeding,9,12 74% loss to follow-up,10 and short duration of follow-up.13
Our estimate of the reduction in systolic blood pressure associated with breast-feeding is similar to the pooled estimate from a recent meta-analysis.27 The pooled difference was greater among small studies (n<300) than larger studies (n>1000), suggesting the possibility of publication bias. The present study, with more than 4500 subjects included in the analysis, is therefore an important addition to the literature.
Mechanisms
A number of mechanisms have been proposed. First, neonatal sodium restriction was associated with a 2-mm Hg reduction in blood pressure17 that persisted into adolescence.18 Differences in sodium ingestion between intervention and control groups were 3-fold.17 In contrast, mean sodium intakes were only 22% higher among formula-fed than breast-fed infants in 963 ALSPAC children 4 months of age (P. Emmett, University of Bristol, personal communication, 2003). It is possible that differences in sodium intake influence later blood pressure at a lower threshold than those achieved in the above trial17 or that longer-term salt intake among breast-fed children differs from that of formula-fed children. Salt ingestion may be a relevant mechanism in studies of children born before sodium in formula milk was reduced.28 A blood pressure–lowering effect of breast-feeding was independent of sodium intake among preterm infants,2 however, and other mechanisms have been suggested.
Second, breast milk contains long-chain polyunsaturated fatty acids (LCPUFAs), important structural components of tissue membrane systems, including the vascular endothelium. Supplementation of infant formula with LCPUFAs was associated with a 3.0-mm Hg reduction in blood pressure,29 suggesting that the LCPUFAs found in breast milk may play a role in blood pressure control.
Third, higher energy and protein intakes30 in bottle-fed compared with breast-fed infants may stimulate insulin secretion31–33 and promote insulin resistance34 that persists into adolescence35 and adulthood.10 Insulin resistance may, in turn, raise blood pressure via stimulation of the sympathetic nervous system, increased renal sodium retention, modulation of cation transport, and smooth muscle hypertrophy.36
Fourth, formula-fed infants are more likely to be overweight than breast-fed infants.6 Controlling for current BMI hardly altered effect estimates, suggesting that breast-feeding does not influence blood pressure via an effect on obesity. The association may reflect the effect of a healthier diet continued throughout childhood or influences on food preferences or taste thresholds for dietary constituents (such as salt or energy intake37), which are in turn related to blood pressure. We were unable to directly address this issue. The absence of confounding by BMI provides some evidence that differential energy imbalance during childhood is an unlikely explanation for the association.
Finally, accelerated postnatal weight gain is associated with raised blood pressure.22 Infants who are growing rapidly, perhaps after prenatal growth restraint, may be formula-fed because they demand more milk.21 The inverse breast-feeding–blood pressure association may be caused by factors related to postnatal growth, rather than being a biological effect of breast-feeding. We found that the association between breast-feeding and blood pressure was not altered by the pattern of infant growth.
Conclusions
Breast-feeding was associated with a 0.8-mm Hg reduction in systolic blood pressure at 7 years, an effect size similar to the blood pressure–lowering effects of salt restriction (-1.3 mm Hg) and exercise (-0.7 mm Hg) among normotensive adults.38 The inverse breast-feeding–blood pressure association may amplify with age,2 suggesting larger benefits in adulthood. Even this small reduction may have important population-health implications, because an increased mortality risk is observed across the blood pressure distribution and not just above threshold levels.39 A 1% reduction in population systolic blood pressure levels is associated with an 
1.5% reduction in all-cause mortality,39 equivalent to a lessening in premature mortality of 8000 and 2000 deaths per year in the United States and United Kingdom, respectively (based on number of US and UK all-cause deaths among men and women age 35 to 64 years).40,41 Approximately 40% of all infants are never breast-fed in the United States or United Kingdom.42,43 If breast-feeding promotion initiatives raised the prevalence of breast-feeding from 60% to 90%, 3000 extra deaths might be prevented among 35- to 64-year-olds per year in these 2 countries, and a similar level of additional excess deaths might occur if breast-feeding rates dropped from 60% to their levels in 1970 (25%42). Although these estimates should be interpreted with caution, because they are based on several assumptions, including causality, they suggest that the wider promotion of breast-feeding is a potential component of the public health strategy to reduce population levels of blood pressure.
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Acknowledgments |
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Dr Martin was supported by a Wellcome Trust Research Training Fellowship in Clinical Epidemiology. ALSPAC has received financial support from the Medical Research Council, the Wellcome Trust, the European Commission, the Department of Health, and the Department of the Environment. We are grateful to the parents and children who took part in the study and to the midwives for their help in recruitment. The ALSPAC study team comprises clinic staff, interviewers, computer technicians, laboratory technicians, clerical workers, research scientists, volunteers, and managers who continue to make the study possible. The ALSPAC study is part of the World Health Organization–initiated European Longitudinal Study of Parents and Children. Colin Steer extracted data for this analysis. Professor Jean Golding commented on earlier drafts.
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Footnotes |
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R.M.M. undertook the initial analysis, wrote the first draft of the paper, and coordinated completion of the paper. Ideas and concepts were frequently discussed between R.M.M., A.R.N., D.G., G.D.S., and P.E. during the writing of the paper, and all authors contributed to the final version. R.M.M. and A.R.N. will act as guarantors.
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References |
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K. K. Ong, P. M. Emmett, S. Noble, A. Ness, D. B. Dunger, and and the ALSPAC Study Team Dietary Energy Intake at the Age of 4 Months Predicts Postnatal Weight Gain and Childhood Body Mass Index Pediatrics, March 1, 2006; 117(3): e503 - e508. [Abstract] [Full Text] [PDF]
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S. Leary, A. Ness, P. Emmett, G. Davey Smith, and ALSPAC Study Team Maternal diet in pregnancy and offspring height, sitting height, and leg length J Epidemiol Community Health, June 1, 2005; 59(6): 467 - 472. [Abstract] [Full Text] [PDF]
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National High Blood Pressure Education Program Wor The Fourth Report on the Diagnosis, Evaluation, and Treatment of High Blood Pressure in Children and Adolescents Pediatrics, August 1, 2004; 114(2/S2): 555 - 576. [Full Text] [PDF]
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Journal Watch Arch. Dis. Child., July 1, 2004; 89(7): 689 - 690. [Full Text] [PDF]
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Minerva BMJ, March 27, 2004; 328(7442): 776 - 776. [Full Text] [PDF]
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