PEDIATRICS Vol. 119 No. 5 May 2007, pp. e1107-e1115 (doi:10.1542/peds.2006-2149)
ARTICLE |
The Effect of Breastfeeding on Cardiorespiratory Risk Factors in Adult Life
Division of Community Health Sciences, St George's, University of London, London, United Kingdom
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ABSTRACT |
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OBJECTIVE. Nutrition in the first weeks of life may program disease risk in adulthood. We examined the influence of initial infant feeding on cardiorespiratory risk factors in adulthood.
PATIENTS AND METHODS. A total of 9377 persons born during 1 week in 1958 in England, Scotland, and Wales were followed-up periodically from birth into adulthood. Infant feeding was recorded from a parental questionnaire at 7 years old as never breastfed, breastfed partially or wholly for <1 month, or breastfed for >1 month. Height; waist circumference; hip circumference; waist/hip ratio; body mass index; blood pressure; forced expiratory volume; total, high-density, and low-density lipoprotein cholesterol; triglycerides; hemoglobin A1c; fibrinogen; fibrin D-dimer; C-reactive protein; von Willebrand factor; and tissue plasminogen activator antigen were measured at 44 to 45 years of age.
RESULTS. Breastfeeding for >1 month was associated with reduced waist circumference, waist/hip ratio, von Willebrand factor, and lower odds of obesity compared with formula feeding after adjustment for birth weight, prepregnancy maternal weight, maternal smoking during pregnancy, socioeconomic position in childhood and adulthood, region of birth, gender, and current smoking status. Infant feeding status was not associated with other cardiorespiratory risk factors after adjustment, except for lower fibrinogen and C-reactive protein levels in women.
CONCLUSIONS. The inverse associations of breastfeeding for >1 month with measures of central obesity and inflammatory markers in the current study are small and of little public health importance. Although there was no substantial long-term protective effect of breastfeeding for >1 month on other cardiorespiratory risk factors in adult life, further studies with contemporaneous data on exclusive breastfeeding are needed to confirm these findings.
Key Words: breastfeeding • cardiovascular risk factors • respiratory risk factors • epidemiology
Abbreviations: FEV1—forced expiratory volume in 1 second • HbA1c—hemoglobin A1c • t-PA—tissue plasminogen activator antigen • vWF—von Willebrand factor • HDL—high-density lipoprotein cholesterol • LDL—low-density lipoprotein cholesterol • CRP—C-reactive protein • CI—confidence interval
Cardiorespiratory disorders are a major cause of death in later life in both the developed and developing world.1 It has been suggested that nutrition in the first weeks of life may program disease risk in adulthood.2 Any such effect is of considerable public health interest, because early infant feeding patterns are potentially modifiable. Breast milk has long been encouraged as the food of choice in infancy, based on numerous short- and long-term health benefits. Breastfeeding has been associated with an improved cardiovascular risk profile3–5 and fewer cardiovascular outcomes in later life (including ischemic heart disease and type 2 diabetes)6–8 compared with formula feeding. However, there is insufficient evidence to conclude whether breastfeeding is protective against cardiovascular mortality.9 It has also been suggested that initial breastfeeding may result in taller height10,11 and reduce the prevalence of obesity.12 However, the results of individual studies for this latter association have differed, showing either protective12 or null effects.13,14 Evidence that breastfeeding influences lung function and respiratory outcomes in later life has been limited and inconclusive.15
Recent systematic reviews have highlighted that publication bias (where smaller studies showing beneficial effects of breastfeeding on health outcome are preferentially published) and lack of adjustments for potentially important confounders are key concerns in establishing whether apparent associations between breastfeeding and health outcomes are causally related.16,17 It is also difficult to examine the long-term consistency of these associations, because few studies have contemporary measurement of infant feeding with follow-up in adult life. This study aims to examine the association between the mode of infant feeding and a range of established cardiorespiratory risk factors in adulthood in a large prospective cohort study, where data on infant feeding were ascertained in childhood and information on a large number of potentially important confounders were measured throughout the life course.
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METHODS |
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Study Design
Persons born in England, Scotland, and Wales during 1 week in March 1958 were recruited for a Perinatal Mortality Survey and have been followed up periodically from birth into adulthood (the British 1958 birth cohort). Participants were invited to a clinical examination by a trained research nurse visiting their home during 2002 to 2004, when cohort members were aged 44 to 45 years. From a target sample of 12069 persons, 9377 (78%) were visited in their home by a team of 122 specially trained nurses from the National Centre for Social Research, who conduct the annual health surveys of England and Scotland.
Infant feeding was recalled by parents (usually the mother) when the child was 7 years of age into 1 of 4 categories: breastfed wholly or partially for >1 month, <1 month, not at all, and unknown. The following were identified as potentially important confounders: region of birth, prepregnancy maternal body size, maternal smoking during pregnancy, birth weight, and socioeconomic position in childhood and adulthood.10,13,17–21 Region of birth, prepregnancy maternal body size, maternal smoking during pregnancy, and birth weight were obtained from the 1958 Perinatal Mortality Survey. Socioeconomic position in childhood was based on father's occupation in 1958 or at 7 years of age if data were unavailable at birth; adult social class was based on the participant's current or most recent occupation at 42 years (or 33 years, if missing). Current smoking status (at 42 years) was defined as never smoker, ex-smoker, or current smoker. Social position and smoking status in adulthood are considered as potential later-life confounders, because they are important predictors of cardiorespiratory risk and are related to infant feeding status in this cohort.
Measurements and Assays in Adulthood
Standing height (measured using a Leicester portable stadiometer [Child Growth Organization, London, United Kingdom]), waist, and hip circumference were measured to the nearest millimeter. Weight was measured to the nearest 0.1 kg in light clothing with shoes removed. BMI was determined as kilograms per meter squared. Blood pressure and pulse rate were measured 3 times (mean used for analyses) in the seated position after a period of 5 minutes of rest using the Omron 705CP automated sphygmomanometer (Omron, Tokyo, Japan), with a large cuff for subjects with a mid-upper arm circumference of 
32 cm. Spirometry was performed in the standing position without nose clips, using the Vitalograph Micro spirometer (Vitalograph Ltd, Buckingham, England). Forced expiratory volume in 1 second (FEV1) was standardized for current height.
Nonfasting venous blood samples were drawn into Sarstedt (Leicester, United Kingdom) polypropylene tubes containing citrate anticoagulant (for measurement of glycosylated hemoglobin [HbA1c], fibrinogen, tissue plasminogen activator antigen [t-PA], and von Willebrand factor [vWF] antigen) and no anticoagulant (for measurement of total cholesterol and high-density lipoprotein (HDL) cholesterol and triglycerides). Total and HDL cholesterol were measured by autoanalyzer, and low-density lipoprotein (LDL) cholesterol levels were derived by algorithm. Fibrinogen was determined by the Clauss method22 (MDA 180 coagulometer; Biomerieux, Basingstoke, United Kingdom). Fibrin D-dimer was measured by ELISA assay (Hyphen, Paris, France). C-reactive protein (CRP) was measured by high-sensitivity nephelometric analysis of latex particles coated with CRP monoclonal antibodies (BN ProSpec protein analyzer; Dade Behring, Marburg, Germany). T-PA and vWF were measured by ELISA assay using a double antibody sandwich (from Biopool, Umea, Sweden, and DAKO, Copenhagen, Denmark, respectively). Written informed consent was obtained from all of the study participants. Ethical approval for the medical examination at 44 to 45 years was obtained from the South East Multicenter Research and Ethnics Committee (ref: 01/1/44).
Statistical Analysis
Waist circumference, hip circumference, waist/hip ratio, HDL cholesterol, triglycerides, HbA1c, fibrinogen, D-dimer, CRP, t-PA, and vWF were log transformed to normalize their distributions. The association between each risk factor and infant feeding status was investigated using a test for trend across all of the infant feeding groups ignoring the group with the unknown infant feeding status. Linear regression was used to compare those breastfed for <1 month and >1 month with those not breastfed at all with adjustment for region of birth, prepregnancy maternal body size, maternal smoking during pregnancy, birth weight, socioeconomic position in childhood and adulthood, smoking in adulthood, and gender. Those with missing data on confounders were included as a separate category in the analyses. Based on previous findings of gender differences in the association between infant feeding and cardiovascular risk,23,24 regression models were extended to test for an interaction between infant feeding status and gender. Parallel analyses were undertaken using logistic regression to examine the relation between the odds of obesity (individuals with BMI 30 kg/m2) and duration of breastfeeding. Differences between the infant feeding groups for the outcomes that were log transformed are reported as percentage differences rather than absolute differences on the log scale. All of the regression analyses included additional adjustment for factors contributing to measurement error of the cardiorespiratory risk factors, such as nurse and instrument effects and laboratory batch; these nuisance factors are specified for each outcome in the results. All of the analyses were performed using Stata 9.2 (Stata Corp, College Station, TX).
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RESULTS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Of the 9377 subjects who participated in the clinical examination at 44 to 45 years, infant feeding status was available for 8172 (87%); the remainder are shown in Table 1 as "unknown" infant feeding status and are excluded from all of the regression analyses. Of those with data on infant feeding, 46% (n = 3772) were breastfed for >1 month, 24% (n = 1960) were breastfed for <1 month, and 30% (n = 2440) were not breastfed at all. Before adjustment, increasing the duration of breastfeeding showed a strong positive linear association with adult height and HDL cholesterol and an inverse trend with BMI, obesity, waist circumference, waist/hip ratio, fibrinogen, D-dimer, CRP, t-PA, and vWF. Duration of breastfeeding showed a weak inverse association with hip circumference (P for trend = .06), triglycerides (P = .06), and HbA1c (P = .08). Infant feeding status was not associated with blood pressure (systolic or diastolic), total or LDL cholesterol, or height-adjusted FEV1 (Table 1).
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There was no difference in the proportion of men (46%) or women (46%) breastfed for more than 1 month. Breastfeeding was more common in higher social classes (similar patterns were observed by childhood and adulthood social economic status) and in the southern part of England compared with northern regions, Wales, or Scotland (Table 2). Mothers who did not smoke during pregnancy were more likely to breastfeed for >1 month (50% compared with 40% of medium smokers and 37% of heavy smokers among those with data on infant feeding). Mothers with relatively lower prepregnancy body size were also more likely to breastfeed. Subjects with higher birth weight were more likely to have been breastfed. Adult current smokers were less likely to have been breastfed for >1 month compared with never-smokers (42% versus 46% among those with data on infant feeding).
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After adjustment for the confounders mentioned above, the apparent beneficial effect of breastfeeding over formula feeding on cardiorespiratory risk factors was attenuated (Table 3). However, being breastfed for >1 month, compared with formula feeding, was still associated with decreased waist circumference (–0.81%; 95% confidence interval [CI]: –1.47% to –0.14%), waist/hip ratio (–0.54%; 95% CI: –0.92% to –0.16%), reduced risk of obesity (relative risk: 0.85; 95% CI: 0.75 to 0.97), and lower levels of fibrinogen (–1.43%; 95% CI: –2.55% to –0.30%), vWF (–2.15%; 95% CI: –4.01% to –0.26%), and marginally lower t-PA (–2.75%; 95% CI: –5.54% to 0.11%), all showing statistically significant inverse trends across known feeding groups (Ps from .004 to .05).
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There was no evidence of an interaction between breastfeeding and gender for any risk factor except for fibrinogen and CRP (interaction P = .05 and .02, respectively). The association of fibrinogen and CRP with breastfeeding seemed to be restricted to women, with no appreciable effect in men. In women, after adjustment, fibrinogen levels were 2.6% lower (95% CI: 4.6% to 1.0% lower; P = .003) in those breastfed for >1 month compared with those not breastfed, and CRP levels were 12.8% lower (95% CI: 21.5% to 3.0% lower; P = .01).
To examine whether the inverse association between breastfeeding and waist circumference, waist/hip ratio, obesity, and the inflammatory makers might be explained by residual confounding, a number of additional factors related to childhood social and cultural environment were identified and adjusted for, including maternal age, level of paternal education, and number of people per household. Adult smoking status was further refined by taking account of the number of cigarettes smoked. Inclusion of these factors in the regression model did not materially alter the findings (data not presented). Current smoking is a strong predictor of the levels of fibrinogen, CRP, and vWF, with smokers having higher levels than former- or never-smokers. Restricting the analyses to former- or never-smokers did not markedly change the results; in women, fibrinogen levels were 1.9% lower and CRP levels 13.6% lower with breastfeeding for >1 month compared with formula feeding. For both men and women, vWF was 2.0% lower and 1.3% lower with breastfeeding for <1 month and >1 month, respectively, compared with formula feeding.
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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In our study, individuals breastfed for >1 month were, on average, taller in adulthood; had lower BMI, waist and hip circumference, waist/hip ratio, total and LDL cholesterol, triglycerides, HbA1c, fibrinogen, t-PA, vWF; were less likely to be obese; and higher blood pressure, FEV1, and HDL cholesterol compared with those who were not breastfed. Those breastfed for <1 month tended to have levels between these 2 groups. The inverse association of breastfeeding duration on established cardiovascular risk factors was attenuated after adjustment for confounding factors. However, the associations with waist circumference (0.8% lower), waist/hip ratio (0.5% lower), obesity (15% lower odds), fibrinogen (3% lower in women), CRP (13% lower in women), t-PA (3% lower), and vWF (2% lower) remained statistically significant after adjustment.
The graded effect across the 3 feeding groups on adult height was markedly reduced after adjustment. This agrees with previous work10,18,25 that has shown no association between infant feeding and attained height in adulthood. A recent meta-analysis found a small effect of breastfeeding on BMI, but this effect was attenuated to the null after adjustment for potentially important confounders (socioeconomic status, maternal smoking, and BMI in early life).19 Similarly, findings from the current study found no association between infant feeding and adult BMI after adjustment. Reports of an association between breastfeeding and obesity in adulthood vary.10,13,25,26 We found the odds of obesity (individuals with BMI 30 kg/m2) to be 15% lower in those breastfed for >1 month compared with those formula fed (adjusted odds ratio: 0.85; 95% CI: 0.75 to 0.97). Our result is similar to findings reported on the same cohort earlier in adulthood13 and agrees with a systematic review reporting a small effect of breastfeeding on the odds of obesity after adjustment (adjusted odds ratio: 0.93; 95% CI: 0.88 to 0.99).17 The prevalence of exclusive formula feeding is approximately one third in Europe and the United States and agrees with the prevalence of not being breastfed in the current study (30%). Therefore, a 15% reduction in obesity could equate to approximately a 4% reduction in the burden of obesity if all mothers were to breastfeed. Based on observational evidence, the relative risk of coronary heart disease27–31 or cardiovascular disease27 outcomes in obese versus nonobese individuals is 
1.5 to 2.0, and for diabetes the relative risk is 2.6.27 Hence, in the current study, where 28% of those formula fed were obese, the effect of being universally breastfed would result in a <2.5% reduction in the incidence of coronary heart disease, cardiovascular disease, or diabetic outcomes. These effects are small and of limited public health importance.
The inverse association of breastfeeding with waist circumference and waist/hip ratio after adjustment is novel and may imply a possible protective effect of breastfeeding on measures of central obesity. It has been suggested that rate of growth in infancy is related to obesity in childhood and that breastfed infants exhibit slower growth rates than formula-fed infants, which results in lower obesity32 and improved insulin resistance in later life.4 Although insulin resistance, which is related to central obesity, was not associated with breastfeeding in a study of middle-aged men,25 a meta-analysis of studies found that those breastfed have a lower risk of type 2 diabetes in later life (odds ratio: 0.61; 95% CI: 0.44 to 0.85) compared with those fed formula.33 Among those without diabetes, those who had been breastfed had lower fasting insulin levels but no difference in fasting glucose levels compared with those fed formula.33 HbA1c levels, which are used as a measure of blood glucose levels over the past 60 days, did not exhibit any appreciable difference between the infant feeding groups in the current study. Central obesity is an important risk factor for cardiovascular disease, insulin resistance, and diabetes,28,34–37 and the risk of cardiovascular disease increases by 30% to 60% comparing the top and bottom quintiles or quartiles of waist circumference in men and women and almost a doubling of risk for a similar difference in waist/hip ratio.28,30,31,38 A similar increase in waist/hip ratio or waist circumference has been found to approximately double the risk of type 2 diabetes.39 These associations are manifest by approximately a 10% to 15% variation in waist circumference or waist/hip ratio. In the current study, those breastfed for >1 month had reduced waist circumference or waist/hip ratio by <1%. Therefore, the potential protective effect of breastfeeding for >1 month on cardiovascular disease and diabetes via any effect on waist circumference or waist/hip ratio is vanishingly small.
The absence of an association with blood pressure is in agreement with 2 systematic reviews16,40 that found no effect in larger studies (with 1000 participants). Evidence of small study bias was observed in these reviews, indicating the presence of publication bias. The authors concluded that the pooled association between breastfeeding and systolic blood pressure may have been exaggerated by large effects reported in smaller studies. Although this study excludes any important lowering effect of breastfeeding on blood pressure, it can not rule out that prolonged exclusive breastfeeding may have a protective effect.41 Studies with follow-up in childhood and adolescence have shown a dose-response relationship between duration of exclusive breastfeeding (rather than mixed feeding) and systolic blood pressure42,43; whether this effect persists into adulthood remains unclear.25 In the current study it was not possible to examine exclusivity of breastfeeding or duration of breastfeeding beyond 1 month.
The lack of an association between lipids and breastfeeding after adjustment disagrees with a meta-analysis that found total and LDL cholesterol levels to be 0.2 mmol/L lower in those breastfed.5 However, it has been suggested that the beneficial effect on lipids requires exclusive breastfeeding for >3 months,44 and it was not possible to examine this in the current study. In agreement with a previous study, we did not find any beneficial effect of breastfeeding on lung function.15
The graded inverse association between breastfeeding and levels of inflammatory markers in the current study was attenuated by adjustment for potential confounders but remained statistically significant for fibrinogen and vWF and marginally significant for t-PA. The differential effect of breastfeeding on fibrinogen and CRP between men and women, with stronger inverse associations in women, was unexpected and may be a chance finding (interaction P = .05 and .02, respectively). The only other study examining fibrinogen levels in adulthood and breastfeeding did not find an association,25 but infant feeding was recalled in adulthood (some 50 years after birth), and the authors acknowledged that selection and recall bias may have affected their results. A long-term follow-up of preterm births that were randomly assigned to breast milk or formula feed exhibited lower levels of CRP in adolescence,45 and lower levels of CRP were found in women (but not men) breastfed for longer durations.21 A lower level of vWF in both men and women in those breast compared with formula feeding is a novel finding. The magnitude of the associations between duration of breastfeeding and levels of the inflammatory markers was not materially altered after exclusion of current smokers, but any potential influence of infant feeding on coronary heart disease incidence is likely to be small.46–49
Prolonged and exclusive breastfeeding has been associated with improved neurocognitive development.50–55 Because socioeconomic status is related to both cognition and health status, adjustment for markers of adult socioeconomic position may not be appropriate, because this may lie on the causal pathway. Although it was only the association of infant feeding with BMI, waist circumference, and waist/hip ratio that were marginally strengthened without adjustment for socioeconomic status, the potential effects of mode of early feeding on cardiovascular27,29,31,37 or diabetic39 outcomes are still modest (<3%) and remain of limited public health importance.
A potential weakness of the current study was that breastfeeding status was not reported as being exclusive and was recalled after 7 years by parental interview. Approximately half of the mothers (46%) reported breastfeeding wholly or partly for >1 month in this study, which agrees well with a report in a specific region of England at this time, where 54% had breastfed for 1 month.56 In terms of the validity of recalling infant feeding status, this has been shown to be accurate 
20 years after birth.57 Although no information on the exclusivity of breastfeeding in the United Kingdom at this time could be found, formula feeding in the late 1950s and early 1960 would probably have consisted of dried cow's milk fortified with iron and vitamins.58 Although the content of formula milk has evolved since this time,59 we believe that our findings would not be materially changed by the introduction of modern formulae in more contemporary cohorts. The British 1958 birth cohort is predominantly white (97%); hence, it was not possible to examine racial differences in the association between infant feeding patterns and cardiorespiratory risk in adult life.
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CONCLUSIONS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Breastfeeding is beneficial for many other reasons, but breastfeeding for >1 month is unlikely to offer substantial protection against cardiorespiratory disease in adult life. The association between breastfeeding and waist circumference, waist/hip ratio, and obesity is of interest and needs to be replicated by other studies that have information on exclusive breastfeeding for longer durations (>1 month). Breastfeeding is associated with early life social environment, which influences adult behavior and lifestyle, and it is important that such confounders operating across the life course are identified and taken into consideration when examining the association between infant feeding and cardiorespiratory outcomes in later life. Although the potential effect of mode of early feeding on inflammatory markers maybe of limited relevance to cardiovascular outcomes, it may be of relevance to other disease mechanisms.
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ACKNOWLEDGMENTS |
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The medical examination in adulthood and related statistical analyses were funded by Medical Research Council grant G0000934, awarded under the Health of the Public initiative. The Medical Research Council played no role in study design, collection, analysis and interpretation of data, writing the report, or submitting the article for publication. Dr Rudnicka was funded by the Medical Research Council (grant no. G0000934). Dr Owen was supported by the British Heart Foundation (grant no. PG/04/072).
We thank the cohort members for their participation in this study and the nurses for performing the measurements in the field. We are grateful to Dr Ian Gibb and his staff at the Department of Clinical Biochemistry Newcastle on Tyne Hospitals National Health Service Trust, and to Prof Gordon Lowe and Anne Rumley at the Department of Medicine, Glasgow Royal Infirmary University National Health Service Trust, Glasgow, United Kingdom, for performing the assays.
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FOOTNOTES |
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Accepted Nov 16, 2006.
Address correspondence to Alicja R. Rudnicka, PhD, Division of Community Health Sciences, St George's, University of London, Cranmer Terrace, London SW17 0RE, United Kingdom. E-mail: arudnick{at}sgul.ac.uk
The authors have indicated they have no financial relationships relevant to this article to disclose.
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