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PEDIATRICS Vol. 111 No. 5 May 2003, pp. 1081-1089

REVIEW ARTICLE

Birth Weight and Blood Cholesterol Level: A Study in Adolescents and Systematic Review

Christopher G. Owen, PhD, Peter H. Whincup, FFPHM, Katherine Odoki, MRCP, Julie A. Gilg, PhD and Derek G. Cook, PhD

From the Department of Public Health Sciences, St George’s Hospital Medical School, London, United Kingdom

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   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Objective. To examine the relationship between birth weight and blood total cholesterol (TC) and to compare its strength with that of the relationship between current body mass index and TC.

Methods. 1) Cross-sectional study of adolescents, with retrospective ascertainment of birth weight from birth records or parental recall; 2) systematic review of studies examining the relations between birth weight and cholesterol at all ages.

Participants. 1) 1532 individuals (92% white, 55% male) in 10 British towns; 2) 28 studies with 32 observations showing the change in TC per 1 kg increase in birth weight—6 in infancy, 14 in adolescents, 12 in adults.

Results. In the cross-sectional study, there was a weak inverse relation between birth weight and TC level (-.061 mmol/L fall in TC per kg increase in birth weight, 95% confidence interval -.131 to .008 mmol/L per kg) which was little affected by adjustment for current body size. The difference in TC corresponding to an interquartile range increase in birth weight (-.03 mmol/L) was approximately a quarter of that for an equivalent increase in body mass index (.11 mmol/L). In the systematic review, an inverse association between birth weight and TC of a similar size to that in the cross-sectional study was observed (-.048 mmol/L per kg, 95% confidence interval -.078 to -.018 mmol/L per kg) similar in strength at all ages.

Conclusion. The relation of fetal nutrition to TC appears to be weak and is probably of limited public health importance when compared with the effects of childhood obesity.

Key Words: birth weight • blood cholesterol • systematic review

Abbreviations: CHD, coronary heart disease • TC, total cholesterol • BMI, body mass index • SE, standard error • SD, standard deviation • CI, confidence interval


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The observation that low birth weight is associated with coronary heart disease (CHD) in adult life has led to the suggestion that fetal undernutrition is an important coronary risk factor.1 In adult life, blood pressure and blood total cholesterol (TC) are powerful determinants of CHD risk;2–4 together with cigarette smoking they account for most of individual variation in CHD risk.5,6 Therefore, it is important to establish whether low birth weight is related to later blood pressure and TC level. Although the relation between birth weight and blood pressure has been reviewed in detail,7,8 the extent to which birth weight is related to TC level has been less clearly resolved. The results of some studies, particularly historical cohort studies, have suggested that low birth weight is related to higher TC levels,9–11 but this has not been the case in all.12 Other studies have suggested that other measures of size at birth (such as crown-heel length13 and abdominal circumference14) may be more important. Studies examining the relation between birth weight and blood cholesterol in contemporary children and adolescents may be of particular interest in defining the continuing public health relevance of the fetal origins hypothesis.15

Therefore, we have examined the relationships between birth weight (and other measures of size at birth) and TC in a large cross-sectional survey of 13 to 16 year olds (the Ten Towns Heart Health Study) and conducted a systematic review of all published studies, quantifying the relations between birth weight and blood cholesterol at all ages, to place our findings in context. To compare the importance of fetal nutrition as an influence on blood cholesterol with that of later obesity, we have compared the strength of relations between size at birth and blood cholesterol with those for current body mass index (BMI) in our own cross-sectional study.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Cross-Sectional Study of 13- to 16-Year-Olds
In the third phase of the Ten Towns Heart Health Study, we examined the cardiovascular risk profile of children 13 to 16 years old in 10 British towns in 1998–1999.16,17 A total of 69 state secondary schools were recruited, corresponding to the random sample of 100 primary schools included in earlier phases. An average of 58 pupils per school (45 of whom had taken part in the previous Ten Towns Studies, 13 randomly selected from the same classes) were invited. Ethical approval was obtained from all relevant local research ethics committees. Written parental and pupil consent was sought for all participants, using reminders where necessary. Preliminary visits were made to all schools by research team members to encourage participation. Measurements were made by a trained field team (4 observers) who visited all schools in the 10 towns, alternating between areas of high and low cardiovascular mortality. Children were examined in light clothing without shoes. Height was measured to the last complete millimeter with a portable stadiometer (CMS Ltd, Camden, United Kingdom), weight was measured to the last complete .1 kg with a digital electronic weighing scale (Soehnle Ltd, Murrhardt, Germany). Pubertal status was ascertained using a confidential self-assessment questionnaire based on Tanner pubic hair, penile, and breast development scales.18 Ethnicity was defined by the research team based on appearance cross-checked with surname (European, Asian, other). A venous blood sample was collected after an overnight fast. Blood samples were frozen (-20°C) within 6 hours of collection and transferred to a central laboratory for analysis within 2 weeks of collection. Total serum cholesterol (mmol/L) was measured using a Hitachi 747 automated analyser (Roche Diagnostics, Indianapolis, IN) at the Royal Free Hospital.19,20 A parental questionnaire (with reply-paid postage), sent immediately after examination, provided information on the child’s birth weight, length of gestation (whether born on time, early, or late and if so by how many weeks), number of older siblings, and on their own occupation(s), which was coded in accordance with the Registrar General’s (Office for National Statistics, United Kingdom) 1990 social class coding manual.21 Head of household’s social class was defined as paternal social class or (where not available) maternal social class. Parents were asked to give permission for the collection of information from birth records, which was sought for all children born at hospitals in or close to the town where they were surveyed. Data collected included birth weight, crown-heel length at birth, and head circumference. In subjects with birth weight data from >1 source, data were taken in order of preference from 1) birth record data; 2) birth registers; and 3) from parental recall (questionnaire data).

Statistical Analysis of Cross-Sectional Study in 13 to 16 Year Olds
Statistical analysis was performed using Intercooled STATA 7.0 for Windows software (Stata Corporation, College Station, TX). TC was normally distributed. Data on sex (2 levels), town (10 levels), ethnicity (3 levels), gestation (6 levels), multiple births (2 levels), maternal smoking during pregnancy (2 levels), parental social class (6 levels), and infant feeding (breast only, bottle only, mixed) were treated as categorical variables. Tanner scale pubic hair development (5 levels),18 breastfeeding duration (3- to 6-month durations—to minimize the effects of imprecise recall), and number of older siblings (4 levels—1, 2, 3, 4 or more) were treated as scores. Birth weight (kg), ponderal index at birth (kg/m3), gestation (weeks), age (years), cholesterol (mmol/L), and measures of current body size (height and BMI) were treated as continuous variables or grouped in fifths where appropriate. BMI (kg/m2) was used as a measure of weight-for-height because of its relative independence of height within the narrow age range in this population, and compared with other indices of body stature (eg, weight-for-height and ponderal index). Ponderal index was used as a measure of thinness at birth.22,23 Associations between TC and birth weight (also ponderal index at birth) were studied using multiple linear regression models within STATA (XI; REG command), taking account of possible sex differences in the relations between age, height, BMI, and cholesterol.

Systematic Review
A systematic review was conducted of published papers, letters, abstracts, and review articles using Embase, Medline, and Web of Science databases. All references concerning the effects of birth weight on cholesterol were identified using a combined text word and MESH heading (for Medline only) search strategy of birth weight (birth weight, birthweight, intrauterine growth retardation, fetal growth retardation), and cholesterol (cholesterol, lipoproteins, or lipids). The review was restricted to studies written in English and conducted on human subjects. The search (completed in August 2001) yielded 1048 references; abstract review suggested that 99 were potentially relevant and an additional 4 references were identified from other sources.9,24–26 Papers were considered relevant if the abstract indicated (or stated) that cholesterol had been measured in different birth weight groups or that regression had been performed between cholesterol and birth weight. From these 103 papers, 56 studies measuring birth weight and cholesterol were identified. Regression coefficients (presenting the difference in TC for a 1-kg rise in birth weight) and standard errors (SEs) were sought for all studies, adjusted first for age and sex (if appropriate), and then in addition for current height and BMI (data for children and adults only); sex-specific analyses were also sought. In studies including different ethnic groups, additional adjustment for ethnicity was sought.27,28 Information was obtained from 5 published study reports directly (with various levels of adjustment—see Table 4). An attempt was made to trace and contact the authors of all studies (including the remaining 49 studies) to request the results of these analyses; investigators were invited to provide raw data if they preferred to do so. Thirty-six authors were contacted and regression coefficients obtained for 22 studies. In all, regression coefficients were thus obtained for 27 of the 56 studies—23 of 41 (56%) of those published in 1990 or later, 4 of 15 (27%) of those published before 1990.29–32


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  		TABLE 4. Studies Included in the Meta-Analysis for Males and Females Combined

 
Statistical Analysis of Systematic Review
A meta-analysis of the relationship between birth weight and cholesterol was conducted. The regression coefficient for cholesterol associated with a 1-kg increase in birth weight and its associated SE was analyzed. Two papers contained raw data allowing regression coefficients (and SE) to be calculated directly.29,30 In 1 study,31 the SE had to be derived based on the t value. In another paper,32 mean TC (and standard deviation [SD]) was given for 5 birth weight groups (along with mean birth weight in each group). A regression coefficient was calculated (weighted by the inverse of the variance in cholesterol) using the weighted XI:REG command in STATA. In 3 studies,11,33,34 regression coefficients (and SE) were derived from the correlation coefficient, number in the study, SD of cholesterol, and birth weight for the population from which the correlation coefficient was derived. However, regression coefficients were replaced by the provision of data in 2 of these studies.11,33 A test for heterogeneity of regression coefficients between studies was conducted using Woolf’s {chi}2 test. Because there was statistically significant (P < .001) heterogeneity between studies, a random effect pooled estimate was used (using the META command in STATA). Possible publication bias was assessed using funnel plots, which examined the relationship between sample size and regression coefficients.35 In addition, Begg36 and Egger37 tests were performed using the METABIAS command within STATA. Differences in regression coefficients between age groups (infants at birth, children 4–16 years of age, adults >16 years of age), and between males and females were explored using the METAREG command.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Cross-Sectional Study of 13- to 16-Year-Olds
In all, 2451 subjects were invited for full measurements of whom 1635 (67%) participated, and 1532 (63%) provided blood samples, of which 1376 were fasting. The mean age of participants was 15.1 years; 842 (55%) were males. Mean TC was 4.11 mmol/L (SD .69) in boys and 4.36 (SD .74) in girls (P < .001 for sex difference). Birth weight data were available for 1461 (95%) of the 1532 individuals (64% of these from birth records, 7% from birth registers, and 29% from parental recall). Mean birth weight was 3.31 kg (SD .53 kg); the prevalence of low birth weight (<2.5 kg) was 6%. Since nonfasting TC levels were similar to fasting levels, the results for nonfasting subjects have been included; exclusion of these subjects made no difference to the results presented. Low-density lipoprotein showed similar patterns to TC throughout (data not shown).

Age, Body Build, Maturation, and Cholesterol (Table 1)
TC fell with increasing age in boys but was unrelated to age in girls; a test for sex interaction was statistically significant (P = .012). TC fell with increasing height and rose with increasing BMI in both sexes. Pubertal status was inversely related to TC in boys and to a lesser extent in girls, although there was no strong evidence of sex interaction (P = .100). Social class, ethnic group, and town (data not shown) showed no consistent relation with TC level. However, all subsequent regression models have been standardized for age, sex (when males and females were combined), town, and ethnicity.


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  		TABLE 1. Current Determinants of TC (mmol/L) at 13 to 16 Years of Age

 
Birth Weight, Gestational Age, and Blood Cholesterol (Table 2)
Birth weight and gestational age were correlated both in boys (r = .59) and in girls (r = .52). Weak inverse associations between birth weight and cholesterol were observed (-.061 mmol/L fall in TC per kg rise in birth weight, 95% confidence interval [CI] -.131 to .008 mmol/L per kg), which were not statistically significant. There was no evidence that the relationship between birth weight and cholesterol differed between fifths of current BMI (test for interaction in boys P = .863, girls P = .688, both P = .557). Length of gestation showed no relation with TC either in boys or girls; adjustment for gestational age had no effect on the birth weight-cholesterol associations observed. Other measures of size at birth, particularly length at birth and ponderal index at birth, showed no relation with TC either for males or females (data not shown).


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  		TABLE 2. Early Life Influences on TC (mmol/L)

 
Birth Weight and Blood Cholesterol: Further Analyses (Table 3)
Since the relation between birth weight and cholesterol was similar in boys and girls, more complex analyses examining the effect of adjustment for body build and maturation were conducted in both sexes combined, but including a term for the difference in the age-cholesterol relationship between the sexes. The relation between birth weight and TC was weakened by adjustment for height but strengthened by adjustment for current obesity (BMI). However, adjustment for both factors together, with or without pubertal status, made little overall difference. Additional adjustment for gestational age, multiple births, number of older siblings, type of infant feeding, and maternal smoking during pregnancy (data not shown) made little difference to the regression coefficient, and merely reduced the number of observations. Similar adjustments to the relation between gestational age and cholesterol level had no effect on the results observed.


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  		TABLE 3. Difference in TC (mmol/L) (SE and P Value) Associated With a 1-kg Increase in Birth Weight

 
Comparison of the Strength of Associations Between Birth Weight and Current BMI on TC
The difference in TC observed for a 1 interquartile increase in birth weight (from 3.03–3.65 kg) and for a 1 interquartile increase in BMI (from 18–22 kg/m2) were compared, using a model with town, age, body mass, and ethnic group. The corresponding differences in TC were -.03 mmol/L (95% CI -.08 to .01, P = .132) and .11 mmol/L (95% CI .07-.16, P < .001), respectively.

Systematic Review of the Effect of Birth Weight on TC
From the 28 studies (including the Ten Towns Health Heart Study) with data on the effect of birth weight on TC, 32 regression coefficients were derived for both sexes (Table 4), 29 for males and females separately (data not shown). Six observations were in infants, 14 in children (4–16 years), and 12 in adults. There was evidence of marked heterogeneity between studies ({chi}231 = 68.1, P < .001), although there was no consistent difference between sexes (P = .657) or between the 3 age groups (P = .565). Twenty-one regression coefficients showed an inverse association between birth weight and cholesterol (11 having 95% CIs bridging the line of no difference), whereas 11 showed a positive association with CIs including the line of no effect (Fig 1). In a random effects model including all studies, each 1-kg increase in birth weight was associated with a -.048 mmol/L decrease (95% CI -.078 to -.018) in TC. The association was slightly weaker when studies of infants were omitted (Table 4). Further adjustment for current height and BMI made little difference to the meta-analysis (Table 4). The exclusion of 2 case-control studies38,39 (restricting results to cross-sectional and cohort studies) made little difference to the meta-analysis. Funnel plots plotting the regression coefficient against the sample size of each study provided no evidence of publication or inclusion bias; in particular, there was no evidence that small studies had only been published when they reported large associations between birth weight and cholesterol (data not shown). Formal Begg and Egger tests for publication bias were not statistically significant. Restriction of the main analysis to studies based on >500 subjects provided a random effects model estimate of -.055 mmol/L decrease per kg increase in birth weight (95% CI -.082 to -.028 mmol/L), similar to that obtained for all studies.



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  		Fig 1. Regression coefficients for the change in TC (mmol/L) and 95% CI (horizontal lines) per 1-kg rise in birth weight for both males and females. The box area of each study is proportional to the inverse of the variance. Study author indicated on the Y axis in ascending order of age (mean age shown in parenthesis). Combined estimate based on a random effects model shown by dashed vertical line and diamond (95% CI).

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In our study of contemporary adolescents aged 13 to 16 years, a weak inverse association between birth weight and serum TC was found, of marginal statistical significance, which was little affected by additional adjustment for body size and maturation. A systematic review and meta-analysis of published and unpublished data showed a similarly weak inverse association between birth weight and TC, which was too small to be considered of public health importance. The weakness of the association between birth weight and blood cholesterol was emphasized by comparison with the strength of the relation between current BMI and blood cholesterol in our study, which was almost 4 times stronger.

Our cross-sectional study was among the largest examining the relationship between birth weight and cholesterol and had considerable statistical power, reliably excluding a fall of .15 mmol/L in blood cholesterol per kg increase in birth weight. The upper confidence value from the systematic review was even tighter (.1 mmol/L), ruling out any important effect of birth weight on cholesterol. Although the response rate in the cross-sectional study was only moderate, mean TC levels were comparable with those in a contemporary group of British children aged 11 to 14 years;40 mean birth weight and the prevalence of low birth weight were also comparable with those of earlier British studies.41,42 The weakness of the association between birth weight and blood cholesterol is not likely to reflect imprecise or biased ascertainment of birth weights, since most were recorded directly from birth records or from a parental questionnaire in which the accuracy of parental birth weight recall has already been established.43 The absence of any consistent relationship between blood lipids and social class in this population suggests that selection bias is unlikely to affect the birth weight-blood cholesterol relationship markedly. Even though there has been considerable interest in the importance of current body size in influencing the relationship between birth size and cardiovascular risk,44,45 the relationship between birth weight and cholesterol in adolescence, although increased in strength by adjustment for BMI, was little affected by combined adjustment for BMI and height.

The systematic review of the relationship between birth weight and blood cholesterol level was based on all reports identified by a systematic search of Medline, Embase, and Web of Science databases, supplemented by citations from other sources. Since regression coefficients could only be extracted directly from a few papers, requests for data were made to many study authors, which were successful in about half of the cases. Funnel and Begg-Egger plots provided no consistent evidence of publication bias. The resulting meta-analysis reliably excludes an effect of public health importance; any publication bias is likely to have strengthened rather than weakened the observed effect. Since the assessment of birth weight in all studies was based either on direct assessment in infancy or retrospectively from birth records, marked imprecision or bias in the ascertainment of birth weight can be discounted (Table 4). The relationship between birth weight and cholesterol was not materially altered by adjustment for current body size (height, BMI, or weight), in contrast with earlier reports on other cardiovascular risk factors, particularly blood pressure.7,8 The relationship between birth weight and cholesterol appeared reasonably consistent across all age groups, providing no evidence of amplification, as postulated to occur with blood pressure.46

It remains possible that birth weight is not the marker of size at birth most strongly related to blood cholesterol; earlier studies have suggested that birth length and abdominal circumference could be more important.13,14 However, in the present study, length at birth and other birth measures including ponderal index and head circumference were unrelated to blood cholesterol. Although abdominal circumference could be important, it is strongly correlated with birth weight (r = .735; C. Martyn, Sheffield Study, personal communication), making the possibility of a strong independent relationship between abdominal circumference and TC unlikely. Although it has been suggested that maternal nutrition may influence blood lipids independent of birth weight, effects are modest12 and require confirmation.

Although fetal nutrition may influence cardiovascular risk via other mechanisms,1 the results of the present study emphasize that the influence of fetal nutrition on later TC is small—a finding similar to that recently reported in a meta-analysis of the relationship between birth weight and blood pressure.7 A 1-kg increase in birth weight is very substantial (~2 SDs); the associated change in TC is of the order of a tenth of an SD or less. The limited importance of fetal nutrition as an influence on TC level is further emphasized by our observation that the influence of adiposity in childhood or adolescence on the level of TC in contemporary children is likely to be considerably stronger than that of fetal nutrition—an observation which is consistent with our earlier observations on blood pressure47 and insulin level.43 Although some earlier reports have suggested that fetal undernutrition may interact with later obesity in the development of cardiovascular risk,48,49 there was no suggestion of such an interaction here. Therefore, these results imply that addressing the developing epidemic of obesity, both in adults and in children, is likely to be of greater importance in the primordial prevention of cardiovascular disease than the improvement of fetal nutrition. However, although fetal nutrition does not appear to be important, breastfeeding in infancy may have a modest long-term beneficial influence on TC level which, if confirmed, should also be considered in public health policy.50


   ACKNOWLEDGMENTS
 
The third phase of the Ten Towns Heart Health Study was supported by a Project Grant from the Wellcome Trust (reference 051187/Z/97/A).

We are grateful to research team members and to all the participating schools, pupils and parents and to the National Health Service staff who helped us to locate birth records and registers. Measurements of TC and LDL-cholesterol were made in the Department of Clinical Biochemistry, Royal Free Hospital (Professor A. F. Winder, Dr M. Thomas). Unpublished data for inclusion in the review were kindly provided by: Dr A. Bavedekar and Dr C. Yajnik (King Edward Memorial Hospital, Pune, India); Dr I. Rogers (formerly Cowin) and P. Emmett (Avon Longitudinal Study of Children and Parents, Institute of Child Health, University of Bristol, United Kingdom); Dr J. Eriksson and Dr T. Forsén (Department of Epidemiology and Health Promotion, National Public Health Institute, Helsinki, Finland); Professor D. Barker, Dr C. Fall, Dr C. Law, Dr C. Martyn, and Dr C. Osmond (Medical Research Council, Environmental Epidemiology Unit, University of Southampton, United Kingdom); Professor R. Hegele and Dr M. R. Ban (Blackburn Cardiovascular Laboratory, University of Western Ontario, Canada); Dr H. Kawabe (Keio University, Tokyo, Japan); Dr R. Morley (Royal Children’s Hospital, Parkville Victoria, Australia); Dr M. Fewtrell (Institute of Child Health, London, United Kingdom); Professor R. Rona and S. Chinn (Guy’s King’s and St Thomas’ School of Medicine, London, United Kingdom), Dr T. Roseboom (Academic Medical Centre, University of Amsterdam, the Netherlands); Dr J. Minami (Department of Hypertension and Cardiorenal Medicine, Dokkyo University School of Medicine, Tochigi, Japan); Dr S. Paaske (Department of Epidemiology and Social Medicine, University of Aarhus, Denmark); Professor B. Falkner (Department of Medicine Division of Nephrology, Thomas Jefferson University, Philadelphia, PA); Dr N. S. Levitt (Department of Medicine, University of Cape Town, South Africa); Dr K. Miura (Department of Public Health, Kanazawa Medical University, Ishikawa, Japan); Dr S. Tenhola (Department of Pediatrics, Kuopio University Hospital, Finland); Dr M. Antal (National Institute of Food Hygiene and Nutrition, Budapest, Hungary); and Dr L. Laurén (Department of Epidemiology and Public Health, Imperial College of Science, Technology and Medicine, London, United Kingdom).


   FOOTNOTES
 
Received for publication Jun 5, 2002; Accepted Oct 15, 2002.

Address correspondence to Christopher G. Owen, PhD, Department of Public Health Sciences, St George’s Hospital Medical School, Cranmer Terrace, London SW17 0RE, United Kingdom. E-mail: c.owen{at}sghms.ac.uk


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 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
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