The European Journal of Public Health Advance Access originally published online on September 1, 2005
The European Journal of Public Health 2006 16(1):21-30; doi:10.1093/eurpub/cki171
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European Perspectives |
Birthweight and blood pressure in five European birth cohort studies: an investigation of confounding factors
Rebecca Hardy1, Ulla Sovio2, Vanessa J. King2, Paula M.L. Skidmore1, Gunnhild Helmsdal3, Sjurdur F. Olsen3, Pauline M. Emmett4, Michael E.J. Wadsworth1, Marjo-Riitta Järvelin2,5 the EURO-BLCS Study Group
1 Medical Research Council National Survey of Health and Development, Department of Epidemiology and Public Health, Royal Free and University College Medical School, London, UK
2 Department of Epidemiology and Public Health, Imperial College London, UK
3 Maternal Nutrition Group, Danish Epidemiology Science Centre, Statens Serum Institute, Copenhagen, Denmark
4 Unit of Paediatric and Perinatal Epidemiology, Division of Community Medicine, University of Bristol, Bristol, UK
5 Department of Public Health Science and General Practice, University of Oulu, Finland
Correspondence: Rebecca Hardy, Medical Research Council National Survey of Health and Development, Department of Epidemiology and Public Health, Royal Free and University College Medical School, 1–19 Torrington Place, London WC1E 6BT, UK, tel: +44 20 7679 1732, fax: +44 20 7813 0280, e-mail: r.hardy{at}nshd.mrc.ac.uk
Received November 6, 2003, accepted November 3, 2004
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Abstract |
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Background: It has been suggested that the association between birthweight and blood pressure has been overstated as a result of publication bias and, within studies, a lack of adjustment for potentially important maternal and socioeconomic confounding factors and ‘overadjustment’ for current body size. This study investigates the impact of potential confounding variables on the birthweight–blood pressure association in birth cohort studies from different time periods and geographical locations in Europe. Methods: Data from five European birth cohort studies (from Finland, the UK, and the Faroe Islands) taking part in the European Birth-Lifecourse-Studies (EURO-BLCS) project were analysed. Birthweight was measured at birth in all cohorts and confounding variable information was collected prospectively at subsequent follow-ups in all cohorts. Regression models were used to assess the unadjusted association between birthweight and blood pressure and then to assess the impact of potential maternal and socioeconomic confounding variables and adjustment for later body size. Analyses were carried out in the same way across all five cohorts. Results: Birthweight was consistently negatively associated with systolic blood pressure (SBP) across all cohorts. Gestational age and possibly maternal pre-pregnancy weight, but not socioeconomic status, may be important confounding factors of the relationship between birthweight and SBP. The size of the birthweight–SBP association in adulthood may be larger than in childhood before adjustment for current body size, although a cohort effect cannot be ruled out. Conclusion: This study highlights the value of future cross-cohort comparisons in the investigation of the foetal origins of adult disease.
Keywords: birthweight, blood pressure, cohort studies, confounding
A systematic review of the relationship between birthweight and systolic blood pressure (SBP)1 suggested that the size of the association, although negative, was considerably smaller than previously reported.2–4 This was thought to be partly due to publication bias and partly due to overestimation of the strength of the association within many individual studies. Suggested reasons for such overestimation were lack of adjustment for potential maternal and socioeconomic confounding factors and ‘overadjustment’ for current body size. However, reviews using the published literature were unable to assess the impact of confounding variables owing to variations in analysis design and the covariates considered. Amplification of the effect of birthweight on SBP with age5 was also disputed by Huxley et al.1 Furthermore, separating a cohort effect from an age effect has to date not been possible as studies with blood pressure measured at older ages are generally of earlier-born cohorts than studies which have blood pressure measured at young ages.
The European Birth-Lifecourse-Studies (EURO-BLCS) project allows us to compare findings from five cohort studies of individuals born at different times and in different geographical locations in Europe. The oldest cohort was born between 1927 and 1937 and the youngest in 1991–1992. We compare the association of birthweight with SBP and diastolic blood pressure (DBP) across these cohorts, investigate the influence on this association of potential confounders selected primarily on the basis of their known associations with birthweight,6 and investigate the effect of adjusting for current body size. Finally, we compare the results from two cohorts, born 20 years apart, with blood pressure measured at approximately the same age. Thus we are able, in one example, to assess the potential cohort effect, independent of age.
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Subjects and methods |
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Table 1 provides background information on all five cohorts and details of blood pressure measurement. The Avon Longitudinal Study of Pregnancy and Childbirth (British 1992) is a cohort of 14 062 live births. The younger of two Northern Finland Birth Cohorts (Finnish 1986) consists of 9432 live births and the older (Finnish 1966) of 12 058 live births. The Medical Research Council National Survey of Health and Development (British 1946) is a cohort study of 5362 births in England, Scotland, and Wales in 1946. The Faroe Islands cohort (Faroe 1927/37) originally included 6379 men born between 1927 and 1937 in the Faroe Islands. Men selected for further examination and included in the present study were identified by screening using the Rose angina questionnaire.7 Blood pressure was measured on a sub-sample of 300 between the ages of 52 and 62 years, half of whom were chosen from the angina group, the other half from the healthy group. In all studies birthweight was measured and recorded immediately after birth or extracted from birth or midwives' records close to the time of birth (table 1). Maternal characteristics which influence birthweight and may also be associated with blood pressure in the offspring were considered as potential confounding variables. Maternal characteristics might be associated with blood pressure in their offspring through their influence on health-related behaviours, such as diet and physical activity. In addition, maternal age, pre-pregnancy weight, and birth order may influence the association of interest through their relationship with risk of conditions in pregnancy such as hypertension and diabetes.8–10 Maternal height may represent a genetic effect and maternal smoking was associated with blood pressure of offspring in previous studies.11,12 Socioeconomic status may provide the underlying explanation as such characteristics are socially distributed. Socioeconomic status may thus also be correlated with birthweight6 and, through inter-generational continuity of social conditions and health behaviours, blood pressure of offspring. Socioeconomic status was therefore considered as a potential confounder. Information on these factors was collected at various follow-up contacts from cohort members and their parents. Height and weight were measured at the same age as blood pressure in all studies.
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Statistical methods |
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Descriptive statistics were obtained for blood pressure, birthweight, and potential confounding variables. Regression models for males and females separately were used to analyse the data from each cohort in the same way. The analyses were repeated for blood pressure at each of the three ages in British 1946. SBP and DBP were analysed as continuous outcome measures and birthweight was fitted as a continuous explanatory variable. Linearity of the association was assessed by addition of a quadratic birthweight term. Adjustment for potential confounding factors common to at least four of the cohorts was performed in a series of five models: (i) maternal factors (mother's age at birth of the cohort member, mother's height, and the birth order of the survey member), (ii) mother's education (defined as appropriate within each cohort) as a marker of childhood socioeconomic status, (iii) variables in models (i) and (ii), (iv) body mass index (BMI) and height measured at the same age as blood pressure, (v) all preceding variables. In addition, gestational age, maternal smoking, pre-pregnancy weight, and paternal social class were assessed in the cohorts where they were available. In Faroe 1927/37, adjustment could not be made for mother's height and education, but all models were adjusted for age and angina status to allow for the different design of this study.
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Results |
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Mean birthweight was highest in Faroe 1927/37, at
4.0 kg (table 2). All other cohorts had a mean birthweight of 3.5 kg, with males being heavier than females. The two Finnish cohorts had heavier mean birthweight than either of the British cohorts. The mean birthweight in Finnish 1986 was 0.17 kg higher than that in British 1946, and 0.07 kg higher than that in Finnish 1966 born 20 years earlier for both males and females. The standard deviation (SD) ranged between 0.50 and 0.55 kg in most cases, being highest among males in British 1992 (SD = 0.58) and lowest among females in British 1946 (SD = 0.48).
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Mean SBP and DBP increased with age, with differences between the oldest and the youngest cohort being greater in males than females (table 2). Both blood pressure measures were very similar for males and females at age 7 years in British 1992, but in Finnish 1986 at age 16 years males already had considerably higher SBP than females. The divergence between the sexes in DBP was only apparent in Finnish 1966 and British 1946. BMI also increased with age across the cohorts. In the adult cohorts, the mean height for men in Finnish 1966 was greater than that in British 1946 and that in Faroe 1927/37. The Finnish 1966 women were also taller on average than the British 1946 women. The mean height among 16-year-old girls in Finnish 1986 was only 1 cm less than the mean adult female height in Finnish 1966, and already greater by 3 cm than that in British 1946, measured at age 53 years (mean height at 36 years in British 1946 was 1 cm greater than at 53 years, and so shrinkage with age was not a major factor in the difference between cohorts). Mean maternal age was slightly lower in both Finnish studies compared with the British studies and was highest in the Faroe Islands cohort. The higher maternal age in Faroe 1927/37 was reflected in the fact that it included the highest proportion of third- or later-born babies (64%) and the lowest proportion of firstborns (19%). British 1992 contained the most firstborn babies (45%). A greater percentage of mothers had low education in the two older cohorts than the younger two.
Unadjusted associations between birthweight and blood pressure
The unadjusted associations between birthweight and SBP were largest among both men and women in British 1946 with blood pressure measured at 36, 43 and 53 years of age (table 3). The weakest associations among males were seen in the youngest two cohorts, Finnish 1986 and British 1992 when blood pressure was measured at 16 and 7 years, respectively, and in Faroe 1927/37 when blood pressure was measured at 52–62 years. The finding in the Faroe Islands cohort did not fit with the trend across the other studies of an increasing association with increasing age but was difficult to interpret as the much smaller sample size resulted in wide confidence intervals around the estimate. For females in the two youngest cohorts the association was non-linear, whereby those of low and high birthweight had higher blood pressure than others. Finnish 1966 was the youngest cohort to exhibit a linear association, although it was somewhat weaker than that seen in British 1946.
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The association between birthweight and DBP (table 4) varied far less across cohorts than that that for SBP. Regression coefficients ranged from –0.6 to 0.0 mmHg per 1 kg higher birthweight in males and from –0.8 to 0.1 mmHg in females. The associations for DBP were smaller than those for SBP in Finnish 1966 and British 1946, but only slightly smaller or similar in Finnish 1986, British 1992, and Faroe 1927/37. Similar to SBP, the association in British 1992 females was not linear, whereas in Finnish 1986 females, in contrast to SBP, the association was linear.
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Adjusted associations between birthweight and blood pressure
For both males and females, adjustment for maternal factors (age of mother at birth of cohort member, mother's height, and birth order) produced small changes in the size of the regression coefficients for SBP, and these changes were inconsistent in direction. The largest change in coefficient was in Faroe 1927/37, where the association was reversed in direction after adjustment, although it was still non-significant (table 3). Similarly, adjustment for mother's education, maternal smoking, and paternal social class produced little consistent change. There was little impact on the association between birthweight and DBP after these confounding variables were accounted for (table 4). In British 1992 and the two Finnish cohorts addition of pre-pregnancy weight slightly strengthened the birthweight–SBP association (table 3). The impact of the additional adjustment for gestational age [after adjustment for the maternal and socioeconomic characteristics in model (iv)] was more variable across cohorts, reducing the size of the association in females in Finnish 1966 but strengthening it among males from the same cohort. For both males and females in Finnish 1986 and females in British 1992, a small negative association became a small positive association after adjustment for gestational age.
Adjustment for current BMI and height resulted in a strengthening of the negative association between birthweight and SBP in all cases except in British 1946 among women at all ages and among men at 53 years, where the effect became weaker. The largest impact on the size of the association was seen in the two youngest cohorts (table 3). The extent and direction of the change in regression coefficient depends on the size of the correlation between birthweight and current body size and between current body size and SBP (table 5). The two youngest cohorts exhibited a substantially larger positive correlation between birthweight and BMI than the older cohorts among both males and females. Correlations between BMI and SBP were also generally stronger in the younger three cohorts than in British 1946, particularly among females. The strong positive correlation between birthweight and height was more consistent across all cohorts, although the correlation between height and SBP weakened and then changed direction with increasing age. Faroe 1927/37 was again the exception to the trend and exhibited a positive non-significant correlation between height and SBP.
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Adjustment for current body size resulted in more consistent effects among both males and females across all cohorts (table 3). Among males, although the negative association became considerably stronger in the Faroes cohort, it was still the weakest effect and remained non-significant (table 3). All other cohorts produced an estimate between –2.0 and –2.4 mmHg per kg birthweight. In females, the associations in British 1992 and Finnish 1986 became linear and significant, and all estimates were between –1.3 and –2.2 mmHg per kg birthweight (table 3). For DBP, a strengthening of the negative effect of birthweight was seen in all cases among males (table 4). In females, the influence of body size was more mixed (table 4).
Additional adjustment for early-life confounding variables had little impact on these findings, with only the association between birthweight and SBP in Faroe 1927/37 changing substantially, although it remained non-significant (model (6) in table 3). Similarly, when additionally adjusting for the extra variables in the three youngest cohorts, the findings were generally very similar to those after adjusting only for current body size (model (12) in table 3), indicating the more powerful confounding effect of current body size compared with gestational age acting in the opposite direction.
Comparison of cohorts with blood pressure measured at a similar age
The unadjusted association between birthweight and SBP in British 1946 at 36 years of age was over double the size of that in Finnish 1966 at 31 years of age among women (table 3). Results were more similar in the two cohorts for men. The size of the association in British 1946 decreased and that in Finnish 1966 increased after adjustment for maternal factors. The impact of the adjustment for current body size was greater in Finnish 1966 for both males and females, with associations becoming more strongly negative. After simultaneous adjustment for all common variables, the associations in Finnish 1966 were stronger than those in British 1946 for both sexes. For DBP, the unadjusted association was negative, but small and not statistically significant, in both sexes in both cohorts. Adjustment for current BMI and height strengthened the associations in Finnish 1966 for both men and women (table 4).
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Discussion |
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All the studies showed a negative unadjusted association between birthweight and SBP in males, with all except the small associations in Finnish 1986 and in Faroe 1927/37 being significant. The two older cohorts which include females (Finnish 1966 and British 1946) also showed linear negative associations. The two younger cohorts (British 1992 and Finnish 1986) exhibited a non-linear relationship where those of lowest and highest birthweight had the highest SBP. Relationships between birthweight and DBP were negative but weaker. In British 1992, the association in males was significant although small and the relationship among females was non-linear, as for SBP.
The findings from Faroe 1927/37 were difficult to interpret for a number of reasons. First, the estimates of association were much less precise because the sample size was considerably smaller than in the other four cohorts. Second, the study design differs in that equal numbers of angina cases and controls were included, and there was a 10-year variation in age within the cohort. Finally, mean birthweight was higher than in the other cohorts by 500 g, no babies had a birthweight of under 2500 g, and only 11 of the 204 had a birthweight of 2500–3000 g. The lack of any ‘at risk’ small babies in the sample might lead to a weaker association between birthweight and SBP in this population.
As we found little confounding of the effect of birthweight on SBP with the available socioeconomic factors, it appears unlikely that childhood socioeconomic status explains the association. It may be that adult socioeconomic status is a confounding factor in the adult cohorts, although previous findings in British 1946 suggest this is not the case.13 Koupilova et al.14 considered a wider range of socioeconomic factors as confounders and concluded that they explained only part of the birthweight–blood pressure association. Our findings do not discount the importance of childhood socioeconomic status as a predictor of blood pressure, independent of birthweight, as previously reported in British 1946.15,16 Maternal age, height, and birth order of survey member had little consistent impact on the association of interest. A slight strengthening of the association was seen in Finnish 1966 males and a weakening in British 1946 males. Information on confounders in all EURO-BLCS studies were collected at the time of birth or at a contact during childhood, meaning that recall bias was limited. In the three cohorts with data on maternal smoking, no attenuation of the effect of birthweight was observed. Others have observed that maternal smoking was associated with both low birthweight and higher blood pressure in the offspring, findings consistent with the foetal programming hypothesis if smoking acts through poor foetal nutrition.11 Another study found that although maternal smoking affected offspring's blood pressure it did not explain the effect of birthweight on blood pressure.12 In our study the most important confounders, although only available in three cohorts, were gestational age and pre-pregnancy weight. Pre-pregnancy weight strengthened rather than weakened the association of interest in all cases. A genetic component may therefore be implicated.
The impact of gestational age was greater than that of pre-pregnancy weight. In females in all three cohorts, and in males in all but Finnish 1966, adjustment for gestational age made the effect of birthweight on SBP either weakly negative or weakly positive and linear, and non-significant. Thus for a given gestational age, there is very little or no effect of birthweight. So perhaps prematurity rather than low birthweight is associated with high blood pressure. Gestational age was available only in the three youngest cohorts, where the unadjusted association was generally weaker or non-linear in the first instance. The results from the only adult cohort which recorded gestational age (Finnish 1966) differ for men and women, with a strengthening of the negative association in males. Gestational age may therefore be more important in determining blood pressure in childhood and adolescence than in adulthood. Few other studies report adjustment for gestational age,17–22 and they provide little evidence of confounding.20–22 However an attenuation of the birthweight–SBP relationship was reported in children aged 5–7 years.18 In some studies21,22 simultaneous adjustment for current body size and other factors make it difficult to interpret the impact of gestational age alone. Adjustment for current body size may overwhelm the confounding effect of the other factors as in our findings.
Our findings suggest that the unadjusted effects in the adult cohorts are stronger and more linear than those in childhood, with the exception of Faroe 1927/37, in agreement with the amplification hypothesis. Interpretation of the association after adjustment for current body size must be cautious as changes in the effect may reflect the importance of postnatal rather than prenatal growth.23 Previous meta-analyses may have underestimated the change from childhood to adulthood in the birthweight–SBP association, since they have generally been based on estimates after adjustment for current BMI. Before such an adjustment in British 1992 and Finnish 1986 there was only a small negative association; after adjustment the association across cohorts was more consistent. Many studies in cohorts of children and adolescents report only the findings after adjustment for current body size,5,18,24–26 while studies that report unadjusted effects as well suggest smaller negative or even positive associations before adjustment,27–29 similar to our findings. The higher correlation between birthweight and childhood and adolescent body size compared with birthweight and adult body size is the cause of the larger impact on the estimates in younger cohorts, as demonstrated by our comparison of correlation coefficients.
Alternatively, the differences in findings across cohorts of different ages may be a result of cohort effects. The curvilinear associations of birthweight with blood pressure seen in the later-born cohorts may be due to differences in birthweight distributions caused by improved chances of survival of low birthweight babies and an increased proportion of macrosomic babies associated with gestational diabetes30,31 and maternal obesity.9,32 Gestational diabetes and increased glucose intolerance are more common among the more obese and among older mothers,9,10 and are associated with increased risk of diabetes and obesity in the offspring33,34 and therefore potentially also high blood pressure. Although, perhaps surprisingly, there was little variation in mean maternal age across the EURO-BLCS cohorts, a higher rate of maternal obesity would be expected for later-born cohorts given the rise in obesity among women during the past decades in many European countries.35
Data are not currently available to test definitively the amplification hypothesis over the whole lifecourse. In studies where the amplification hypothesis has been tested, generally in cohorts of children with a few followed through to adolescence and early adulthood, findings have been inconsistent.5,19,36–41 The hypothesis has also been tested within British 1946, and although an increase in the negative association was observed between 36 and 53 years, the change was not significant.16 Currently, few cohorts born at different times have blood pressure measured at the same age. We show similarities in the association between two cohorts born 20 years apart and in different countries of Europe where blood pressure has been measured at a similar age (31 and 36 years). In males, a negative association was seen before and after adjustment in both cohorts and a very similar size effect after adjustment for maternal factors. That suggests little or no cohort effect in this example. There were, however, differences between females in the two cohorts and in the impact of the adjustment for current body size, largely as a result of the higher correlations between BMI and blood pressure in Finnish 1966.
Our findings relating to DBP were consistent with those for SBP, although the associations with birthweight were not as strong. They were also consistent with the findings from most previous studies, where little evidence of an association before adjustment for current body size has been observed.4 Further, it is likely that many studies did not present findings for DBP because of a lack of significant association. Foetal growth may operate mainly or only through an influence on SBP. However, DBP may be measured less accurately than SBP, especially using mercury sphygmomanometers. Further, the recording depends on which of the Korotkoff sounds were recorded, potentially leading to some recording differences.
In conclusion, gestational age and possibly maternal pre-pregnancy weight may be important confounding factors of the relationship between birthweight and SBP. Socioeconomic status does not appear to be a confounding variable, and the impact of other maternal characteristics was relatively small and inconsistent across cohorts. The size of the birthweight–SBP association in adulthood may be larger than in childhood before adjustment for current body size, although a cohort effect cannot be ruled out. This study indicated the importance of investigating the influence of confounding variables individually, in particular without adjustment for current body size. It also highlighted the need for careful interpretation of results adjusted for current body size, particularly when comparing across cohorts of different ages, and the value of future cross-cohort comparisons in the investigation of the foetal origins of adult disease.
Key points
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Acknowledgments |
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This research was funded by the European Commission Quality of Life and Management of Living Resources Programme, contract number QLG1-CT-2000-01643. The National Survey of Health and Development is funded by the UK Medical Research Council and the core of the Northern Finland Birth Cohort Studies by the Academy of Finland. The Avon Longitudinal Study of Parents and Children is further supported by the UK Medical Research Council, the Wellcome Trust, the Department of the Environment, the University of Bristol, and various medical charities and commercial companies. The Faroese cohort was supported by the Faroease Research Council.
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 D. A. Lawlor, A. Hubinette, P. Tynelius, D. A. Leon, G. D. Smith, and F. Rasmussen Associations of Gestational Age and Intrauterine Growth With Systolic Blood Pressure in a Family-Based Study of 386 485 Men in 331 089 Families Circulation, February 6, 2007; 115(5): 562 - 568. [Abstract] [Full Text] [PDF]
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