Centre for Paediatric Epidemiology and Biostatistics, Institute of Child Health, 30 Guilford Street, London WC1N 1EH, UK
* Correspondence: Centre for Paediatric Epidemiology and Biostatistics, Institute of Child Health, 30 Guilford Street, London WC1N 1EH, UK. E-mail: L.Li{at}ich.ucl.ac.uk
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Abstract |
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Methods The 1958 British birth cohort study includes all children born between March 3, 1958 and March 9, 1958, who were followed to age 41 yr, and one-third of their offspring in 1991. Childhood height in each generation (measured at 7 yr for cohort members and 418 yr for offspring) was converted to a standard deviation score based on the 1990 British growth reference. We used multilevel models to analyse influences on height in order to allow for the hierarchical within-family data structure.
Results Childhood height increased by 1 cm between 1958 cohort members and their offspring. Several influences on childhood height in the older generation (maternal smoking, breastfeeding, maternal age, social class, maternal education, and parental divorce) did not affect childhood height in the younger generation. Parental height was most strongly associated with childhood height and effects did not diminish between generations [adjusted increase 2 cm for 1 maternal or paternal height standard deviation score (SDS)]. Third- or later-borns and those with three or more siblings had deficits of 12 cm (adjusted estimates) in both generations. Other factors, particularly indicators of socioeconomic position, showed weaker effects in the younger generation. For example, the growth deficit of 1.1 cm (adjusted estimate) among cohort members from households with >1.5 persons/room had disappeared in the offspring.
Conclusions Within Great Britain, the adverse effects of environmental factors on childhood height have lessened between recent generations.
Accepted 4 August 2004
Genetic effects on height are well accepted.1,2 Environmental influences have also been identified,36 with several factors, especially in early life, acting to delay growth. Depending on the severity and duration of the inhibitory factor, adult height may also be affected.7 However, given the increases in height seen across many populations,810 the magnitude of genetic and environmental influences may have changed over time.11,12 Greater increases in height have been found among children from poorer socioeconomic backgrounds, indicating that improvements in environmental factors may be having less effect on groups that already have favourable living conditions.13,14 Some evidence exists to suggest that in wealthy countries environmental factors explain a decreasing proportion of the variance in height,15 but this evidence is scant. The 1958 British birth cohort includes information on height and its determinants for two generations, and hence provides a rare opportunity to evaluate the changing role of genetic and environmental factors.
We investigated influences on childhood height in participants in the 1958 British birth cohort and their offspring. These generations span a period when the standard of living increased, as reflected in the decline of infant mortality in Britain: from 230 per 100 000 population in 1958 to 100 per 100 000 in 1983.16 We examined potential influences on childhood height, as identified from the literature,3,1719 including (i) parental height, as an indicator of genetic potential; (ii) prenatal factors, including maternal age at childbirth, maternal smoking during pregnancy, and birthweight; and (iii) early-life factors, including infant-feeding method, birth order, number of younger siblings, social class, housing tenure, household crowding, parental divorce, maternal education, and disability in childhood. Our aim was to establish whether genetic and environmental factors have similar effects on height in both generations.
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Methods |
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Explanatory variables
Information for cohort members was recorded in 1958; for offspring it was recorded in 1991, unless otherwise stated.
Data analysis
All height measures, including childhood height of cohort members (at 7 yr) and offspring (at ages 418 yr) and parental heights, were converted to standard deviation scores (SDSs) for the specific age and sex, based on the 1990 British growth reference.23 As expected, heights for the two generations were correlated, both between cohort members and offspring (r = 0.43) and between offspring from the same family (r = 0.39). To allow for the hierarchical data structure, effects on childhood height were estimated using multilevel models,24 with cohort members and offspring as 'level-1' units and families as 'level-2' units (see Appendix). We first modelled height SDS on age, sex, and each potential explanatory factor separately. Because the cohort members' age at the birth of their child was negatively correlated with the age of their offspringand also because the effect of environmental factors could vary during the growth periodwe tested for interactions with age for each factor of interest. All interactions were nonsignificant, possibly because most (77%) of the offspring sample were aged <10 yr. We therefore included age of the child in models of offspring height to reduce possible confounding effects of maternal age. For the models of childhood height in the cohort, we then added mid-parental height SDS, the average of both parents, and for the models of offspring height we added one parental measure. For both generations we included prenatal and early-life factors separately to estimate their effects; paternal and maternal height SDSs were also analysed separately. The relationship between birthweight and childhood height was estimated before and after adjustment for gestational age. Differences in effects between generations were tested. The percentage of variance explained by each factor was calculated as the change in the variance after adding the factor to the model divided by the total variance of height. The sample size for offspring (3077 418-year-olds) (Figure 1) was reduced to 2462 with complete data on explanatory factors. This analysis sample for the offspring was smaller than that for cohort members (n = 7993); hence, nonsignificant estimates for offspring were calculated using the larger sample size for cohort members (t-tests, based on the standard errors calculated from standard deviation for the offspring sample, but using the size of the cohort sample). All estimates remained nonsignificant (except for disability), and thus changes in the magnitude of effects could not be attributed to differences in sample size. Differences in height SDS were transformed to centimetres for a 7-year-old.
Analyses are presented for both sexes, combined with an adjustment for sex. This approach was justified because interactions of sex with each factor were mostly nonsignificant [P > 0.05, except for the interaction with housing tenure for the offspring (P = 0.03)]. The nonsignificant interactions with sex within generations ensure that changes in the effect of each factor between generations do not differ by sex. In respect of sample representativeness, we found that the sample of cohort members available for analysis (n = 7993) resembled the original birth study for childhood social class (21.3% were from classes IV&V, compared with 20.4% of those with data at age 7 yr) and for childhood height (122.5 cm at 7 yr in the analysis sample vs 122.4 cm in the full sample at 7 yr). Finally, the analyses were repeated separately for each factor using all subjects with information on that factor, and the results were similar to those presented here. Analyses were performed using SAS for UNIX and MLwiN.
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Results |
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Prenatal factors
The association between birthweight and childhood height was statistically significant in both generations: for every kilogram of birthweight, mean height SDS increased by 0.51 (2.6 cm), compared with 0.32 (1.7 cm) in offspring. The effect of birthweight was similar after controlling for gestational age, with an adjusted estimates of 0.55 (2.8 cm) and 0.39 SDS (2.0 cm), respectively (Table 2), although it weakened with adjustment for parental height and was unaffected by further adjustment for early-life factors. Maternal smoking during pregnancy was significantly associated with childhood height only among cohort members, with a growth deficit for children of heavier smokers (10 cigarettes/day) of 0.24 SDS (1.2 cm), reducing to 0.06 SDS (0.3 cm) with adjustment for mid-parental height, birthweight, and other factors (Table 2).
Early-life factors
No effect of breastfeeding on childhood height was found in either generation after adjustment for other factors. Birth order was associated with height in both generations, independently of other factors, with third- or later-borns being shorter on average than first-borns, by 0.32 SDS (1.7 cm) among cohort members and by 0.26 SDS (1.3 cm) among offspring (Table 2). Number of younger siblings was also consistently associated with childhood height, with children who had 3 siblings being shorter than those with <2 by 0.17 SDS (0.9 cm) and 0.14 SDS (0.7 cm) among cohort members and offspring, respectively, after adjusting for other factors (Table 2).
Housing tenure was significantly associated with height, with children from social housing being shorter than those from owneroccupier households, by 0.36 SDS (1.9 cm) among cohort members and by 0.15 SDS (0.8 cm) among offspring. After allowing for other factors, the difference reduced but remained significant in both generations. Fewer offspring (4.2%) lived in private-rented housing than cohort members (17.1%), and this group was taller than children from owneroccupier households only among offspring (Table 2). Mean height SDS reduced with increasing level of crowding, although the strength of the relationship reduced significantly in the offspring. Cohort members from households with >1.5 persons/room were shorter than those from households with <1 person/room by 0.65 SDS (3.4 cm); a deficit of 0.3 SDS (1.6 cm) in offspring became nonsignificant after allowing for other factors. Social class was significantly associated with the childhood height of cohort members, with children from classes IV and V being shorter by 0.39 SDS (2 cm) than those from classes I and II; however, this became nonsignificant after allowing for other factors (Table 2). No effect of social class was seen in the offspring.
Cohort members whose parents had separated or divorced were shorter on average, by 0.2 SDS (1 cm), than those whose parents had not, but the effect was nonsignificant after allowing for other factors and no effect was found in offspring (Table 2). Finally, there was an association with disability in both generations: a height deficit of 0.14 SDS (0.7 cm) and 0.16 SDS (0.8 cm) remained in cohort members and offspring, respectively, after adjustment for other factors (Table 2).
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Discussion |
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This is, to our knowledge, the first study to examine the changing influence on childhood height of a wide range of factors starting from before birth, although there is an extensive literature on social inequalities in childhood and adult height in the 1958 cohort and elsewhere.3,7,14,17 The 1958 cohort is representative of the initial birth sample.20,22 However, the offspring are a generation born to parents before their 30th birthday, rather than a randomly selected population sample, and their mothers are therefore younger on average (24.4 yr) than the general population (27.0 yr in 1986).28 Yet, most importantly, the offspring resemble the general population in many respects, including birthweight, social class, and height.23,29 One limitation is that some information was available only for one parent of the offspring (e.g. paternal or maternal height, and maternal education). Mid-parental height was used for cohort members, and height of one parent for the offspring. Thus we are better able to control for genetic influences in cohort members. The diminished effect of environmental influences on height was, however, already evident before allowance was made for parental height. Data available on the two generations in this study are extensive and present a unique opportunity to explore the change or stability of early-life influences on childhood height. The Application of multilevel models was important to incorporate the covariance structure of these data and to permit a comparison of influences across generations. Further analyses of these data (reported elsewhere) based on a comparison of parentoffspring pairs (rather than all cohort members) support the main findings of the present study of weakening environmental influences on height.30
Of the factors that we examined, three remained important predictors of childhood height across the two generations, namely, parental height, birthweight, and birth order. Parental height explained most of the variation in height in both generations. However, the effect of parental height was stronger in the second generation. This finding is consistent with a study in Finland in which heritability of height increased from a cohort born before 1929 to those born in 194757.15 Heritability is likely to be greater in affluent societies because there will be less impact of environmental factors that interfere with the achievement of individuals' genetic height potential than in societies with a low standard of living.
Second, for birthweight, there was a strong association in both generations, with a 2.6 cm and a 1.7 cm increase for each kilogram of birthweight in cohort members and offspring, respectively. The slightly weaker relationship among offspring may be partly due to measurement bias, as their reported birthweights may be less accurate than the measurements obtained for cohort members.31 Also, there was a tendency for a weaker linear relationship in the offspring, although a quadratic relationship was nonsignificant. This might be expected because of improved survival and postnatal growth among low-weight births.
Third, for birth order, later-born children were shorter in both generations examined in this study, as seen elsewhere,3,17,32 though not in all studies.33 We found an adjusted deficit of 1.7 cm and 1.3 cm for third- or later-borns for the older and younger generation, respectively. Mechanisms for the association are not well established, although some suggest that it is due to an effect of family size on postnatal nutrition.34 However, the birth-order effect in our study was independent of other factors, and it is therefore possible that it is a reflection of maternal uterine factors during fetal development. The deficit for third- or later-borns was smaller (though not significantly so) in the offspring than in the cohort members. However, the contribution of this factor to the percentage of height variance explained will have reduced over time because there are fewer higher-order births among offspring than among the earlier generation. Our study will underestimate the percentage of third- and later-born offspring (9.8%), since mothers were aged 30 yr or less. Nevertheless, there is evidence from elsewhere that the prevalence of higher-order births has been decreasing in Great Britain.35
Similar proportions of children with a disabling condition were identified in both generations, and it is notable that their deficit in growth had not improved over time.
Diminishing influence of environmental factors
Most of the effect of environmental factors on childhood height had diminished between generations in our study. This was notable for prenatal and postnatal influences, including maternal smoking, number of younger siblings, and measures of socioeconomic status. We showed, for example, height deficits of 1.9 cm and 0.8 cm, respectively, for cohort members and offspring living in social housing, and deficits of 3.4 cm and 1.6 cm, respectively, for those in overcrowded homes. Thus the risk associated with childhood disadvantage appears to have reduced over time, as suggested elsewhere by ourselves30 and others.11 However, some effects on childhood height have remained in the second generation, notably number of younger siblings and household crowding. But fewer offspring have >3 younger siblings and fewer live in households with >1.5 persons/room, and so proportionally fewer children are exposed to the risks associated with these factors.
The influence of maternal smoking during pregnancy on childhood height was evident only in cohort members, acting through its contribution to fetal growth. It is unlikely that the weaker effect of maternal smoking on offspring height is due to a lower mean consumption among those smoking >10 cigarettes/day: 35% of mothers of the offspring sample smoked 20 cigarettes/day, compared with 16% of mothers of the cohort generation. Also, the lack of an effect in the offspring is consistent with a study of a more recent generation in which children of smoking mothers had complete catchup in the first few years of life.36 It therefore appears that impaired growth in height due to adverse fetal conditions can be overcome by improved conditions and nutrition in early life.37
With respect to infant-feeding method, studies of early British cohorts found that those who were breastfed during the 1920s1940s were taller in childhood and adulthood.38 But in the 1958 cohort the benefit of breastfeeding for height was attributable to other early-life factors, consistent with findings from the 1970 cohort,39 while the absence of an association in the offspring agrees with results from another recent cohort, born in 199293.33 Thus, the relationship between breastfeeding and growth may have changed over time, possibly due to improvements in the nutritional adequacy of infant formula or to better postnatal diet more generally.
Finally, it is recognized that parental divorce can cause distress and be a major disruption in children's lives. We and others have previously shown a deficit in height associated with parental divorce7 or family conflict40 in boys, but not in girls, although the deficit did not persist into adulthood.7 In the present study, we found no evidence that the growth of a recent generation of children has been affected by parental divorce or separation.
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Appendix: A model for comparing height across two generations |
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Let yij be the height SDS of individual i in family j(i = 1, 2, ..., nj and j = 1, 2, ..., m) and xij a level-1 explanatory variable; then height SDS can be modelled as a function of an explanatory variable (at either level). Here k is dependent on j (k = nj 1). A single two-level model with one level-1 explanatory variable X can be formulated as
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The fixed effects ß0 and 0 represent the mean intercepts, ß1 and
1 represent the slope associated with the explanatory variable for cohort members and offspring, respectively. µ1j and µ2j are random effects (between families) for cohort members and offspring with mean 0. The parameter
ij is the level-1 residual for the offspring with
.
This model assumes that there is level-2 variance [between-family variance ] for cohort members, but no level-1 variance (within family) can be specified, as there is only one cohort member per family. For offspring, the level-1 and level-2 variances are
and
, respectively (total variance) =
Assuming that the covariance between cohort members and their offspring is Cov(µ1j, µ2j) =
12 and also Cov (µ2j, µij) = 0, the correlation between cohort members and any of their offspring is therefore,
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KEY MESSAGES
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Acknowledgments |
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References |
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