Abstract
Background
Early exposure to socioeconomic disadvantage is associated with obesity. Here we investigated how early, and conducted mediation analyses to identify behavioural factors in adulthood that could explain why.
Methods
Among 931 participants in the New England Family Study, we investigated the associations of family socioeconomic disadvantage measured before birth and at age 7 years with the following measures of adiposity in mid-adulthood (mean age = 44.4 years): body mass index (BMI), waist circumference and, among 400 participants, body composition from dual-energy X-ray absorption scans.
Results
In linear regressions adjusting for age, sex, race and childhood BMI Z-score, participants in the highest tertile of socioeconomic disadvantage at birth had 2.6 additional BMI units in adulthood [95% confidence interval (CI) = 1.26, 3.96], 5.62 cm waist circumference (95% CI = 2.69, 8.55), 0.73 kg of android fat mass (95% CI = 0.25, 1.21), and 7.65 higher Fat Mass Index (95% CI = 2.22, 13.09). Conditional on disadvantage at birth, socioeconomic disadvantage at age 7 years was not associated with adult adiposity. In mediation analyses, 10–20% of these associations were explained by educational attainment and 5–10% were explained by depressive symptoms.
Conclusions
Infancy may be a sensitive period for exposure to socioeconomic disadvantage, as exposure in the earliest years of life confers a larger risk for overall and central adiposity in mid-adulthood than exposure during childhood. Intervention on these two adult risk factors for adiposity would, if all model assumptions were satisfied, only remediate up to one-fifth of the excess adult adiposity among individuals born into socioeconomically disadvantaged households.
Keywords: Socioeconomic disadvantage, adiposity, body mass index, fat mass, sensitive period, mediation, depressive symptoms, education
Key Messages
This study examined socioeconomic disparities in anthropometric measures of obesity (body mass index and waist circumference) and measures of body composition from DXA scans (android fat mass, android: gynoid percent fat ratio, Fat Mass Index).
Socioeconomic disadvantage around the time of birth was more strongly associated with adult obesity than disadvantage in childhood, resulting in higher body mass index, larger waist circumference and more android fat and total body fat.
Educational attainment and depressive symptoms in adulthood were partial mediators (i.e. up to one-fifth) of the association between early life disadvantage and adult obesity; intervention on these factors might remediate a small portion of adult disparities.
Introduction
Socioeconomic disadvantage early in the life course is associated with excess risk of obesity, and this excess risk continues into adulthood.1 However, it remains unclear when during childhood exposure to socioeconomic disadvantage first begins to elevate obesity risk. This information is needed to guide intervention strategies targeting early life risk factors for disparities in obesity.2 As with any developmental process characterized by sensitive periods of heightened susceptibility to environmental influences, reducing the population prevalence of and disparities in obesity requires knowledge not only of risk factors but also of their developmental timing.
Participants in the Panel Study of Income Dynamics exposed to low family income during their first year of life had elevated body mass index (BMI) as adults; however, exposure to low family incomes after age 1 year had no lasting relationship with BMI in adulthood.3 Interventions on income or mechanisms linked to income might therefore have no effect on obesity if not provided during the first year of life. Accordingly, the first aim of this study is to investigate sensitive periods of exposure to socioeconomic adversity during childhood—that is, times when exposure has a stronger association with adult adiposity.
The second aim is to investigate whether the consequences of childhood socioeconomic disadvantage on adult obesity might be mitigated by reducing exposure to adult risk factors. In other words, long after sensitive periods have passed, can the socioeconomic gradient in obesity be reduced? We conduct mediation analyses to estimate how much excess adiposity among adults exposed to disadvantage during childhood could be averted via intervention on six adult risk factors: educational attainment,4,5 physical activity, fruit and vegetable consumption,6 alcohol consumption,7–9 cigarette smoking10,11 and depressive symptoms.12,13
Methods
Sample
Participants were selected from the New England Family Study cohort, which comprises the adult offspring born 1959–66 to participants in the Boston and Providence sites of the Collaborative Perinatal Project (CPP). Between 2005 and 2007, 618 (68.8% of those selected) CPP offspring participated in a study of the pathways linking educational attainment to health;14 between 2010 and 2011, 400 (76.6% of those selected) CPP offspring participated in a study of the early life origins of ageing in mid-life that included dual-energy X-ray absorption (DXA) scans.15,16 There were 87 individuals who participated in both projects, resulting in a combined study sample of 931. Anthropometric measures of adiposity were investigated in the full sample, whereas measures derived from DXA scans were investigated in the subsample of 400 participants.
Measures
Socioeconomic disadvantage at birth and age 7
Responses to social history interviews administered when CPP mothers were enrolled during pregnancy and again at the child’s 7-year assessment were used to construct composite measures of socioeconomic disadvantage.17 Each measure had multiple components that were given a score of 0 (no or low disadvantage), 0.5 (medium disadvantage) or 1 (high disadvantage). The components were summed to produce a composite score categorized as low, medium or high, based on tertiles of their distribution in the study sample. The composite score included parental education (greater than high school, high school, less than high school), parental income (greater than 150% of the US poverty threshold, 100–150% of the poverty threshold, less than the poverty threshold), parental occupation (non-manual, manual, unemployed), family structure (two parents, one parent and parent divorced, separated or widowed), and household crowding (<1 person per room, 1–1.5 persons per room, >1.5 persons per room).
Adiposity
BMI in adulthood was derived from weight and height obtained from participants wearing light clothing without shoes, using a calibrated stadiometer and weighing scale operated by trained research technicians. Waist circumference was assessed by the smallest horizontal circumference between the participant’s ribs and iliac crest at the end of a normal expiration. Three measures of adiposity were derived from DXA scans: android fat mass (measuring centrally located fat), android-gynoid percent fat ratio18–20 (measuring central to hip-area body fat distribution) and total fat mass.21–24 Fat Mass Index was corrected for height by computing the ratio of total fat (kg)/height raised to the power of −0.5 (determined from a log-log regression of fat mass on height in the study sample).25,26 In childhood, weight and height at age 7 years were used to derive BMI Z-scores based on Centers for Disease Control and Prevention (CDC) growth charts.27
Hypothesized mediators of the association between early life disadvantage and adult adiposity measured in adulthood
Education was measured in years. Depressive symptoms were assessed with the 10-item Center for Epidemiologic Studies Depression Scale (CES-D).28 Participants reported the number of cigarettes smoked per day. Physical activity was assessed using the International Physical Activity Questionnaire Short Form29 and analysed as mean metabolic equivalent of task (MET) min per day spent engaging in moderate or vigorous physical activity. Mean daily fruit and vegetable consumption was assessed using a 25-item Food Frequency Questionnaire.30 Average daily alcohol consumption was assessed via self-report that measured consumption of beer, wine and liquor.
Analytic methods
To address the study’s first aim (identification of sensitive periods in childhood), we analysed socioeconomic disadvantage at birth alone and then together with disadvantage at age 7 years in linear regression models of adiposity. A stronger association of disadvantage at birth with adiposity than disadvantage at 7 years (adjusting for disadvantage at birth) would support a sensitive period effect of disadvantage in infancy.31 At the time the CPP was conducted, disadvantage was associated with lower BMI in childhood; analyses of childhood socioeconomic disadvantage therefore adjusted for BMI Z-score at 7 years (and therefore are interpreted relative to the change in adiposity from childhood to adulthood). In theory this brings results in alignment with contemporary cohorts in which an early disadvantage–lower BMI association is not present; in practice it focuses interpretation on factors related to disadvantage that lead to more rather than less adiposity. Adjusting for childhood BMI in the mediation analyses also addresses potential confounding by childhood growth of the association between behavioural factors in adulthood and adiposity. Based on evidence that early life conditions have stronger effects on adult obesity in females than males,1 we tested sex-by-disadvantage cross-product interactions in each model. Linear regression models for BMI and waist circumference included random intercepts for each of 113 sibling sets. As there were only 13 sibling sets in the DXA sample, a linear model with the ordinary least square estimator was used for the analyses of android fat mass, android-gynoid percent fat ratio and Fat Mass Index.
Mediation analyses were conducted to address the second aim by estimating the indirect effect of socioeconomic disadvantage through the adult adiposity risk factors that were associated with childhood disadvantage. Mediation analyses were implemented in Imai et al.’s mediation package in R which derives estimates of indirect effects under a counterfactual framework using nonparametric simulations; indirect effects are estimated from coefficients in two models, one for the mediator given exposures and confounders, and one for the outcome given mediators, exposures and confounders.32–35 Given a three-level exposure (Low, Medium and High Disadvantage), indirect effects are estimated for both the Medium vs Low and the High vs Low contrasts. For identified mediators we also estimated ‘path specific’ effects.36–38 Analyses also controlled for age at adult interview, sex, and race (White vs Non-White).
Missing data across all study variables ranged from 1% to 7% (Supplementary Table 1, available as Supplementary data at IJE online); however, requiring the analysis sample to have complete data on all study variables would exclude nearly 20% of participants. Accordingly we imputed 100 complete datasets using fully conditional specification39 implemented in IVEWare v0.3.40 In addition to all analysis variables and interactions of sex with all analysis variables, the imputation models included auxiliary variables that were associated with the probability of missingness or likely predictive of the values of missing data (pregnancy and delivery complications and maternal smoking during pregnancy, offspring’s birthweight, weeks of gestation at delivery and cognitive test scores during childhood). All analyses were conducted separately within each imputed dataset; point estimates were obtained by taking the average over the estimates from all imputed datasets, and the standard errors were obtained by combining the within imputation variance and the between imputation variance.41
Results
Characteristics of the analysis sample (n = 931) and the DXA subsample (n = 400) are presented in Table 1, which shows the distributions of socioeconomic disadvantage at the time of participants’ birth and at age 7 years. Though these were moderately correlated (r = 0.56), 44% of participants were in different categories of disadvantage at birth and age 7. Table 1 also shows the distributions of sex (58% female), race (75% White) and age at interview (mean = 44.4 years). The mean adult BMI for the sample was 29.9 km/m2, higher than the US average of approximately 26.5 and close to the cut-point of 30 for obesity.42 The mean waist circumference was 97.4 cm, and in the DXA subsample, participants had on average 3.1 kg of android fat. Distributions of adult adiposity according to disadvantage at birth are presented in Figure 1 (and in Supplementary Figure 1 for males and females separately). These show, for all measures of adult adiposity except android-gynoid percent fat ratio, distributions that are shifted up with higher childhood disadvantage at birth.
Table 1.
Characteristics of participants in the New England Family Study project on early life disadvantage and adult adipositya
| Full sample (n = 931) Percent (n) or mean (SE) | DXA sample (n = 400) Percent (n) or mean (SE) | |
|---|---|---|
| Socioeconomic disadvantage at birth | ||
| High | 33.5 (313) | 48.0 (194) |
| Medium | 39.1 (363) | 36.7 (145) |
| Low | 27.5 (255) | 15.3 (61) |
| Socioeconomic disadvantage at age 7 years | ||
| High | 34.5 (321) | 45.5 (182) |
| Medium | 32.1 (300) | 31.3 (125) |
| Low | 33.4 (310) | 23.4 (93) |
| Sex | ||
| Male | 41.7 (388) | 43.3 (173) |
| Female | 58.3 (543) | 56.7 (227) |
| Race | ||
| White | 74.8 (696) | 65.0 (260) |
| Non-White | 25.2 (140) | 35.0 (140) |
| Mean (SE) Age at Interview | 44.4 (0.1) | 47.0 (0.1) |
| Adiposity in childhood and adulthood, mean (SE) | ||
| BMI Z-Score at age 7 | 0.2 (0.03) | 0.2 (0.05) |
| Adult BMI | 29.9 (0.3) | 30.3 (0.4) |
| Adult waist circumference, cm | 97.4 (0.6) | 98.7 (0.9) |
| Android fat mass, kg | 3.1 (0.1) | |
| Android-gynoid percent fat ratio | 107.0 (2.6) | |
| Fat Mass Index | 39.6 (0.9) | |
| Hypothesized disadvantage-adiposity mediators, mean (SE) | ||
| Years of education | 13.6 (0.1) | 13.3 (0.1) |
| Moderate and vigorous physical activity (MET) | 3046.9 (108.8) | 2447.9 (162.7) |
| Fruits and vegetables per day | 2.4 (0.7) | 2.3 (0.1) |
| Drinks of alcohol per month | 15.8 (1.0) | 17.3 (1.7) |
| Cigarettes smoked per day | 4.4 (0.3) | 4.9 (0.4) |
| CESD scale of depressive symptoms | 16.6 (0.2) | 17.7 (0.3) |
SE, standard error.
Characteristics shown are based on the average of 100 multiply imputed datasets.
Figure 1.
Distributions of adult adiposity according to socioeconomic disadvantage at birth. Violin plots show outlines of kernel density plots with box plots inside. Body mass index and waist circumference (cm) were measured in the full sample (n = 931); android fat mass (kg), android-gynoid percent fat ratio and fat mass index were measured in the DXA subsample (n = 400).
In linear regression analyses of anthropometric measures of adiposity (Table 2, Model 1), high socioeconomic disadvantage at birth (relative to low disadvantage) was associated with an increase of 2.61 BMI units (95% CI: 1.26, 3.96) and 5.62 cm (95% CI: 2.69, 8.55) of waist circumference between childhood and adulthood. Children in disadvantaged households at birth had 0.7 kg (95% CI: 0.25, 1.21) more android fat in adulthood as well as 7.65 additional Fat Mass Index units (95% CI: 2.22, 13.09). No positive linear trend between disadvantage and adiposity was observed; rather, adults in the Medium and High categories of childhood disadvantage had similarly higher adiposity as adults in the Low category of disadvantage. There were no significant interactions identified between childhood disadvantage and sex.
Table 2.
Associations of socioeconomic disadvantage at birth and age 7 years with body size and composition in adulthood in the New England Family Studya
| Body mass index | Waist circumference | Android fat mass, kg | Android-gynoid percent fat ratio | Fat Mass Index | |
|---|---|---|---|---|---|
| Model 1 | |||||
| Socioeconomic disadvantage at birth | |||||
| High | 2.61 (1.26, 3.96) | 5.62 (2.69, 8.55) | 0.73 (0.25, 1.21) | 3.19 (−7.95, 14.33) | 7.65 (2.22, 13.09) |
| Medium | 2.23 (0.98, 3.48) | 5.22 (2.39, 7.76) | 0.75 (0.27, 1.23) | 6.06 (−5.96, 18.07) | 8.63 (3.22, 14.04) |
| Low | Reference | Reference | Reference | Reference | Reference |
| F (df = 2), Pb | 8.5 (<0.001) | 9.1 (<0.001) | 5.2 (0.005) | 0.6 (0.579) | 5.0 (0.007) |
| BMI Z-score, age 7 | 2.56 (1.99, 3.13) | 4.59 (3.36, 5.81) | 0.44 (0.27, 0.61) | 2.41 (−2.27, 7.10) | 5.45 (3.49, 7.41) |
| Model 2 | |||||
| Socioeconomic disadvantage at birth | |||||
| High | 1.76 (0.19, 3.33) | 3.78 (0.37, 7.18) | 0.53 (−0.05, 1.12) | 1.81 (−11.24, 14.85) | 4.92 (−1.65, 11.49) |
| Medium | 1.71 (0.35, 3.07) | 4.19 (1.27, 7.11) | 0.59 (0.03, 1.15) | 5.97 (−6.64, 18.57) | 6.26 (0.02, 12.51) |
| Low | Reference | Reference | Reference | Reference | Reference |
| F (df = 2), Pb | 3.4 (0.034) | 4.1 (0.017) | 2.2 (0.115) | 0.6 (0.544) | 1.9 (0.147) |
| Socioeconomic disadvantage at age 7 | |||||
| High | 1.56 (0.10, 3.03) | 3.56 (0.40, 6.72) | 0.30 (−0.19, 0.79) | 2.84 (−10.50, 16.17) | 3.95 (−1.59, 9.50) |
| Medium | 0.84 (−0.49, 2.17) | 1.19 (−1.69, 4.07) | 0.24 (−0.25, 0.72) | −2.40 (−13.25, 8.45) | 3.85 (−1.63, 9.33) |
| Low | Reference | Reference | Reference | Reference | Reference |
| F (df = 2), Pb | 2.2 (0.109) | 2.6 (0.071) | 0.7 (0.488) | 0.5 (0.611) | 1.1 (0.327) |
| BMI Z-score, age 7 | 2.59 (2.02, 3.16) | 4.66 (3.34, 5.89) | 0.44 (0.27, 0.61) | 2.59 (−2.21, 7.38) | 5.46 (3.49, 7.42) |
Linear regression coefficients and 95% confidence intervals from models of body mass index (n = 931), waist circumference (n = 931) android fat mass (n = 400), android-gynoid percent fat ratio (n = 400) and fat mass index (n = 400) also controlling for age at interview, sex and race/ethnicity.
F tests and P-values correspond to the joint significance of High and Medium disadvantage.
Conversely, disadvantage at age 7 years was not strongly associated with change in adiposity since childhood, except possibly for waist circumference (Model 2, Table 2; see Supplementary Figure 2 for plots of the coefficients for disadvantage at birth and disadvantage at 7 years, to compare the strength of their associations with adult adiposity). Given the weight of evidence pointing to disadvantage at birth as the relevant period of exposure for development of adiposity in adulthood, we assessed mediated effects only for disadvantage at birth.
Socioeconomic disadvantage at birth was associated with four of the six risk factors examined for adult adiposity: education, fruit and vegetable consumption, cigarette smoking and depressive symptoms (but not physical activity or alcohol consumption). Those in the High category of disadvantage had 2.25 fewer years of education (95% CI: −2.71, −1.79), consumed 1.13 fewer daily servings of fruits and vegetables (95% CI: −1.50, −0.77), smoked 5.14 more cigarettes per day (95% CI: 3.66, 6.62), and scored 2.12 points higher on the CESD-10 scale of depressive symptoms (95% CI: 1.09, 3.14) than those with Low disadvantage (Table 3). Accordingly, mediation analyses focused on these four risk factors.
Table 3.
Associations of socioeconomic disadvantage at birth with behavioural factors in adulthooda
| Dependent variable | Medium vs low disadvantage | High vs low disadvantage | F, df = 2 (P) |
|---|---|---|---|
| Mean (SD) years of education | −1.51 (−1.93, −1.09) | −2.25 (−2.71, −1.79) | 47.5 (<0.001) |
| Moderate and vigorous physical activity (MET) | 489.9 (−37.6, 1017.3) | 326.2 (−250.8, 903.1) | 1.7 (0.193) |
| Fruits and vegetables per day | −0.51 (−0.84, −0.18) | −1.13 (−1.50, −0.77) | 18.6 (<0.001) |
| Drinks of alcohol per month | 0.20 (−4.59, 4.99) | −4.38 (−9.61, 0.84) | 2.1 (0.123) |
| Cigarettes smoked per day | 2.34 (0.99, 3.69) | 5.14 (3.66, 6.62) | 23.3 (<0.001) |
| CESD scale of depressive symptoms | 1.60 (0.66, 2.53) | 2.12 (1.09, 3.14) | 8.9 (<0.001) |
SD, standard deviation.
Results of linear regression models for hypothesized adult mediators also adjusting for sex, race, BMI Z-score at age 7, and age at adult interview (n = 931). Regression coefficients and 95% confidence intervals shown.
Education and depressive symptoms were identified as mediators of the associations of early life disadvantage with adult BMI and waist circumference (Table 4). The magnitude of the indirect effects should be viewed relative to the estimates of total effects in Table 2. For example, Medium (vs Low) disadvantage at birth was associated with a 2.23 higher mean BMI (Table 2); 0.37 (95% CI: 0.08, 0.70) of that increase was mediated by lower educational attainment, and 0.20 (95% CI: 0.04, 0.40) of that increase was mediated by higher depressive symptoms in adulthood. Corresponding indirect effects for the High (vs Low) category of disadvantage (which had a total effect of 2.61) were 0.55 for education (95% CI: 0.12, 1.02) and 0.27 for depressive symptoms (95% CI: 0.07, 0.52). The indirect effect estimates for education were 10–20% of the magnitude of the total effect of disadvantage on adult BMI and 15–22% on adult waist circumference; for depressive symptoms, they were nearly 5–10% of the total effects (see Supplementary Table 2 for estimates and 95% confidence intervals of the proportions of total effects mediated).
Table 4.
Indirect effect estimates from mediation analyses of the obesogenic effects of socioeconomic disadvantage at birth on adult body size and compositiona
| Body mass index |
Waist circumference (cm) |
|||
|---|---|---|---|---|
| Medium vs Low disadvantage | High vs Low disadvantage | Medium vs Low disadvantage | High vs Low disadvantage | |
| Indirect effect Estimate (95% CI) | Indirect effect Estimate (95% CI) | Indirect effect Estimate (95% CI) | Indirect effect Estimate (95% CI) | |
| Years of education | 0.37 (0.08, 0.70) | 0.55 (0.12, 1.02) | 0.84 (0.21, 1.56) | 1.26 (0.32, 2.26) |
| Fruits and vegetables per day | −0.05 (−0.21, 0.09) | −0.10 (−0.40, 0.18) | −0.03 (−0.36, 0.28) | −0.07 (−0.70, 0.55) |
| Cigarettes smoked per day | −0.08 (−0.24, 0.06) | −0.17 (−0.50, 0.14) | 0.002 (−0.31, 0.32) | 0.005 (−0.67, 0.68) |
| Depressive symptoms | 0.20 (0.04, 0.40) | 0.27 (0.07, 0.52) | 0.50 (0.15, 0.98) | 0.69 (0.24, 1.27) |
| Android fat mass (kg) |
Android-gynoid percent fat ratio |
Fat Mass Index |
||||
|---|---|---|---|---|---|---|
| Medium vs Low Disadvantage | High vs Low Disadvantage | Medium vs Low Disadvantage | High vs Low Disadvantage | Medium vs Low Disadvantage | High vs Low Disadvantage | |
| Indirect effect Estimate (95% CI) | Indirect effect Estimate (95% CI) | Indirect effect Estimate (95% CI) | Indirect effect Estimate (95% CI) | Indirect effect Estimate (95% CI) | Indirect effect Estimate (95% CI) | |
| Years of education | 0.09 (−0.08, 0.27) | 0.12 (−0.10, 0.35) | 1.03 (−3.50, 4.75) | 1.35 (−4.58, 6.14) | 0.57 (−1.36, 2.54) | 0.75 (−1.78, 3.30) |
| Fruits and vegetables per day | −0.02 (−0.10, 0.04) | −0.04 (−0.16, 0.07) | 0.27 (−1.66, 2.26) | 0.48 (−2.80, 3.70) | −0.38 (−1.36, 0.35) | −0.67 (−2.15, 0.61) |
| Cigarettes smoked per day | −0.04 (−0.14, 0.03) | −0.07 (−0.21, 0.05) | 0.14 (−1.66, 1.83) | 0.22 (−2.64, 2.84) | −0.87 (−2.07, -0.02) | −1.42 (−3.06, -0.05) |
| Depressive symptoms | 0.03 (−0.05, 0.12) | 0.03 (−0.05, 0.13) | 0.02 (−2.15, 1.63) | 0.03 (−2.40, 1.80) | −0.03 (−0.96, 0.88) | −0.03 (−1.06, 0.98) |
Indirect effect estimates and corresponding 95% confidence intervals presented for the Medium and High categories of disadvantage at birth vs the Low disadvantage category adjusting for age at adult interview, sex, race and BMI Z-score at 7 years. Results based on a simulation-based approach in which models for the mediator and outcome were fitted and indirect effects were estimated after 10 000 simulations of the counterfactual outcomes for the Medium and High categories of the mediators.
The indirect effects of depressive symptoms controlling for participants’ attained education (‘path specific’ effects) were substantially reduced but still non-zero. For BMI, the path-specific effects of high and medium disadvantage through depressive symptoms were 0.15 (95% CI: 0.01, 0.34) and 0.11 (95% CI: 0.001, 0.28), respectively; for waist circumference, they were 0.38 (95% CI: 0.06, 0.85) and 0.29 (95% CI: 0.02, 0.69), respectively.
Among the behavioural risk factors, only cigarette smoking emerged as a mediator of the effects of disadvantage at birth on body composition. The indirect effects of cigarette smoking carried a negative sign (−1.42 for high and −0.87 for medium disadvantage); therefore, adjusting for smoking unmasks the even larger (direct) effect of disadvantage.
Discussion
This study posed two questions regarding the association between socioeconomic disadvantage during childhood and adult adiposity: (i) when during childhood is the association strongest?; and (ii) can the association be mitigated in part by reducing exposure to adult risk factors for obesity?
We addressed the first question through analyses of socioeconomic disadvantage measured before participants’ birth and again when they were 7 years old. Disadvantage before birth was associated with higher BMI in adulthood, higher waist circumference, higher android fat mass and higher Fat Mass Index; these associations were generally stronger than those of disadvantage at age 7 conditional on disadvantage at birth. The prenatal period and infancy may therefore be a sensitive period for exposure to socioeconomic disadvantage; this suggests that the increase in adiposity from childhood to adulthood among individuals raised in socioeconomically disadvantaged households is due to pathways to obesity established during the first months of life. Whereas a previous report from the New England Family Study showed that disadvantage in childhood was associated with adult obesity, that study measured disadvantage cumulatively from birth through 7 years.43 Here we identified infancy as the period when disadvantage was most strongly associated with participants’ long-term risk of adiposity.
Our study demonstrates that the socioeconomic gradient in obesity, which has increased over time,44 may have early childhood origins. Previous studies have also found sensitive periods for exposure to socioeconomic disadvantage during childhood but, as noted above, most of those studies did not examine disadvantage as early as infancy. There are several explanations for infancy being a sensitive period for exposure to disadvantage. First, obesity-related risk factors present during gestation could be more common among socioeconomically disadvantaged pregnancies. For example, Robinson et al.2 reported that cumulative exposure to maternal obesity, excess gestational weight gain, smoking during pregnancy and low maternal vitamin D were associated with a higher risk of offspring obesity. Second, early growth has been shown to predict adult overweight;45 thus, a sensitive period could reflect socioeconomic differences in growth during the earliest years of life. As our analyses adjusted for early growth, this explanation would imply that the sensitive period effect also involves factors connected to adiposity change between childhood and adulthood. Third, family-level adversities that are associated with risk for obesity may confer risk earlier than demonstrated in previous studies.46
We addressed the second aim of our study by conducting mediation analyses of four factors in adulthood that were associated with early life disadvantage: educational attainment, fruit and vegetable consumption, cigarette smoking and depressive symptoms. Two of these factors, education and depressive symptoms, had positive indirect effects between early life disadvantage and adult adiposity. Educational attainment is a reliable predictor of obesity.4,47 However, quasi-experimental studies of education suggest that standard analyses such as ours may overstate the health benefits of expanding educational opportunities,14 as educational inequalities in health may also be attributable to familial factors which increase risk of poor health before school entry. Depression and obesity are strongly related to one another in epidemiological studies.48 Their association is bidirectional and likely includes a non-causal component due to shared risks.49 Two additional factors, physical activity and alcohol consumption, were initially considered as potential mediators but were not pursued given that they were not associated with childhood disadvantage. Other factors unmeasured here that are important for understanding adiposity, such as caloric intake, need to be pursued in future research.
Socioeconomic disadvantage was measured in a cohort from 1959 to 1966. In the 1960s, poverty was associated with a higher risk of underweight, not overweight as it is today.50 For that reason, we presented analyses adjusting for BMI Z-score at age 7 years. Because within a single birth cohort it is not possible to account for secular trends, we cannot establish whether or not our findings regarding sensitive periods and mediation would generalize to more recent cohorts. However, childhood disadvantage is associated with obesity in more recent generations51–53 and our finding regarding a very early sensitive period for exposure to disadvantage is consistent with current thinking on the developmental origins of obesity.54
Socioeconomic disadvantage levels at birth and at age 7 years were moderately correlated with each other (r = 0.56), with 44% of the sample shifted into different categories of disadvantage at 7 years from their category at birth. However, the persistence of disadvantage during childhood might have presented a challenge in evaluating the relative strength of their influences on adiposity; whereas our results are consistent with a sensitive period in infancy, they do not exclude the possibility that both time points are important and thus could also support an accumulation model. In addition, with only two time points during childhood studied, we have provided only a partial test of sensitive periods. Evaluations of disadvantage at intermediary time points, as well as time points extending into adolescence, are needed.
The behavioural factors in adulthood that were used in mediation analyses were assessed concurrently with adiposity. This presents two issues: first, the temporality among the behavioural factors and adiposity could not be established; the two risk factors that emerged with indirect effects, education and depression, are known to be associated.55 Second, current measures of the behavioural factors may not accurately reflect participants’ cumulative history of them. This measurement error would likely bias mediation effects towards the null.
Conclusions
Socioeconomic disadvantage at the very beginning of life was associated with adult adiposity, based on anthropometric measures as well as by direct measures of central adiposity. If our findings regarding infancy being a ‘disparity-sensitive period’ for exposure to socioeconomic disadvantage are replicated, addressing disparities in obesity and related diseases will require interventions during infancy or even earlier. Our findings also need to be extended to cover a broader range of potential behavioural factors that could be targeted in adulthood. Nevertheless, if all assumptions were met regarding no unmeasured confounding, and if the temporality among education, depressive symptoms and adiposity is as our analyses assume, up to one-fifth of the excess adiposity linked with early childhood disadvantage would be averted.
Funding
This work was supported by grants RC2AG036666 and R01AG048825 from the National Institute on Aging and by the Intramural Research Program of the Eunice Kennedy Shriver National Institute of Child Health and Human Development.
Supplementary Material
Acknowledgements
This work used the computational resources of the NIH HPC Biowulf cluster [http://hpc.nih.gov]. We appreciate the expert data management and statistical programming support of Ms Kathleen McGaffigan and Ms Gina Ma. We are grateful for the insightful comments of members of the NICHD Social and Behavioral Sciences Branch (Brian Fairman, Denise Haynie, Christine Hill, Kuba Jeffers, Leah Lipsky, Jeremy Luk, Tonja Nansel, Bruce Simons-Morton and Kay Sita).
This work was presented at the 2016 meeting of the Society for Behavioral Medicine, Washington, DC, and at the 2017 Population Health Science Workshop at Boston University, Boston, MA.
Conflict of interest: None declared.
References
- 1. Senese LC, Almeida ND, Fath AK, Smith BT, Loucks EB.. Associations between childhood socioeconomic position and adulthood obesity. Epidemiol Rev 2009;31:21–51. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2. Robinson SM, Crozier SR, Harvey NC.. Modifiable early-life risk factors for childhood adiposity and overweight: an analysis of their combined impact and potential for prevention. Am J Clin Nutr 2015;101:368–75. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3. Ziol-Guest KM, Duncan GJ, Kalil A.. Early childhood poverty and adult body mass index. Am J Public Health 2009;99:527–32. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4. Roskam AJ, Kunst AE, Van Oyen H. et al. Comparative appraisal of educational inequalities in overweight and obesity among adults in 19 European countries. Int J Epidemiol 2010;39:392–404. [DOI] [PubMed] [Google Scholar]
- 5. Birnie K, Cooper R, Martin RM. et al. Childhood socioeconomic position and objectively measured physical capability levels in adulthood: a systematic review and meta-analysis. PLoS One 2011;6:e15564.. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6. Moore CJ, Cunningham SA.. Social position, psychological stress, and obesity: a systematic review. J Acad Nutr Diet 2012;112:518–26. [DOI] [PubMed] [Google Scholar]
- 7. Das-Munshi J, Leavey G, Stansfeld SA, Prince MJ.. Does social disadvantage over the life-course account for alcohol and tobacco use in Irish people? Birth cohort study. Eur J Public Health 2014;24:594–99. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8. Kavanagh A, Bentley RJ, Turrell G, Shaw J, Dunstan D, Subramanian SV.. Socioeconomic position, gender, health behaviors and biomarkers of cardiovascular disease and diabetes. Soc Sci Med 2010;71:1150–60. [DOI] [PubMed] [Google Scholar]
- 9. Bendsen NT, Christensen R, Bartels EM. et al. Is beer consumption related to measures of abdominal and general obesity? A systematic review and meta-analysis. Nutr Rev 2013;71:67–87. [DOI] [PubMed] [Google Scholar]
- 10. Gilman SE, Abrams DB, Buka SL.. Socioeconomic status over the life course and stages of cigarette use: initiation, regular use, and cessation. J Epidemiol Community Health 2003;57:802–08. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11. Canoy D, Wareham N, Luben R. et al. Cigarette smoking and fat distribution in 21,828 British men and women: a population-based study. Obes Res 2005;13:1466–75. [DOI] [PubMed] [Google Scholar]
- 12. Gaysina D, Hotopf M, Richards M, Colman I, Kuh D, Hardy R.. Symptoms of depression and anxiety, and change in body mass index from adolescence to adulthood: results from a British birth cohort. Psychol Med 2011;41:175–84. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13. McLaughlin KA, Conron KJ, Koenen KC, Gilman SE.. Childhood adversity, adult stressful life events, and risk of past-year psychiatric disorder: a test of the stress sensitization hypothesis in a population-based sample of adults. Psychol Med 2010;40:1647–58. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14. Loucks EB, Buka SL, Rogers ML. et al. Education and coronary heart disease risk associations may be affected by early-life common prior causes: a propensity matching analysis. Ann Epidemiol 2012;22:221–32. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15. Loucks EB, Britton WB, Howe CJ. et al. Associations of dispositional mindfulness with obesity and central adiposity: the New England family study. Int J Behav Med 2016;23:224–33. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16. Loucks EB, Huang YT, Agha G. et al. Epigenetic mediators between childhood socioeconomic disadvantage and mid-life body mass index: the New England family study. Psychosom Med 2016;78:1053–65. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17. Chin-Lun Hung G, Hahn J, Alamiri B. et al. Socioeconomic disadvantage and neural development from infancy through early childhood. Int J Epidemiol 2015;44:1889–99. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18. Okosun IS, Seale JP, Lyn R.. Commingling effect of gynoid and android fat patterns on cardiometabolic dysregulation in normal weight American adults. Nutr Diabetes 2015;5:e155.. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19. Samsell L, Regier M, Walton C, Cottrell L.. Importance of android/gynoid fat ratio in predicting metabolic and cardiovascular disease risk in normal weight as well as overweight and obese children. J Obes 2014;2014:1.. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20. Sun Q, van Dam RM, Spiegelman D, Heymsfield SB, Willett WC, Hu FB.. Comparison of dual-energy x-ray absorptiometric and anthropometric measures of adiposity in relation to adiposity-related biologic factors. Am J Epidemiol 2010;172:1442–54. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21. Bann D, Cooper R, Wills AK. et al. Socioeconomic position across life and body composition in early old age: findings from a British birth cohort study. J Epidemiol Community Health 2014;68:516–23. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22. Liu P, Ma F, Lou H, Liu Y.. The utility of fat mass index vs. body mass index and percentage of body fat in the screening of metabolic syndrome. BMC Public Health 2013;13:629.. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23. Ramsay SE, Whincup PH, Shaper AG, Wannamethee SG.. The relations of body composition and adiposity measures to ill health and physical disability in elderly men. Am J Epidemiol 2006;164:459–69. [DOI] [PubMed] [Google Scholar]
- 24. van den Berg G, van Eijsden M, Vrijkotte TG, Gemke RJ.. BMI may underestimate the socioeconomic gradient in true obesity. Pediatr Obes 2013;8:e37–40. [DOI] [PubMed] [Google Scholar]
- 25. VanItallie TB, Yang MU, Heymsfield SB, Funk RC, Boileau RA.. Height-normalized indices of the body’s fat-free mass and fat mass: potentially useful indicators of nutritional status. Am J Clin Nutr 1990;52:953–59. [DOI] [PubMed] [Google Scholar]
- 26. Wells JC, Cole TJ; ALSPAC study team. Adjustment of fat-free mass and fat mass for height in children aged 8 y. Int J Obes 2002;26:947–52. [DOI] [PubMed] [Google Scholar]
- 27. Kuczmarski RJ, Ogden CL, Guo SS. et al. 2000 CDC growth charts for the United States: methods and development. Vital Health Stat 2002;246:1–190. [PubMed] [Google Scholar]
- 28. Andresen EM, Malmgren JA, Carter WB, Patrick DL.. Screening for depression in well older adults: evaluation of a short form of the CES-D (Center for Epidemiologic Studies Depression Scale). Am J Prev Med 1994;10:77–84. [PubMed] [Google Scholar]
- 29. Lee PH, Macfarlane DJ, Lam TH, Stewart SM.. Validity of the International Physical Activity Questionnaire Short Form (IPAQ-SF): a systematic review. Int J Behav Nutr Phys Act 2011;8:115.. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30. Michaud DS, Skinner HG, Wu K. et al. Dietary patterns and pancreatic cancer risk in men and women. J Natl Cancer Inst 2005;97:518–24. [DOI] [PubMed] [Google Scholar]
- 31. Green MJ, Popham F.. Life course models: improving interpretation by consideration of total effects. Int J Epidemiol 2017;46:1057–62. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32. VanderWeele TJ. Mediation: introduction and regression-based approaches In: Explanation in Causal Inference: Methods for Mediation and Interaction. New York, NY: Oxford University Press, 2015, p. 20–65. [Google Scholar]
- 33. Imai K, Keele L, Yamamoto T.. Identification, inference and sensitivity analysis for causal mediation effects. Stat Sci 2010;25:51–71. [Google Scholar]
- 34. Imai K, Keele L, Tingley D.. A general approach to causal mediation analysis. Psychol Methods 2010;15:309–34. [DOI] [PubMed] [Google Scholar]
- 35. Tingley D, Yamamoto T, Hirose K, Keele L, Imai K.. mediation: R package for causal mediation analysis. J Stat Softw 2014;59:1–38.26917999 [Google Scholar]
- 36. Huang YT, Cai T.. Mediation analysis for survival data using semiparametric probit models. Biometrics 2016;72:563–74. [DOI] [PubMed] [Google Scholar]
- 37. Imai K, Yamamoto T.. Identification and sensitivity analysis for multiple causal mechanisms: revisiting evidence from framing experiments. Polit Anal 2013;21:141–71. [Google Scholar]
- 38. Vanderweele TJ, Vansteelandt S, Robins JM.. Effect decomposition in the presence of an exposure-induced mediator-outcome confounder. Epidemiology 2014;25:300–06. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 39. Van Buuren S, Brand JPL, Groothuis-Oudshoorn CGM, Rubin DB.. Fully conditional specification in multivariate imputation. J Stat Comput Simul 2006;76:1049–64. [Google Scholar]
- 40. Raghunathan T, Solenberger P, Berglund P, Van Hoewyk J. IVEware: imputation and variance estimation software. Regents of the University of Michigan. 2016.
- 41. Rubin DB. Multiple Imputation for Nonresponse in Surveys. Hoboken, NJ: Wiley-Interscience, 2004. [Google Scholar]
- 42. Ogden CL, Carroll MD, Kit BK, Flegal KM.. Prevalence of childhood and adult obesity in the United States, 2011-2012. JAMA 2014;311:806–14. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 43. Non AL, Roman JC, Gross CL. et al. Early childhood social disadvantage is associated with poor health behaviours in adulthood. Ann Hum Biol 2016;43:144–53. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 44. Clarke P, O’Malley PM, Johnston LD, Schulenberg JE.. Social disparities in BMI trajectories across adulthood by gender, race/ethnicity and lifetime socioeconomic position: 1986-2004. Int J Epidemiol 2009;38:499–509. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 45. Cunningham SA, Kramer MR, Narayan KM.. Incidence of childhood obesity in the United States. N Engl J Med 2014;370:403–11. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 46. Davis CR, Dearing E, Usher N. et al. Detailed assessments of childhood adversity enhance prediction of central obesity independent of gender, race, adult psychosocial risk and health behaviours. Metabolism 2014;63:199–206. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 47. Webbink D, Martin NG, Visscher PM.. Does education reduce the probability of being overweight? J Health Econ 2010;29:29–38. [DOI] [PubMed] [Google Scholar]
- 48. de Wit L, Luppino F, van Straten A, Penninx B, Zitman F, Cuijpers P.. Depression and obesity: a meta-analysis of community-based studies. Psychiatry Res 2010;178:230–35. [DOI] [PubMed] [Google Scholar]
- 49. Afari N, Noonan C, Goldberg J. et al. Depression and obesity: do shared genes explain the relationship? Depress Anxiety 2010;27:799–806. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 50. Phipps SA, Burton PS, Osberg LS, Lethbridge LN.. Poverty and the extent of child obesity in Canada, Norway and the United States. Obes Rev 2006;7:5–12. [DOI] [PubMed] [Google Scholar]
- 51. Gustafsson PE, Persson M, Hammarstrom A.. Socio-economic disadvantage and body mass over the life course in women and men: results from the Northern Swedish Cohort. Eur J Public Health 2012;22:322–27. [DOI] [PubMed] [Google Scholar]
- 52. Lee H, Harris KM, Gordon-Larsen P.. Life course perspectives on the links between poverty and obesity during the transition to young adulthood. Popul Res Policy Rev 2009;28:505–32. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 53. Shaw RJ, Green MJ, Popham F, Benzeval M.. Differences in adiposity trajectories by birth cohort and childhood social class: evidence from cohorts born in the 1930s, 1950s and 1970s in the west of Scotland. J Epidemiol Community Health 2014;68:550–56. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 54. Gillman MW. Early infancy—a critical period for development of obesity. J Dev Orig Health Dis 2010;1:292–99. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 55. Peyrot WJ, Lee SH, Milaneschi Y. et al. The association between lower educational attainment and depression owing to shared genetic effects? Results in ∼25, 000 subjects. Mol Psychiatry 2015;20:735–43. [DOI] [PMC free article] [PubMed] [Google Scholar]
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