Socioeconomic status throughout life and body mass index: a systematic review and meta-analysis

This article aimed to systematically review the association between socioeconomic status according to the life course models and the body mass index (BMI) in adults. A review was performed following the guidelines of the PRISMA. The studies were identified in the MEDLINE/PubMed, LILACS and Web of Science databases. The eligible articles investigated the association between at least one life course model (risk accumulation, critical period or social mobility) and BMI. In order to assess the quality of the selected articles, the NOS checklist was applied to each study. Eleven articles were selected for the systematic review, and seven articles were selected for the meta-analysis. The average score and the median in the NOS checklist were 6.4, within a maximum possible score of 8 points. The most used model was social mobility. Regarding meta-analysis, there was association between lower life course socioeconomic status and BMI among women. BMI mean difference (MD) was higher among those who remained with low socioeconomic status throughout life when compared with those who maintained a high socioeconomic status (MD: 2.17, 95%CI: 1.48; 2.86). Before that, the BMI MD was higher among those with upward mobility, compared with those who maintained a high socioeconomic status throughout life (MD: 1.20, 95%CI: 0.73; 1.68). The risk of overweight was also higher among women who maintained low socioeconomic status (summary RR: 1.70, 95%CI: 1.05; 2.74); however, according to the GRADE, the studies presented very low quality evidence. For men, no association was observed. Having low socioeconomic status sometime during life is associated with higher BMI in adulthood.


Introduction
It is well established that obesity is one of the most important risk factors for mortality and morbidity and that it has been increasing globally in all age groups 1,2 . The prevalence of global obesity tripled between 1975 and 2014 2 . According to the World Health Organization (WHO), in 2014, an estimated over 1.9 billion adults (39% of the adults aged 18 or older) were overweight and, out of these, over 600 million were obese (13%) 2 .
The body mass index (BMI) is a simple index, calculated by dividing the weight in kilograms by the height squared in meters. It is commonly used to classify underweight, overweight and obesity in adults 3 .
In an attempt to capture the cumulative and dynamic nature of the socioeconomic status, several life course models have been developed. The social mobility model considers the process by which people move up or down the social hierarchy throughout their life cycle. This model presupposes that changes in the socioeconomic position can affect the adult's health 4 and considers both intragenerational (within the same generation) and intergenerational (between two or more generations) trajectories 5 . The socioeconomic status accumulation model refers to the continuation of the childhood social conditions through their life and assumes that environments and/or experiences accumulate over the years, with a dose-response effect -since the impact on an individual's health would increase as the number, duration and intensity of those exposures increased -and affects the risk of becoming sick in adulthood 4 . The critical period model presupposes that there are time windows within which exposure can cause irreversible effects in the structure and functions of organs and tissues, which in the future may trigger illnesses 4 .
Although several studies have tried to demonstrate the association between socioeconomic status and various health indicators, such as childhood and adulthood, particularly in certain phases of life 6,7,8,9,10,11,12 , very few studies have tried to use socioeconomic status throughout life as exposure for BMI in adulthood. Many studies have limited themselves to investigating the effect of the social conditions on only one life stage and, consequently, the temporal nature of this association has not been considered, leading to a partial explanation of how socioeconomic status contributes to health outcomes 13 . Besides, there is no record of a systematic review that has evaluated the effect of socioeconomic status over time, encompassing the three life course models, on BMI in adulthood. Newton et al. 14 performed a systematic review and meta-analysis; however, the authors only evaluated a lifelong socioeconomic status model (social mobility) by comparing individuals who, throughout life, remained with low socioeconomic status with those who maintained a high socioeconomic status.
This systematic review aimed to identify longitudinal studies that have evaluated socioeconomic status through life during the life course models and verify its association with BMI. Moreover, it intended to identify the most used models and to summarize its data with a meta-analysis.

Data sources and literature search
This study is a systematic review, following the guidelines of the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA), a protocol that defines the main items that must be reported in systematic reviews and meta-analyses 15 . The identification of the articles was carried out by searching the LILACS, PubMed/MEDLINE and Web of Science databases, as well as by tracking down bibliographical references from the articles selected for analysis. The systematic review protocol was registered in the International Prospective Register of Systematic Reviews (PROSPERO; registration number: CRD42018093713).
The search was carried out from September 2017 to December 2017, with an update conducted in December 2018 that found no new publications, and included three groups of terms for identifying the articles. The first group comprised terms related to socioeconomic status: ("life course epidemiology", "socioeconomic status", "socio-economic position", "socioeconomic trajectories", "changes of socioeconomic status", "socioeconomic position", "social mobility", "life course socioeconomic Cad. Saúde Pública 2019; 35(10):e00125518 position", "risk accumulation", "critical period" and "life course models"). The second group consisted of terms related to body mass index ("obesity", "body mass index", "adiposity" and "body composition"). Finally, the third group comprised terms that outline the study's design ("cohort studies" and "longitudinal studies"). The Boolean operator "or" was used within each groups, whereas the operator "and" was used between the three groups. Only terms in English were used. The search was complemented by investigating the references from the selected articles.
The search strategy was limited to publications of original investigations conducted with human beings, but with no restrictions as for age, date and language. The articles found were transferred to the software EndNote (http://www.endnote.com/) for the reading of titles and abstracts, and for selecting full texts.

Study selection and data extraction
Two reviewers (I.O.B. and L.S.V.) selected the articles to be included in the review, and the disagreements between them were settled by a third reviewer (M.C.F.A.). The reviewers excluded articles which did not evaluate at least one of the life course models (critical period, risk accumulation and social mobility) with the BMI outcome, and those which did not assess BMI in adults or did not consider background and life experiences when assessing socioeconomic status, that is, those studies that did not measured socioeconomic status in at least two life phases.
Studies were included in the meta-analysis if they reported a quantitative estimate (e.g. odds ratio (OR), relative risk (RR), mean BMI, prevalence) and standard errors or standard deviation (SD) or 95% confidence interval (95%CI) between life course socioeconomic status and BMI.

Quality assessment
The Newcastle-Ottawa Scale (NOS) checklist was applied to each study. The NOS assesses the quality of nonrandomized studies with case-control or cohort designs. The scale judges three perspectives: study groups selection, comparability of the groups and the assortment of exposure or outcome, providing a general score with values ranging from 0 to 9 16 . The NOS was applied independently by the two reviewers (I.O.B. and L.S.V.).
In addition to evaluating the methodological quality of the studies using the NOS, the GRADE (Grading of Recommendations, Assessment, Development and Evaluation) was used to summarize the general quality of the evidence. GRADE classifies the quality of evidence and the strength of recommendation provided by systematic reviews, scientific advice, and clinical guidelines 17,18 . It is a way of representing confidence in the provided information, by classifying the level of evidence and expressing the emphasis, so that a particular conduct is adopted or rejected in the case of clinical trial reviews. The starting point is the appreciation of the research design. Outcomes from randomized clinical trials started the evaluation with a high-quality score (4 points), while those generated by observational studies started as low quality (2 points). Next, a weighting is performed to decrease or increase the quality of evidence. Five factors may decrease the quality of evidence score and three factors may increase it 17 .
The risk of bias (lack of randomization, lack of allocation concealment, and lack of blinding), inconsistency (when there is significant and unexplained variability in results from different trials), indirect evidence, imprecision (when wide confidence intervals mar the quality of the data) and publication bias (when studies with "negative" findings remain unpublished) may decrease the quality of evidence score 17 .
A large effect (when the effect is so large that bias common to observational studies cannot possibly account for the result), the dose-response relation (when the result is proportional to the degree of exposure) and all plausible biases only reducing an apparent treatment effect (when all possible confounders would only reduce the observed effect. Thus, it is likely that the actual effect is larger than the data suggests) may increase the quality of evidence score 17 . Using these criteria, the level of evidence was classified, among the four levels shown by the GRADE: high quality, moderate quality, low quality and very low quality. In high quality evidences, additional research is very unlikely to change the prevalence estimate shown by the systematic review. When the study has very low-quality evidence, its prevalence estimate is very uncertain, and new studies are necessary 17,18 .

Statistical analysis
To strengthen the study, a meta-analysis was conducted with the model of social mobility and the studied outcome. We performed meta-analyses regarding BMI mean difference (MD) in adulthood, making the following comparisons: individuals who continued in a low socioeconomic status category throughout life with individuals who continued in high socioeconomic status; individuals with upward mobility with individuals who remained in high socioeconomic status throughout life; and individuals with downward mobility with individuals with upward mobility throughout life. In addition, meta-analyses were performed regarding prevalence of obesity in adulthood, comparing individuals who, throughout life, remained in a low socioeconomic status category with those who remained in high socioeconomic status. For this, random-effects models were used.
We assessed heterogeneity across studies using the I 2 statistic to approximate the proportion of total variation in the estimates due to between-study heterogeneity. All statistical analyses were performed using STATA software, version 12.1 (https://www.stata.com).

Article selection
A total of 6,942 articles was identified. After excluding duplicates, 5,620 titles were screened, 53 articles were selected for full text assessment and 11 manuscripts were included in the review, although only seven articles were included in the meta-analysis. Of these four articles that were not included, one did not evaluate social mobility and three did not report data required for meta-analysis ( Figure 1).

General characteristics
As for the general characteristics, the oldest publication dated from 2003; 2 articles were from middle-income countries 7,19 and 9 were from high-income countries 20,21,22,23,24,25,26,27,28 . The size of the samples ranged from 623 to 13,701 individuals (Table 1). Concerning the quality assessment of the articles, the average score and the median in the NOS scale were 6.4 and 6.0, respectively, within a maximum possible score of 8 points. The greatest limitations in the assessed articles were: not describing differential losses, not indicating the rate of follow-up, inadequate adjustment or lack of adjustment for confounding variables and not describing the results by sex (see Supplementary Table: http://cadernos.ensp.fiocruz.br/site/public_site/arquivo/supl-table-e00125518_2905.pdf).

Exposure assessment
The variables used for constructing the socioeconomic status variable through life were heterogeneous. The variables used included: level of education, occupation, family income, employment status and home ownership (Table 1).

Figure 1
Illustration of literature search.
As for "socioeconomic status throughout life", only two studies assessed the three life course models (risk accumulation, critical period and social mobility) simultaneously 25,26 ; seven studies assessed only social mobility 7,19,20,23,24,27,28 ; one study assessed critical period and socioeconomic status accumulation 22 and one study investigated social mobility and socioeconomic status accumulation 21 (Table 1).

Social mobility
Out of the seven articles that analyzed social mobility among women 7,19,21,24,25,26,28 , five verified that women who continued with low socioeconomic status throughout life had a higher mean BMI 7,19,24,26 or higher prevalence of obesity 28 , and one study found that women with downward social mobility were more likely to be overweight or obese compared to those who maintained a high socioeconomic status throughout life 21 . Among men, out of the seven studies that assessed social mobility 7,19,21,24,25,26,28 , six did not find associations 7,19,21,25,26,28 . One study verified that men with low socioeconomic status throughout life had, on average, a higher BMI 24 .
The forest plots of the meta-analyses of the BMI MD between individuals of both sexes who remained in a low socioeconomic status category and those who remained in a high socioeconomic status category throughout life are displayed in Figure 2. With regard to the BMI MD between men who remained in a low socioeconomic status category and those who remained in a high socioeconomic status category throughout life, there was no significant difference (MD: 0.38, 95%CI: -0.34; 1.11). Among females, the mean BMI difference was higher among those who remained with low socioeconomic status compared with those who maintained a high socioeconomic status throughout  7,26 . There was evidence of significant heterogeneity across the included studies (males: I 2 = 85.3%, p-value = 0.000, and females: I 2 = 71.9%, p-value = 0.007).
The forest plots of the meta-analyses of the BMI MD between individuals of both sexes with upward mobility and those who remained in a high socioeconomic status category throughout life are shown in Figure 3. With regard to the BMI MD between men with upward mobility and those who remained in a high socioeconomic status category throughout life, there was no significant difference (MD: 0.12, 95%CI: -0.61; 0.86). Among females, the BMI MD was higher among those with upward mobility compared with those who maintained a high socioeconomic status throughout life; the pooled estimate of the BMI MD was 1.20 (95%CI: 0.73; 1.68). There was evidence of significant heterogeneity across the included studies (males: I 2 = 83.1%, p-value = 0.000, and females: I 2 = 58.5%, p-value = 0.047).
In relation to the categorical data, only two studies were included in the meta-analysis ( Figure  4). There was no significant difference in the RR of overweight by life course socioeconomic status among males (summary RR: 1.19, 95%CI: 0.77; 1.85). Differently, females who continued with low  Regarding the GRADE assessment for the association between socioeconomic status throughout life and BMI MD and prevalence of obesity in adulthood, the association was considered of very low quality because of problems regarding study design and high statistical heterogeneity.

Risk accumulation
Risk accumulation was assessed in four articles 21,22,25,26 . It was observed that a higher mean BMI and a higher prevalence of excess weight in adulthood were associated with women who had an accumulation of socioeconomic disadvantage throughout life, as compared to the women who did not 22,25,26 .
Gustafsson et al. 22 showed that, among women with low socioeconomic status accumulation, aged 16 to 43 years, BMI was, on average, 0.8kg/m 2 higher than women who did not accumulate low socioeconomic status (β: 0.80, 95%CI: 0.47; 1.14). Boylan et al. 21 , also evaluating women, showed that the OR of overweight/obesity among those who accumulated low socioeconomic status, from 17 to 38 years of age, was 3.6 times greater (95%CI: 1.7; 7.7) than those who accumulated a high socioeconomic status. Murray et al. 25 showed that, among women, 1-unit increase in socioeconomic status score (a higher score means lower socioeconomic status) was associated with an increase of 0.91 in BMI at age 53 (95%CI: 0.66; 1.61). Among men, out of the four studies, only Gustafsson et al. 22 found the same results observed among women, while the other three did not find any associations 21,25,26 . Gustafsson et al. 22 showed that, among men with low socioeconomic status accumulation and between 16 to 30 years of age, BMI was, on average, 0.34kg/m 2 higher than men who did not accumulate low socioeconomic status (β: 0.34, 95%CI: 0.05; 0.63).

Figure 4
Summary of relative risk for overweight comparing individuals who continued in low socioeconomic status category throughout life with individuals who remained in high socioeconomic status throughout life.

Critical period
The critical period model was analyzed in three studies 22,25,26 . Out of those, Padyab & Norberg 26 did not observe an association with BMI for any of the sexes. Gustafsson et al. 22 verified that, among women, adolescence (16 years old) was a critical period, that is, the BMI of adolescents with low socioeconomic status was, on average, 1.54kg/m 2 times higher when compared with adolescents who did not show low socioeconomic status (β: 1.54, 95%CI: 0.77; 2.32). Gustafsson et al. 22 found no association among men. Murray et al. 25 showed that, among men, childhood was a critical period, indicating that the BMI of boys with low socioeconomic status was, on average, 1.46kg/m 2 times higher when compared to boys who did not present low socioeconomic status (β: 1.46, 95%CI: 1.14; 1.77).

Social mobility, risk accumulation and critical period
Two studies assessed the three life course models 25,26 . Both of the studies found that the model that best explains the association between socioeconomic status throughout life and BMI, among women, is the risk accumulation model, as it was concluded that the more periods with low socioeconomic status throughout life, the higher the BMI 25,26 . Among men, only one study observed an association 25 , showing that the critical period in childhood was the best model (the critical period model showed a match as good as the one of the saturated model, which includes all the hypotheses, and is better than the social mobility and risk accumulation) 30 . Therefore, men that were exposed to a low socioeconomic status in childhood showed, on average, a higher BMI in adulthood 25 .

Discussion
The BMI of women with upward mobility was, in general, higher than the BMI of those who kept a high socioeconomic status throughout life. Before that, women who remained with low socioeconomic status throughout life had a higher mean BMI or higher prevalence of obesity as compared to those who maintained a high socioeconomic status throughout life. Findings among men were less consistent. Newton et al. 14 found similar results despite having used longitudinal and cross-sectional studies in meta-analysis. This pattern is consistent with the hypothesis of risk accumulation, in which a greater duration of exposure to low socioeconomic status is associated with a bigger risk of high BMI 4 . The risk accumulation may also be due to the clustering of exposures, for example, individuals with lower socioeconomic status are more likely to be born with low birth weight 31 , to have unhealthy diets 32 and to be less physically active during leisure time 33 and, therefore, had a greater risk of high BMI.
The fact that individuals with upward mobility show BMI values higher than individuals that kept a high socioeconomic status throughout life suggests that childhood might be a critical period. It is likely that these individuals with low socioeconomic status in childhood had less access to healthcare and information, as compared to those who kept a high socioeconomic status throughout life.
The evidence of heterogeneity among the included studies is an important point. Although it is not possible to perform subgroup analyses because of the small number of studies included in the metaanalyses, some divergent aspects stand out among the studies included in the meta-analysis, especially among men. While Murray et al. 25 and Langenberg et al. 24 showed a negative effect between socioeconomic status and mean BMI difference (men who maintained low socioeconomic status over time had a mean BMI difference greater than those who maintained high socioeconomic status throughout life), Padyab & Norberg 26 and Aitsi-Selmi et al. 7 showed a positive effect between socioeconomic status and mean BMI difference (men who maintained low socioeconomic status throughout life had a MD in BMI lower than those who maintained high socioeconomic status throughout life). The converging points between Murray et al. 25 and Langenberg et al. 24 are as follows: both accompanied individuals from birth to 53 years of age, both studies were performed in high-income countries, both used occupation to assess the socioeconomic status and the results of the two studies were statistically significant. Aitsi-Selmi et al. 7 followed birth individuals at 23/25 years of age in a middle-income country, used income to assess socioeconomic status, and adjusted the analyses for birth weight. Padyab & Norberg 26 , meanwhile, followed the individuals from birth to 60 years of age and used occupation to evaluate the socioeconomic status. Padyab & Norberg 26 and Aitsi-Selmi et al. 7 did not find statistically significant results.
Concerning the critical period, further research is necessary to elucidate the results, as only two out of the three articles evaluating the critical period found an association with BMI in adulthood, one found an association among women (critical period in adolescence) 22 and one among men (critical period in childhood) 25 .
About the different results between men and women, literature shows that it can be explained by differences in the eating behavior, parity, social pressure for women to be thin and occupation 34,35 . Assumpção et al. 36 , in a population-based study, evinced a better quality diet among women, as opposed to men, especially due to higher consumption of fruit, vegetables and milk and dairy. Concerning parity, there is evidence that women's level of education is inversely related to birth rate 37,38 . Since childbirth is associated with a long-term increase in obesity 39,40 , this could explain why the association between socioeconomic status and BMI is stronger among women than among men. In relation to social pressure, there is evidence that it is heavier against overweight and obesity in women and this pressure is even greater among women with a higher socioeconomic status 34,41 .
In addition, some evidence suggests that obesity is associated with occupation, where weight discrimination is comparable to the rates of color and age discrimination, especially among women. After using the microdata from the National Longitudinal Survey of Youth (NLSY), carried out in the United States, Cawley 42 reported that, among women, an increase in two standard deviations in weight is associated with a 9% decrease in salaries, an effect equivalent to one and half years of education or three years of work experience. When it comes to men, there is no consensus. Also based on It is important to discuss the reverse causality of our findings. The meta-analysis conducted by Kim & von dem Knesebeck 45 evaluated the bidirectionality of the socioeconomic level and BMI. The authors observed a consistent relation between obesity and subsequent income 45 . One possible explanation is the greater discrimination in workplaces, people with obesity have lower wages, spend more time unemployed, are classified as less qualified and work longer hours than people with healthy average weight 45,46,47,48 . Consequently, discrimination may lead to adverse effects on the individual's health, such as impairment of psychosocial well-being, social isolation, lack of health care, binge eating, shame and guilt related to the body and development of obesity 49,50 .
The strengths of this review include the search in multiple bibliographical bases, the manual revision of the list of references from the articles included, the independent search for duplicates to minimize selection errors, the use of a protocol following established guidelines and a scale to assess the quality of the articles, the exclusion of studies that measured retrospectively the childhood socioeconomic status (cross-sectional studies) and the fact that there is not any systematic review about socioeconomic status throughout life and BMI in adulthood that encompasses the three life course models.
An important limitation to be highlighted is the scale to evaluate the quality of the articles. If a study has a single major flaw (e.g. lack of adjustment for important confounders), that would decrease our confidence in its results, but it would still receive a high quality rating despite the fact that this methodological flaw alone should decrease substantially our trust in the study results. Another relevant limitation was the very low quality of evidence from the studies included in this review, mainly due to the observational design and several methodological limitations that compromised the quality of the evidence; thus, our results should be interpreted with caution.
It is recommended that future longitudinal studies evaluate the relation between the socioeconomic level throughout life and BMI in adult life with greater methodological rigor, considering the importance of not adjusting for mediating variables, but rather for confounding variables. Besides, more studies are needed to evaluate the critical period and risk accumulation models. About one third of the articles did not adjust the analyses for potential confusion factors 21,23,24,25 and adjusted their analyses for mediators such as alcohol drinking, smoking, physical activity and diet, which may have led to an underestimated effect measure 7,22,26 . None of the studies indicated whether the individuals were different in relation to the participation in the study according to the assessed models, that is, whether individuals that kept a low socioeconomic status throughout life participated more than individuals that continued with a high socioeconomic status throughout life, which could lead to a selection bias. Another possible bias present in the assessed articles are the losses to follow-up, inherent to cohort studies. Moreover, the majority of the studies used only one life course model (social mobility), therefore the meta-analysis was only performed for this model.
Concerning the heterogeneity of the indicators used for evaluating socioeconomic status throughout life, it is possible to observe that, in high-income countries, the chosen indicators were occupation and level of education, while in middle-income countries, the preferred indicator was family income. Both middle-income studies were carried out in Brazil, a country that has had a widespread expansion in education, as well as several incentives for the access to higher education by those layers of society that were before left out. Therefore, it is reasonable to assume a reduction in the discriminating effect of the education level for younger generations and, consequently, a preference for family income as a more discriminating factor, given that occupation, in countries such as Brazil, poses limitations due to the lack of precision in measurement and classification 51 . It was also found that a large number of the studies used dichotomous variables for socioeconomic status (high/low), which were usually limited to two points in time, such as childhood and adulthood. This may have led to a disregard of a possible important variation in socioeconomic status because a long period was not assessed. Studies on socioeconomic status throughout life that include three or more points in time enable the analysis of more informative trajectories than studies assessing only two points.
Maintaining a low socioeconomic status throughout life, particularly among women, is associated with higher BMI values. Studies that assess the causal mechanisms of this association are necessary for indicating interventions that can minimize this effect.