Educational attainment but not measures of current socioeconomic circumstances are associated with leukocyte telomere length in healthy older men and women

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Abstract

Low socioeconomic status (SES) may be associated with accelerated biological aging, but findings relating SES with telomere length have been inconsistent. We tested the hypotheses that shorter telomere length and telomerase activity would be related more robustly to education, an early life indicator of socioeconomic position, than to current indicators of socioeconomic circumstances. Healthy men and women aged 53–76 years from the Whitehall II epidemiological cohort provided blood samples from which telomere length was assessed in 448 and telomerase activity in 416. Educational attainment was classified into four levels, while household income and grade of employment were measured as indicators of current socioeconomic circumstances. Age, gender, blood pressure, glycated hemoglobin, high density lipoprotein cholesterol, smoking, body mass index and physical activity were included as covariates. We found that lower educational attainment was associated with shorter telomere length after controlling statistically for biological and behavioral covariates. Neither household income nor employment grade was related to telomere length. The association between telomere length and education remained significant after adjusting for current socioeconomic circumstances. In men, highest levels of telomerase activity were found in the lowest education group. We conclude that low SES defined in terms of education but not current socioeconomic circumstances is associated with shortened telomeres. Low educational attainment may be an indicator of long-term SES trajectories, and be associated with accumulated allostatic load resulting in telomere shortening. Education may also promote problem-solving skills leading to reduced biological stress responsivity, with favorable consequences for biological aging.

Highlight

► Lower educational attainment is associated with shorter leukocyte telomere length in healthy older men and women, and may reflect more rapid cellular aging in lower socioeconomic status individuals.

Introduction

The pronounced social gradient in health and premature mortality is well established, and has become an issue of worldwide concern (CSDH, 2008). Individuals of lower socioeconomic status (SES) are prone to the early development of diseases of older age, including coronary heart disease (CHD), type 2 diabetes, chronic pulmonary disease and some cancers (Jemal et al., 2008, Mackenbach et al., 2008). The SES gradient has multiple determinants, including differential access to health care, health-related behaviors, physical exposures across the life course, and psychosocial factors (Adler and Rehkopf, 2008). Understanding how socioeconomic circumstances influence the pathophysiological processes underlying chronic physical illness may highlight novel approaches to prevention. Lower SES is associated with dysregulation of stress-related biological processes indicative of chronic allostatic load (McEwen, 1998, Seeman et al., 2010). Lower SES adults show impaired post-stress recovery in cardiovascular and hemostatic processes (Steptoe et al., 2002, Steptoe et al., 2003), autonomic dysregulation (Hemingway et al., 2005), heightened cytokine responses to acute stress (Brydon et al., 2004), and chronic mild inflammation (Loucks et al., 2006, Nazmi et al., 2010a).

One theory that might integrate these observations is that lower SES leads to acceleration of the aging process (Adams and White, 2004). This effect might be indexed by telomere length (Adler and Stewart, 2010). Telomeres are complex DNA–protein structures that cap and stabilize the physical ends of chromosomes (Blackburn et al., 2006). Mammalian telomeric DNA consists of tandem repeats of the sequence TTAGGG that extend over several thousand base-pairs. Synthesis and maintenance of telomeres is a complex process requiring a specialized reverse transcriptase (telomerase) which adds TTAGGG repeats onto the DNA 3′ ends. In the absence of telomerase or when this enzyme is expressed at low levels, DNA synthesis during cell division results in the progressive shortening of telomeric DNA. In addition, due to its high G content, telomeric DNA is very susceptible to oxidative damage and the generation of single strand breaks. Hence, telomere shortening is also affected by the oxidative burden of the cell (von Zglinicki, 2002). Telomere erosion eventually compromises telomere integrity, triggering a DNA damage response which results in the onset of senescence (d’Adda di Fagagna et al., 2003). Telomerase may also have a direct role in chromosome end protection and in cell survival, independent of telomere length maintenance (Chan and Blackburn, 2004). Telomere shortening has been observed in vivo in association with normal aging (Aubert and Lansdorp, 2008) and with age-related disease, and short telomeres are associated with increased risk of premature myocardial infarction (Brouilette et al., 2003) and mortality (Cawthon et al., 2003, Epel et al., 2009).

The existing evidence relating telomere length with SES is inconsistent. Cherkas et al. (2006) showed in a large study of female twins that lower SES defined by occupational class was associated with shorter telomeres independently of chronological age, body mass, smoking and physical activity. But subsequent studies have failed to replicate this observation (Adams et al., 2007, Batty et al., 2009, Kananen et al., 2010, Risques et al., 2010) and in a study of older Chinese men, an association between higher SES and shorter telomeres was reported (Woo et al., 2009).

These findings have primarily emerged from opportunistic analyses of population studies carried out for other reasons, in which the sampling structure was not focused on SES. Studies have also varied in the measure of SES, and in the stage at life at which SES is ascertained. Occupational grade, income and educational attainment are the commonest measures. Occupation and income are indicators of current socioeconomic circumstances, whereas education is typically completed early in life and partly dictates life-course trajectories (Mirowsky and Ross, 2003). Inflammatory damage may have a particularly pronounced effect relatively early in life, when the rate of telomere attrition is high (Frenck et al., 1998), and SES in early adult life may predict later oxidative damage (Janicki-Deverts et al., 2009). Telomerase preferentially elongates shortened telomeres, and the cellular level of telomerase activity is under multiple additional controls. While these processes are poorly understood in normal human leukocytes, they could be related to telomere shortness. Therefore, we included telomerase enzyme activity levels in these analyses.

If long-term accelerated cellular aging is characteristic of lower SES, we conjectured that reduced telomere length might be associated more robustly with education than with income or occupational grade. This possibility was tested in a subsample from the Whitehall II study, a large population cohort recruited specifically to investigate the association between SES and cardiovascular disease risk (Marmot et al., 1991).

Section snippets

Participants

Participants in this study were recruited from the Whitehall II epidemiological cohort, a sample of 10,308 London-based civil servants initially assessed in 1985–1988 when aged 35–55 years (Marmot and Brunner, 2005). A subsample of 543 men and women of white European origin, with no history or objective signs of coronary heart disease, no previous diagnosis or treatment for hypertension, diabetes, inflammatory diseases, or allergies, was recruited for an investigation of the relationship between

Results

Table 1 summarizes the characteristics of the different educational attainment groups. One hundred and eighty (35.6%) of participants had a college/university degree, 153 (30.2%) had obtained A levels, 132 (26.1%) O levels, and 41 (8.1%) had no educational qualifications. There was no difference in gender distribution between educational attainment groups. However, participants with lower education were slightly older, were less likely to be currently in paid employment, and had lower incomes

Discussion

The results of this study suggest that in healthy men and women in the age range 53–76 years, greater education is associated with longer leukocyte telomeres. This effect was independent of age and gender, and of biological and behavioral risk factors including blood pressure, glycated hemoglobin, HDL-cholesterol, BMI, smoking status and physical activity. By contrast, we found no significant associations between household income or occupational grade and telomere length. Interestingly, the

Acknowledgments

This study was supported by the Medical Research Council UK (G0601647) and the British Heart Foundation (RG/05/006).

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