Indoor air pollution from solid fuels and peripheral Blood DNA methylation: Findings from a population study in Warsaw, Poland

doi:10.1016/j.envres.2014.08.017

Environmental Research

Volume 134, October 2014, Pages 325-330

https://doi.org/10.1016/j.envres.2014.08.017 Get rights and content

Highlights

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We examined the associations of indoor air pollution with blood DNA methylation.
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Indoor air pollution was associated with reduced DNA methylation in non-smoking women.
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Using solid fuel before age 20 was associated with decreased DNA methylation.
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There was no association between indoor air pollution and IFG2/H19 ICR methylation.

Abstract

DNA methylation is a potential mechanism linking indoor air pollution to adverse health effects. Fetal and early-life environmental exposures have been associated with altered DNA methylation and play a critical role in progress of diseases in adulthood. We investigated whether exposure to indoor air pollution from solid fuels at different lifetime periods was associated with global DNA methylation and methylation at the IFG2/H19 imprinting control region (ICR) in a population-based sample of non-smoking women from Warsaw, Poland. Global methylation and IFG2/H19 ICR methylation were assessed in peripheral blood DNA from 42 non-smoking women with Luminometric Methylation Assay (LUMA) and quantitative pyrosequencing, respectively. Linear regression models were applied to estimate associations between indoor air pollution and DNA methylation in the blood. Compared to women without exposure, the levels of LUMA methylation for women who had ever exposed to both coal and wood were reduced 6.70% (95% CI: −13.36, −0.04). Using both coal and wood before age 20 was associated with 6.95% decreased LUMA methylation (95% CI: −13.79, −0.11). Further, the negative correlations were more significant with exposure to solid fuels for cooking before age 20. There were no clear associations between indoor solid fuels exposure before age 20 and through the lifetime and IFG2/H19 ICR methylation. Our study of non-smoking women supports the hypothesis that exposure to indoor air pollution from solid fuels, even early-life exposure, has the capacity to modify DNA methylation that can be detected in peripheral blood.

Introduction

Approximately half of the world׳s population uses solid fuels including coal, wood, dung, and crop residues for cooking or home heating (Torres-Duque et al., 2008). Usage distributions vary among countries with the largest prevalence in rural areas of developing countries, while a number of households in developed countries still use wood or other biomass products for heating (Naeher et al., 2007, Forum of International Respiratory Studies (FIRS) Task Force on Health Effects of Biomass Exposure, 2008). The fuels are typically burned inefficiently in open fires, leading to high emission rates and high levels of indoor air pollution (Lewtas, 2007, Forum of International Respiratory Studies (FIRS) Task Force on Health Effects of Biomass Exposure, 2008). Products of incomplete combustion contain particulate matter (PM), carbon monoxide, nitrogen and sulfur oxides, and many organic compounds such as carcinogens, e.g. (or including) polycyclic hydrocarbons (Lewtas, 2007, Forum of International Respiratory Studies (FIRS) Task Force on Health Effects of Biomass Exposure, 2008). In light of the high concentrations of the many pollutants, exposure to indoor air pollution presents a huge global public health concern (WHO International Agency for Research on Cancer Monograph Working Group, 2006, Naeher et al., 2007). The Global Burden of Disease project (GBD-2010) has estimated that household air pollution due to the use of solid cookfuels is responsible for about 3.9 million premature deaths each year, and about 4.8% of the global burden of disease (Smith et al., 2014). Based on evidence in both humans and experimental animals, exposure to indoor emissions from household combustion of coal has been concluded as a carcinogen to human, while biomass-smoke exposure (mainly wood) is a probable carcinogen to human (Straif et al., 2006). Although the amount of indoor air pollution exposure depends on the type of fuel used, the nature of the combustion, the location and the length of time exposed to polluted environment, women and children who are at home for most of the day are the most vulnerable (IARC, 2010). Further, there has been evidence linked to early-life (prenatal, infants, children and adolescents) periods exposure to air pollution with adulthood health effects in both animal and human studies (Soto-Martinez and Sly, 2010, Weldy et al., 2013). Although the underlying biological mechanisms are not clear, one possible mechanism is that there are epigenetic alterations resulting from these exposures, which play a role in the development of adverse health effects.

It is now widely acknowledged that epigenetic alterations can have various impacts on disease susceptibility and development. As an important mechanism of epigenetic changes, aberrant DNA methylation, including loss of genome-wide (global) methylation and site-specific hypermethylation, has been attributed to carcinogenesis and many other diseases (Baylin and Jones, 2011, Brennan and Flanagan, 2012). The level of DNA methylation is sensitive to various types of environmental exposures including benzene, arsenic, lead, persistent organic pollutants, as well as air pollutants, especially the exposures during early-life period (Bernal and Jirtle, 2010, Lambrou et al., 2012, Tang et al., 2012, Janssen et al., 2013). There is a large literature on DNA methylation alterations at the tissue level; more recently, peripheral blood DNA methylation changes in white blood cells have also been investigated as risk factor or potential cancer risk markers in some studies (Terry et al., 2011). However, data on how exposure to indoor air pollution both over the lifetime and during different periods of the lifetime is related to global methylation in blood DNA are still very limited.

Insulin-like growth factor 2 (IGF2) is one of two ligands within the genome׳s insulin network, and is necessary for the proper control of somatic growth, especially throughout early life (Werner and Le Roith, 2000, Livingstone, 2013). The IGF2/H19 gene locus is involved in early development through DNA methylation, and is one of the best studied imprinted genomic loci (Ollikainen and Craig, 2011). Genomic imprinting is a form of gene silencing that is regulated by gene-specific imprinting control regions (ICRs) through parent-of-origin differential methylation (Bell and Felsenfeld, 2000). Both animal models and human studies have shown that adverse prenatal environmental exposure is associated with subsequent IGF2 ICR methylation disruption (Wu et al., 2004, Heijmans et al., 2008), suggesting this may be an “environmental sensor” or biomarker of environment exposure. There are a few studies of the associations of early-life exposure to indoor air pollution with methylation of IGF2/H19 ICR in blood DNA from women.

To better understand the relationship of exposure to indoor air pollution from solid fuels at different lifetime periods with blood DNA methylation levels, we evaluated global DNA methylation and methylation levels of IGF2/H19 ICR in peripheral blood in population-based women who had never smoked cigarettes.

Section snippets

Study population

The study population was derived from the population-based controls of a case-control study of lung cancer conducted in Warsaw, Poland during 1998–2001. The population-based controls were randomly selected from the electronic registry of residents of Warsaw, Poland, and were frequency-matched to cases by age group (±3 years), geographic area, and gender. Details of the recruitment methods have been published elsewhere (Lissowska et al., 2005, Zeka et al., 2006). Interviews were completed for

Results

Table 1 summarizes selected characteristics of never-smoking women with DNA samples from Warsaw, Poland. Among them, 34 (80.9%) reported ever used any solid fuel at homes during their lifetime, with the mean lifetime duration of exposure of 27.0 years. The main solid fuel exposure type was coal, with 24 (57.1%) women having used coal and 7 (16.7%) having used both coal and wood during their lifetime. The mean level of LUMA methylation was 68.5% among 42 participants in the study population.

Discussion

To our knowledge, this is the first population-based study to access associations of exposure to indoor air pollution from solid fuels with global DNA methylation in peripheral blood. We found that ever exposure to indoor air pollution from solid fuel was associated with decreased levels of global methylation in peripheral blood among never-smoking women. Similarly, using both coal and wood for heating or cooking before age 20 was associated with reduction in global DNA methylation. Our

Conflict of interest

No potential conflicts of interest were disclosed.

Funding sources

This work was supported by Mount Sinai Children׳s Environmental Health Center (CEHC Pilot Grant Program 0285-7451) and the European Commission׳s Inco-Copernicus Programme (Contract IC15-CT96-0313). In Warsaw, the study was supported by a grant from the Polish State Committee for Scientific Research (Grant SPUB-M-COPERNICUS/P-05/DZ-30/99/2000). Regina Martinez worked on this study under Mount Sinai Undergraduate Research Scholarship.

Acknowledgments

This study would not have been possible without the support of all the study participants and the research staffs from Warsaw, Poland. The authors thank G. Ferro for his expertise regarding data management.

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Indoor air pollution from solid fuels and peripheral Blood DNA methylation: Findings from a population study in Warsaw, Poland

Highlights

Abstract

Introduction

Section snippets

Study population

Results

Discussion

Conflict of interest

Funding sources

Acknowledgments

Environ. Int.

Exp. Cell Res.

Mutat. Res.

Lancet Oncol.

Rapid DNA methylation changes after exposure to traffic particles

Am. J. Respir. Crit. Care Med.

A decade of exploring the cancer epigenome – biological and translational implications

Nat. Rev. Cancer

Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene

Nature

Epigenomic disruption: the effects of early developmental exposures

Birth Defects Res. A: Clin. Mol. Teratol.

Epigenetic epidemiology for cancer risk: harnessing germline epigenetic variation

Methods Mol. Biol.

Prenatal tobacco smoke exposure affects global and gene-specific DNA methylation

Am. J. Respir. Crit. Care Med.

Prenatal tobaccosmoke exposure and genomic DNA methylation in a multiethnic birth cohort

Cancer Epidemiol. Biomarker Prev.

The role of developmental plasticity and epigenetics in human health

Birth Defects Res. C: Embryo Today Rev.

Global DNA hypomethylation is associated with in utero exposure to cotinine and perfluorinated alkyl compounds

Epigenetics

Persistent epigenetic differences associated with prenatal exposure to famine in humans

Proc. Natl. Acad. Sci. USA

Placental DNA hypomethylation in association with particulate air pollution in early life

Part. Fibre Toxicol.

A panel study of occupational exposure to fine particulate matter and changes in DNA methylation over a single workday and years worked in boilermaker welders

Environ. Health

Effects of paternal folate deficiency on the expression of insulin-like growth factor-2 and global DNA methylation in the fetal brain

Mol. Nutr. Food Res.

Arsenic exposure and DNA methylation among elderly men

Epidemiology

Cigarette smoking and DNA methylation

Front. Genet.

Lung cancer and indoor pollution from heating and cooking with solid fuels: the IARC international multicentre case-control study in Eastern/Central Europe and the United Kingdom

Am. J. Epidemiol.