Systemic inflammatory changes and increased oxidative stress in rural Indian women cooking with biomass fuels

https://doi.org/10.1016/j.taap.2012.04.004Get rights and content

Abstract

The study was undertaken to investigate whether regular cooking with biomass aggravates systemic inflammation and oxidative stress that might result in increase in the risk of developing cardiovascular disease (CVD) in rural Indian women compared to cooking with a cleaner fuel like liquefied petroleum gas (LPG). A total of 635 women (median age 36 years) who cooked with biomass and 452 age-matched control women who cooked with LPG were enrolled. Serum interleukin-6 (IL-6), C-reactive protein (CRP), tumor necrosis factor-alpha (TNF-α) and interleukin-8 (IL-8) were measured by ELISA. Generation of reactive oxygen species (ROS) by leukocytes was measured by flow cytometry, and erythrocytic superoxide dismutase (SOD) was measured by spectrophotometry. Hypertension was diagnosed following the Seventh Report of the Joint Committee. Tachycardia was determined as pulse rate > 100 beats per minute. Particulate matter of diameter less than 10 and 2.5 μm (PM10 and PM2.5, respectively) in cooking areas was measured using real-time aerosol monitor. Compared with control, biomass users had more particulate pollution in indoor air, their serum contained significantly elevated levels of IL-6, IL-8, TNF-α and CRP, and ROS generation was increased by 37% while SOD was depleted by 41.5%, greater prevalence of hypertension and tachycardia compared to their LPG-using neighbors. PM10 and PM2.5 levels were positively associated with markers of inflammation, oxidative stress and hypertension. Inflammatory markers correlated with raised blood pressure. Cooking with biomass exacerbates systemic inflammation, oxidative stress, hypertension and tachycardia in poor women cooking with biomass fuel and hence, predisposes them to increased risk of CVD development compared to the controls. Systemic inflammation and oxidative stress may be the mechanistic factors involved in the development of CVD.

Highlights

► Effect of chronic biomass smoke exposure on cardiovascular health was investigated. ► Serum markers of systemic inflammation and oxidative stress were studied. ► Biomass using women had increased systemic inflammation and oxidative stress. ► Indoor air pollution and observed changes were positively associated.

Introduction

Unprocessed solid biomass such as dried cow dung cake, wood and crop residues is still used for cooking and room heating in a majority of rural households in India and neighboring countries. For example, 72% households in India, 88% in Bangladesh, 80% in Nepal, 72% in Pakistan and 67% in Sri Lanka use biomass for daily household cooking (WHO, 2006). Poverty is the main reason behind the use of biomass as most of the rural people can't afford cleaner fuel with their modest income. Besides, cleaner fuels such as compressed natural gas or liquefied petroleum gas (LPG) are not readily available in the remote villages. Cooking in the Indian villages is generally done by the womenfolk in traditional earthen ovens in poorly ventilated kitchen. Since biomass is not combustion efficient, it emits high level of smoke that causes severe indoor air pollution (IAP).

Biomass smoke contains a wide spectrum of potentially health-damaging pollutants that include coarse, fine and ultrafine particles, carbon monoxide (CO), oxides of nitrogen and sulfur, transitional metals, polycyclic aromatic hydrocarbons, volatile organic compounds and bioaerosols (Morawska and Zhang, 2002, Smith, 2000). The level of particulate matter of less than 10 μm in diameter (PM10) in biomass-using households in India especially during cooking time far exceeds traffic-generated PM10 level in the cities (Balakrishnan et al., 2002, Ezzati and Kammen, 2002, Smith, 1993). Ultrafine particles (UFPs) having a diameter of less than 0.1 μm represent a substantial proportion of particulate pollutants in biomass smoke (Naeher et al., 2005). Inhaled UFPs can readily cross the alveolar-capillary barrier reaching the blood stream (Elder and Oberdörster, 2006, Nemmar et al., 2002). In circulation, UFPs adsorb onto the surface of erythrocytes and can travel to all vital organs of the body including the brain (Oberdörster et al., 2004). Therefore, exposure to biomass smoke can mediate systemic alterations besides its adverse effects on the lung and the airways. In conformity with this, we have recently reported greater prevalence of hypertension among relatively young, never-smoking housewives of rural India who cooked exclusively with biomass than their age- and sex-matched neighbors who cooked with LPG (Dutta et al., 2011).

The mechanism of hypertension among biomass users, however, is currently unknown. An intimate relationship exists between inflammation, endothelial dysfunction and hypertension (Tycinska et al., 2011). Subtle or overt activation of inflammatory mediators is frequent among hypertensives (Laffer and Elijovich, 2010). In fact, hypertension has been considered in part as an inflammatory disorder (Gupta et al., 2011, Montecucco et al., 2011). Inflammation may lead to oxidative stress and up-regulated production of blood coagulation proteins that increase the risk of cardiovascular diseases (Knol et al., 2009) primarily by potentiating blood pressure (Ibald-Mulli et al., 2001, Touyz and Briones, 2011, Urch et al., 2005). Oxidative stress and endothelial dysfunction are consistently observed in hypertensive subjects, and accumulating evidence suggests that they also have a causal role in the molecular processes leading to hypertension (Touyz and Briones, 2011).

PM10, PM2.5 (particulate matter of less than 2.5 μm in diameter) and UFPs present in biomass smoke are able to mediate oxidative stress and to produce pro-inflammatory mediators that may lead to pulmonary as well as systemic inflammation (Donaldson et al., 2001, Donaldson et al., 2005, Pope et al., 2004). PMs induce liver to produce pro-inflammatory mediators interleukin-6 (IL-6) and C-reactive protein (CRP; Delfino et al., 2009, Hertel et al., 2010), and blood coagulation proteins (Metassan et al., 2010). Elevation of CRP in human blood accompanies inflammation and cardiovascular diseases (CVDs; Kusche-Vihrog et al., 2011). CRP causes stiffness of vascular endothelium and consequent development of hypertension (Kusche-Vihrog et al., 2011). Inflammation may lead to oxidative stress. Oxidative stress is tightly regulated by a balance between production of reactive oxygen species (ROS) such as superoxides and hydrogen peroxides and their removal by antioxidant enzymes including superoxide dismutases (SODs), heme oxygenase-1, NAD(P)H quinone oxidoreductase-1, catalase and thioredoxin. ROS are natural byproducts of metabolism and these molecules play important roles in cell signaling. However, excessive levels of ROS due to up-regulated production and/or decreased removal by antioxidants can be toxic to the cells (Gao and Mann, 2009, Lee et al., 2005, Mann et al., 2007, Motohashi and Yamamoto, 2004). Collectively, these reports suggest that chronic inhalation of biomass smoke may lead to inflammation and oxidative stress which, in turn, can raise arterial blood pressure.

Though there have been numerous studies from the western world, there have been very few reports on this aspect from this part of the world, especially from India. We found it utterly necessary to undertake such a study in India as conditions in the developing countries like India vary greatly from the conditions of the developed countries of the western world. We aimed to study if biomass smoke aggravated systemic inflammation and oxidative stress in a group of never-smoking, poor rural women in eastern India who cooked exclusively with biomass for the past five years or more compared to their neighbors those who cooked with liquefied petroleum gas (LPG), a relatively cleaner fuel. For this, we examined the biomarkers of inflammation and oxidative stress that are well-established by renowned scientists of the western world. We also examined if there was any possible impact on their arterial blood pressure.

Section snippets

Participant recruitment and sample size

This cross-sectional study was conducted in 6 villages in Hooghly, Howrah, Burdwan and Birbhum districts of West Bengal, a state in eastern India. The villages were selected on the basis of the following criteria: i. the location should be at least 5 km away from the national or state highways to minimize the impact of vehicular pollution, ii. no air-polluting industry like coal-based thermal power plant, brick kiln, sponge iron factory and rice mill within 5 km radius in order to control the

Demographic characteristics of the participants

Demographic and socio-economic characteristics of biomass- and LPG-using women are compared in Table 1. It is apparent that the two groups were well-matched with respect to age, body mass index (BMI), years and hours of cooking, passive smoking due to presence of smokers in the family, food habit, and number of family members. However, they differed significantly (p < 0.05) with respect to education, family income and presence of separate kitchen. Compared with controls, biomass users were less

Discussion

This study has shown that chronic inhalation of smoke during daily household cooking with biomass aggravates oxidative stress and systemic inflammation, and increases the prevalence of hypertension and tachycardia among women in rural India. Like the present finding, a Guatemalan study has earlier shown higher prevalence of hypertension in women who cooked exclusively with biomass (McCracken et al., 2007). Since hypertension and tachycardia are known risk factors for CVD (Whitworth, 2005),

Conflict of interest

The authors declare that there are no conflicts of interest.

Acknowledgments

The study was funded by Council of Scientific and Industrial Research, India and Central Pollution Control Board, Delhi under Ministry of Environment and Forests, Government of India.

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