Association of systemic inflammation with marked changes in particulate air pollution in Beijing in 2008

doi:10.1016/j.toxlet.2012.05.014

Toxicology Letters

Volume 212, Issue 2, 20 July 2012, Pages 147-156

https://doi.org/10.1016/j.toxlet.2012.05.014 Get rights and content

Abstract

Many studies have linked ambient fine particulate matter (aerodynamic diameters less than 2.5 μm, PM_2.5) air pollution to increased morbidity and mortality of cardiovascular diseases in the general population, but the biologic mechanisms of these associations are yet to be elucidated. In this study, we aimed to evaluate the relationship between daily variations in exposure to PM_2.5 and inflammatory responses in mice during and for 2 months after the Beijing Olympic Games. Male C57BL/6 mice were exposed to Beijing PM_2.5 or filtered air (FA) in 2008 during the 2 months of Beijing Olympic and Paralympic Games, and for 2 months after the end of the Games. During the Games, circulating monocyte chemoattractant protein 1 and interleukin 6 were increased significantly in the PM_2.5 exposure group, when compared with the FA control group, although there were no significant inter-group differences in tumor necrosis factor-α or interferon-γ, or in macrophages, neutrophils or lymphocytes in the spleen or thymus between these 2 groups. However, macrophages were significantly increased in the lung and visceral fat with increasing PM_2.5. After the Olympic Games, there were no significant PM_2.5-associated differences for macrophages, neutrophils or lymphocytes in the thymus, but macrophages were significantly elevated in the lung, spleen, subcutaneous and visceral fat with increasing PM_2.5, and the numbers of macrophages were even higher after than those during the Games. Moreover, the number of neutrophils was markedly higher in the spleen for the PM_2.5-exposed- than the FA-group. These data suggest that short-term increases in exposure to ambient PM_2.5 leads to increased systemic inflammatory responses, primarily macrophages and neutrophils in the lung, spleen, and visceral adipose tissue. Short-term air quality improvements were significantly associated with reduced overall inflammatory responses.

Highlights

► During the Games, circulating MCP-1 and IL-6 were increased in the PM_2.5 group. ► Macrophages were increased in the lung and visceral fat with increasing PM_2.5. ► After the Games, macrophages were elevated in lung, spleen, and adipose by PM_2.5. ► After the Games, neutrophils were infiltrated in the spleen by PM_2.5 exposure.

Introduction

Many studies from large population cohorts have provided compelling associations between ambient fine particulate matter (PM_2.5, particles less than 2.5 μm in aerodynamic diameter) air pollution exposure and increased cardiovascular morbidity and mortality (Miller et al., 2007, Pope et al., 2004), but the biologic mechanisms of these associations and underlying factors remain unclear. Although inflammation appears to play a critical role in this process as demonstrated by numerous investigations (Dandona et al., 2004, Hotamisligil, 2006, Shoelson et al., 2006), the systemic responses in inflammation are yet to be elucidated.

The ambient PM_2.5 air pollution in Beijing during the 2008 Olympic and Paralympic Games (from August 8th to September 17th) decreased remarkably as a result of a series of air quality control measurements that were implemented by the Beijing municipal government, including banning the use of more than half of the motor vehicles in Beijing, moving or closing pollution-emitting factories in and around the city, and reducing heavy-duty truck traffic (Wang et al., 2009, Wang et al., 2010). The marked changes of air quality during and after the Olympic Games provided a unique opportunity to investigate the effects of ambient pollutant exposure and the level changes associated with systemic and tissue inflammation. A number of investigations have focused on the effect of air quality improvement on the heart rate variability, asthma and other diseases in human by using this advantage (Li et al., 2010, Liang et al., 2011, Wu et al., 2010, Wu et al., 2011), few studies performed such an investigation on animals. We therefore conducted this study to evaluate the relationship between the PM_2.5 exposure and changes in systemic and tissue inflammation in mice exposed to PM_2.5 air pollution during and after the Olympic Games. The objectives of this study were also to determine whether reduced PM_2.5 air pollution with improved air quality in Beijing during the Olympic Games was associated with a persistent reduction in inflammation.

Section snippets

Animals and diets

Male C57BL/6 mice (8-week-old) were purchased from Animal Center of Peking University (Beijing, China). All groups had access to rodent diet and water ad libitum throughout the study duration. The mice were housed on a 12-h light–dark cycle in a temperature-controlled room at 23 °C. NIH guidelines for the care and use of laboratory animals were strictly followed, and all experiments were approved by the Animal Care and Use Committee at Peking University and the Ohio State University.

Air pollutant exposure

Air

Exposure characterization

As shown in Fig. 1, PM_2.5 exposure levels are presented as daily averaged PM_2.5 mass concentrations measured from the sampling filter of the exposure chamber. The mean of the individual PM_2.5 mass concentrations over the period of the Olympic Games (from August 8th to September 17th, 54.62 ± 5.03 μg/m³) were significantly lower than those of the period after (from September 18th to December 10th, 76.88 ± 7.68 μg/m³, P < 0.05), but still well above the 24-h U.S. National Ambient Air Quality Standard

Discussion

In this study, in view of the significant air quality improvement in Beijing during the 2008 Olympic Games, we assessed real-time, “real world” exposure to PM_2.5 during and after the Olympic Games associated with statistically significant differences in exposure levels, and evaluated the relationship between PM_2.5 and systemic and tissue inflammation with three major inflammatory cell lineages: neutrophil, monocyte/macrophage, and lymphocyte. The main findings of this investigation were that

Conflict of interest statement

There are no competing interests.

Acknowledgements

This work was supported in part by National Institute of Health grant ES016588, ES017412, ES018900 to Dr. Sun, Ministry of Science and Technology of China grant 2006BAI19B06 and National Science Foundation of China grant 30571534 to Dr. Guo. The authors would like to thank Hong Liu at Beijing University for her technical support.

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¹: Contributed equally.

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Association of systemic inflammation with marked changes in particulate air pollution in Beijing in 2008

Abstract

Highlights

Introduction

Section snippets

Animals and diets

Air pollutant exposure

Exposure characterization

Discussion

Conflict of interest statement

Acknowledgements

Trends in Immunology

Science of the Total Environment

Atmospheric Environment

Systemic inflammation, endothelial dysfunction, and activation in clinically healthy children exposed to air pollutants

Inhalation Toxicology

A unique role of monocyte chemoattractant protein 1 among chemokines in adipose tissue of obese subjects

Journal of Clinical Endocrinology and Metabolism

Inflammation, oxidative stress, and obesity

International Journal of Molecular Sciences

Adipose tissue as an endocrine organ: from theory to practice

Journal of Pediatrics (Rio de Janeiro)

Inflammation and metabolic disorders

Nature

Reactive oxygen species have a causal role in multiple forms of insulin resistance

Nature

Granulocyte activation markers in induced sputum: comparison between chronic obstructive pulmonary disease, asthma, and normal subjects

American Journal of Respiratory and Critical Care Medicine

Disease distribution and medical resources during the Beijing 2008 Olympic and Paralympic Games

Chinese Medical Journal (England)

Low doses of urban air particles from Buenos Aires promote oxidative stress and apoptosis in mice lungs

Inhalation Toxicology

Long-term exposure to air pollution and incidence of cardiovascular events in women

New England Journal of Medicine

Ambient particulate matter accelerates coagulation via an IL-6-dependent pathway

Journal of Clinical Investigation

Adipokines in inflammation and metabolic disease

Nature Reviews Immunology