Abstract
This study’s aim was to investigate the post-effect of an air quality improvement on systemic inflammation and circulating microparticles in asthmatic patients during, and 2 months after, the Beijing Olympics 2008. We measured the levels of circulating inflammatory cytokines and microparticles in the peripheral blood from asthma patients and healthy controls during (phase 1), and 2 months after (phase 2) the Beijing 2008 Olympic Games. The concentrations of circulating cytokines (including TNFα, IL-6, IL-8, and IL-10) were still seen reduced in phase 2 when compared with those in phase 1. The number of circulating endothelial cell-derived microparticles was significantly lower during the phase 2 than that during phase 1 in asthma patients. The level of plasma lipopolysaccharide-binding protein (LBP) was significantly decreased in asthmatics in phase 2. The level of norepinephrine was significantly higher in phase 2 than that in phase 1 in plasma from both asthma patients and healthy subjects. There were no significant differences in the gene profile for the toll-like receptor (TLR) signaling from peripheral blood mononuclear cells. In vitro, microvesicles from patients with asthma impaired the relaxation to bradykinin and contraction to acetylcholine, whereas microparticles from healthy subjects did not. These data suggested that reduction in systemic pro-inflammatory responses and circulating LBP and increased level of norepinephrine in asthma patients persisted even after 2 months of the air pollution intervention. These changes were independent of the TLR signaling pathway. Circulating microparticles might be associated with airway smooth muscle dysfunction.
Similar content being viewed by others
References
Pope, C.A. 3rd, R.T. Burnett, G.D. Thurston, M.J. Thun, E.E. Calle, et al. 2004. Cardiovascular mortality and long-term exposure to particulate air pollution: epidemiological evidence of general pathophysiological pathways of disease. Circulation 109: 71–77.
Miller, K.A., D.S. Siscovick, L. Sheppard, K. Shepherd, J.H. Sullivan, et al. 2007. Long-term exposure to air pollution and incidence of cardiovascular events in women. The New England Journal of Medicine 356: 447–458.
Rich, D.Q., H.M. Kipen, W. Huang, G. Wang, Y. Wang, et al. 2012. Association between changes in air pollution levels during the Beijing Olympics and biomarkers of inflammation and thrombosis in healthy young adults. JAMA 307: 2068–2078.
Amabile, N., A.P. Guerin, A. Leroyer, Z. Mallat, C. Nguyen, et al. 2005. Circulating endothelial microparticles are associated with vascular dysfunction in patients with end-stage renal failure. Journal of the American Society of Nephrology 16: 3381–3388.
Huang, W., G. Wang, S.E. Lu, H. Kipen, Y. Wang, et al. 2012. Inflammatory and oxidative stress responses of healthy young adults to changes in air quality during the Beijing Olympics. American Journal of Respiratory and Critical Care Medicine 186: 1150–1159.
Bateman, E.D., S.S. Hurd, P.J. Barnes, J. Bousquet, J.M. Drazen, et al. 2008. Global strategy for asthma management and prevention: GINA executive summary. The European Respiratory Journal 31: 143–178.
Periard, D., C.M. Boulanger, S. Eyer, N. Amabile, P. Pugin, et al. 2007. Are circulating endothelial-derived and platelet-derived microparticles a pathogenic factor in the cisplatin-induced stroke? Stroke 38: 1636–1638.
Ayers, L., B. Ferry, S. Craig, D. Nicoll, J.R. Stradling, et al. 2009. Circulating cell-derived microparticles in patients with minimally symptomatic obstructive sleep apnoea. The European Respiratory Journal 33: 574–580.
Xu, X., F. Deng, X. Guo, P. Lv, M. Zhong, et al. 2012. Association of systemic inflammation with marked changes in particulate air pollution in Beijing in 2008. Toxicology Letters 212: 147–156.
Wu, S., F. Deng, J. Niu, Q. Huang, Y. Liu, et al. 2010. Association of heart rate variability in taxi drivers with marked changes in particulate air pollution in Beijing in 2008. Environmental Health Perspectives 118: 87–91.
Wang, W., T. Primbs, S. Tao, and S.L. Simonich. 2009. Atmospheric particulate matter pollution during the 2008 Beijing Olympics. Environmental Science & Technology 43: 5314–5320.
Carnow, B.W., R.M. Senior, R. Karsh, S. Wessler, and L.V. Avioli. 1970. The role of air pollution in chronic obstructive pulmonary disease. JAMA 214: 894–899.
Viegi, G., S. Maio, F. Pistelli, S. Baldacci, and L. Carrozzi. 2006. Epidemiology of chronic obstructive pulmonary disease: health effects of air pollution. Respirology 11: 523–532.
Andersen, Z.J., M. Hvidberg, S.S. Jensen, M. Ketzel, S. Loft, et al. 2011. Chronic obstructive pulmonary disease and long-term exposure to traffic-related air pollution: a cohort study. American Journal of Respiratory and Critical Care Medicine 183: 455–461.
Bruske, I., R. Hampel, M.M. Socher, R. Ruckerl, A. Schneider, et al. 2010. Impact of ambient air pollution on the differential white blood cell count in patients with chronic pulmonary disease. Inhalation Toxicology 22: 245–252.
van Eeden, S.F., W.C. Tan, T. Suwa, H. Mukae, T. Terashima, et al. 2001. Cytokines involved in the systemic inflammatory response induced by exposure to particulate matter air pollutants (PM(10)). American Journal of Respiratory and Critical Care Medicine 164: 826–830.
Milutinovic, S., D. Nikic, L. Stosic, A. Stankovic, and D. Bogdanovic. 2009. Short-term association between air pollution and emergency room admissions for chronic obstructive pulmonary disease in Nis, Serbia. Central European Journal of Public Health 17: 8–13.
Anderson, H.R., C. Spix, S. Medina, J.P. Schouten, J. Castellsague, et al. 1997. Air pollution and daily admissions for chronic obstructive pulmonary disease in 6 European cities: results from the APHEA project. The European Respiratory Journal 10: 1064–1071.
Schikowski, T., D. Sugiri, U. Ranft, U. Gehring, J. Heinrich, et al. 2005. Long-term air pollution exposure and living close to busy roads are associated with COPD in women. Respiratory Research 6: 152.
Pope, C.A. 3rd, R.T. Burnett, M.J. Thun, E.E. Calle, D. Krewski, et al. 2002. Lung cancer, cardiopulmonary mortality, and long-term exposure to fine particulate air pollution. JAMA 287: 1132–1141.
Hoek, G., B. Brunekreef, S. Goldbohm, P. Fischer, and P.A. van den Brandt. 2002. Association between mortality and indicators of traffic-related air pollution in the Netherlands: A cohort study. Lancet 360: 1203–1209.
Halatek, T., M. Stepnik, J. Stetkiewicz, A. Krajnow, B. Kur, et al. 2011. The inflammatory response in lungs of rats exposed on the airborne particles collected during different seasons in four European cities. Journal of Environmental Science and Health. Part A, Toxic/Hazardous Substances & Environmental Engineering 46: 1469–1481.
Andersen, Z.J., K. Bonnelykke, M. Hvidberg, S.S. Jensen, M. Ketzel, et al. 2012. Long-term exposure to air pollution and asthma hospitalisations in older adults: a cohort study. Thorax 67: 6–11.
Koenig, J.Q. 1999. Air pollution and asthma. The Journal of Allergy and Clinical Immunology 104: 717–722.
Li, Y., W. Wang, H. Kan, X. Xu, and B. Chen. 2010. Air quality and outpatient visits for asthma in adults during the 2008 Summer Olympic Games in Beijing. Sci Total Environ 408: 1226–1227.
Mutlu, G.M., D. Green, A. Bellmeyer, C.M. Baker, Z. Burgess, et al. 2007. Ambient particulate matter accelerates coagulation via an IL-6-dependent pathway. The Journal of Clinical Investigation 117: 2952–2961.
Thompson, A.M., A. Zanobetti, F. Silverman, J. Schwartz, B. Coull, et al. 2010. Baseline repeated measures from controlled human exposure studies: associations between ambient air pollution exposure and the systemic inflammatory biomarkers IL-6 and fibrinogen. Environmental Health Perspectives 118: 120–124.
Xu, X., Z. Yavar, M. Verdin, Z. Ying, G. Mihai, et al. 2010. Effect of Early Particulate Air Pollution Exposure on Obesity in Mice: Role of p47phox. Arteriosclerosis, Thrombosis, and Vascular Biology 30: 2518–2527.
Calderon-Garciduenas, L., R. Villarreal-Calderon, G. Valencia-Salazar, C. Henriquez-Roldan, P. Gutierrez-Castrellon, et al. 2008. Systemic inflammation, endothelial dysfunction, and activation in clinically healthy children exposed to air pollutants. Inhalation Toxicology 20: 499–506.
Dandona, P., A. Aljada, and A. Bandyopadhyay. 2004. Inflammation: the link between insulin resistance, obesity and diabetes. Trends in Immunology 25: 4–7.
Hotamisligil, G.S. 2006. Inflammation and metabolic disorders. Nature 444: 860–867.
Houstis, N., E.D. Rosen, and E.S. Lander. 2006. Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 440: 944–948.
Shoelson, S.E., J. Lee, and A.B. Goldfine. 2006. Inflammation and insulin resistance. The Journal of Clinical Investigation 116: 1793–1801.
Su, G.L., R.L. Simmons, and S.C. Wang. 1995. Lipopolysaccharide binding protein participation in cellular activation by LPS. Critical Reviews in Immunology 15: 201–214.
Wright, S.D., R.A. Ramos, P.S. Tobias, R.J. Ulevitch, and J.C. Mathison. 1990. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science 249: 1431–1433.
Dubin, W., T.R. Martin, P. Swoveland, D.J. Leturcq, A.M. Moriarty, et al. 1996. Asthma and endotoxin: lipopolysaccharide-binding protein and soluble CD14 in bronchoalveolar compartment. The American Journal of Physiology 270: L736–L744.
Martin, T.R., J.C. Mathison, P.S. Tobias, D.J. Leturcq, A.M. Moriarty, et al. 1992. Lipopolysaccharide binding protein enhances the responsiveness of alveolar macrophages to bacterial lipopolysaccharide. Implications for cytokine production in normal and injured lungs. The Journal of Clinical Investigation 90: 2209–2219.
Brass, D.M., J.D. Savov, G.S. Whitehead, A.B. Maxwell, and D.A. Schwartz. 2004. LPS binding protein is important in the airway response to inhaled endotoxin. The Journal of Allergy and Clinical Immunology 114: 586–592.
Imrich, A., Y. Ning, and L. Kobzik. 2000. Insoluble components of concentrated air particles mediate alveolar macrophage responses in vitro. Toxicology and Applied Pharmacology 167: 140–150.
Soukup, J.M., and S. Becker. 2001. Human alveolar macrophage responses to air pollution particulates are associated with insoluble components of coarse material, including particulate endotoxin. Toxicology and Applied Pharmacology 171: 20–26.
Becker, S., M.J. Fenton, and J.M. Soukup. 2002. Involvement of microbial components and toll-like receptors 2 and 4 in cytokine responses to air pollution particles. American Journal of Respiratory Cell and Molecular Biology 27: 611–618.
Dignat-George, F., L. Camoin-Jau, F. Sabatier, D. Arnoux, F. Anfosso, et al. 2004. Endothelial microparticles: a potential contribution to the thrombotic complications of the antiphospholipid syndrome. Thrombosis and Haemostasis 91: 667–673.
Faure, V., L. Dou, F. Sabatier, C. Cerini, J. Sampol, et al. 2006. Elevation of circulating endothelial microparticles in patients with chronic renal failure. Journal of Thrombosis and Haemostasis 4: 566–573.
Sabatier, F., P. Darmon, B. Hugel, V. Combes, M. Sanmarco, et al. 2002. Type 1 and type 2 diabetic patients display different patterns of cellular microparticles. Diabetes 51: 2840–2845.
Simoncini, S., M.S. Njock, S. Robert, L. Camoin-Jau, J. Sampol, et al. 2009. TRAIL/Apo2L mediates the release of procoagulant endothelial microparticles induced by thrombin in vitro: a potential mechanism linking inflammation and coagulation. Circulation Research 104: 943–951.
Sun, Q., X. Hong, and L.E. Wold. 2010. Cardiovascular effects of ambient particulate air pollution exposure. Circulation 121: 2755–2765.
Acknowledgements
This work was supported in part by the National Natural Sciences Foundation of China grant (nos. 81170040 and 81470229 to J. Gao), National Institute of Health grants (ES016588, ES017412, ES018900 to Q. Sun).
The authors acknowledge Professor Roy Pleasants of Duke University for critical reading and editing of this manuscript. The authors thank Yi Ma for the technical support in the measurement of lung function and Ms. Jessica Ruby for editing of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.
Competing Interests
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Gao, J., Xu, X., Ying, Z. et al. Post-Effect of Air Quality Improvement on Biomarkers for Systemic Inflammation and Microparticles in Asthma Patients After the 2008 Beijing Olympic Games: a Pilot Study. Inflammation 40, 1214–1224 (2017). https://doi.org/10.1007/s10753-017-0564-y
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10753-017-0564-y