Journal of Preventive Medicine and Public Health

The Korean Society for Preventive Medicine (대한예방의학회)
권호 표지
DOI QR코드

DOI QR Code

Physical Activity- and Alcohol-dependent Association Between Air Pollution Exposure and Elevated Liver Enzyme Levels: An Elderly Panel Study

  • Kim, Kyoung-Nam (Department of Preventive Medicine, Seoul National University College of Medicine) ;
  • Lee, Hyemi (Department of Preventive Medicine, Seoul National University College of Medicine) ;
  • Kim, Jin Hee (Department of Environmental Health, Graduate School of Public Health, Seoul National University) ;
  • Jung, Kweon (Seoul Metropolitan Institute of Public Health and Environment) ;
  • Lim, Youn-Hee (Institute of Environmental Medicine, Seoul National University Medical Research Center) ;
  • Hong, Yun-Chul (Department of Preventive Medicine, Seoul National University College of Medicine)
  • Received : 2015.02.23
  • Accepted : 2015.04.30
  • Published : 2015.05.31
Download PDF
⟨ Previous Next ⟩

Abstract

Objectives: The deleterious effects of air pollution on various health outcomes have been demonstrated. However, few studies have examined the effects of air pollution on liver enzyme levels. Methods: Blood samples were drawn up to three times between 2008 and 2010 from 545 elderly individuals who regularly visited a community welfare center in Seoul, Korea. Data regarding ambient air pollutants (particulate matter ${\leq}2.5{\mu}m$ [$PM_{2.5}$], nitrogen dioxide [$NO_2$], ozone [$O_3$], carbon monoxide, and sulfur dioxide) from monitoring stations were used to estimate air pollution exposure. The effects of the air pollutants on the concentrations of three liver enzymes (aspartate aminotransferase [AST], alanine aminotransferase [ALT], and ${\gamma}$-glutamyltranspeptidase [${\gamma}$-GTP)]) were evaluated using generalized additive and linear mixed models. Results: Interquartile range increases in the concentrations of the pollutants showed significant associations of $PM_{2.5}$ with AST (3.0% increase, p=0.0052), ALT (3.2% increase, p=0.0313), and ${\gamma}$-GTP (5.0% increase, p=0.0051) levels; $NO_2$ with AST (3.5% increase, p=0.0060) and ALT (3.8% increase, p=0.0179) levels; and $O_3$ with ${\gamma}$-GTP (5.3% increase, p=0.0324) levels. Significant modification of these effects by exercise and alcohol consumption was found (p for interaction <0.05). The effects of air pollutants were greater in non-exercisers and heavy drinkers. Conclusions: Short-term exposure to air pollutants such as $PM_{2.5}$, $NO_2$, and $O_3$ is associated with increased liver enzyme levels in the elderly. These adverse effects can be reduced by exercising regularly and abstinence from alcohol.

Keywords

References

  1. Burnett RT, Stieb D, Brook JR, Cakmak S, Dales R, Raizenne M, et al. Associations between short-term changes in nitrogen dioxide and mortality in Canadian cities. Arch Environ Health 2004;59(5):228-236. https://doi.org/10.3200/AEOH.59.5.228-236
  2. de Kok TM, Driece HA, Hogervorst JG, Briede JJ. Toxicological assessment of ambient and traffic-related particulate matter: a review of recent studies. Mutat Res 2006;613(2-3):103-122. https://doi.org/10.1016/j.mrrev.2006.07.001
  3. Hong YC, Lee JT, Kim H, Kwon HJ. Air pollution: a new risk factor in ischemic stroke mortality. Stroke 2002;33(9):2165-2169. https://doi.org/10.1161/01.STR.0000026865.52610.5B
  4. Maynard D, Coull BA, Gryparis A, Schwartz J. Mortality risk associated with short-term exposure to traffic particles and sulfates. Environ Health Perspect 2007;115(5):751-755. https://doi.org/10.1289/ehp.9537
  5. Pope CA 3rd, Dockery DW. Health effects of fine particulate air pollution: lines that connect. J Air Waste Manag Assoc 2006; 56(6):709-742. https://doi.org/10.1080/10473289.2006.10464485
  6. Kim JH, Hong YC. GSTM1, GSTT1, and GSTP1 polymorphisms and associations between air pollutants and markers of insulin resistance in elderly Koreans. Environ Health Perspect 2012; 120(10):1378-1384. https://doi.org/10.1289/ehp.1104406
  7. Zhao J, Gao Z, Tian Z, Xie Y, Xin F, Jiang R, et al. The biological effects of individual-level PM(2.5) exposure on systemic immunity and inflammatory response in traffic policemen. Occup Environ Med 2013;70(6):426-431. https://doi.org/10.1136/oemed-2012-100864
  8. Lim YH, Kim H, Kim JH, Bae S, Park HY, Hong YC. Air pollution and symptoms of depression in elderly adults. Environ Health Perspect 2012;120(7):1023-1028. https://doi.org/10.1289/ehp.1104100
  9. Kelly FJ. Oxidative stress: its role in air pollution and adverse health effects. Occup Environ Med 2003;60(8):612-616. https://doi.org/10.1136/oem.60.8.612
  10. Kim JH, Choi YH, Bae S, Park HY, Hong YC. eNOS gene polymorphisms modify the association of PM(10) with oxidative stress. Toxicol Lett 2012;214(3):263-267. https://doi.org/10.1016/j.toxlet.2012.09.006
  11. Moller P, Folkmann JK, Forchhammer L, Brauner EV, Danielsen PH, Risom L, et al. Air pollution, oxidative damage to DNA, and carcinogenesis. Cancer Lett 2008;266(1):84-97. https://doi.org/10.1016/j.canlet.2008.02.030
  12. Nel A. Atmosphere. Air pollution-related illness: effects of particles. Science 2005;308(5723):804-806. https://doi.org/10.1126/science.1108752
  13. Romieu I, Moreno-Macias H, London SJ. Gene by environment interaction and ambient air pollution. Proc Am Thorac Soc 2010; 7(2):116-122. https://doi.org/10.1513/pats.200909-097RM
  14. Rossner P Jr, Svecova V, Milcova A, Lnenickova Z, Solansky I, Sram RJ. Seasonal variability of oxidative stress markers in city bus drivers. Part I. Oxidative damage to DNA. Mutat Res 2008; 642(1-2):14-20. https://doi.org/10.1016/j.mrfmmm.2008.03.003
  15. Yamada J, Tomiyama H, Yambe M, Koji Y, Motobe K, Shiina K, et al. Elevated serum levels of alanine aminotransferase and gamma glutamyltransferase are markers of inflammation and oxidative stress independent of the metabolic syndrome. Atherosclerosis 2006;189(1):198-205. https://doi.org/10.1016/j.atherosclerosis.2005.11.036
  16. Lioudaki E, Ganotakis ES, Mikhailidis DP. Liver enzymes: potential cardiovascular risk markers? Curr Pharm Des 2011;17(33): 3632-3643. https://doi.org/10.2174/138161211798220945
  17. Rosen P, Nawroth PP, King G, Moller W, Tritschler HJ, Packer L. The role of oxidative stress in the onset and progression of diabetes and its complications: a summary of a Congress Series sponsored by UNESCO-MCBN, the American Diabetes Association and the German Diabetes Society. Diabetes Metab Res Rev 2001;17(3):189-212. https://doi.org/10.1002/dmrr.196
  18. Tomaru M, Takano H, Inoue K, Yanagisawa R, Osakabe N, Yasuda A, et al. Pulmonary exposure to diesel exhaust particles enhances fatty change of the liver in obese diabetic mice. Int J Mol Med 2007;19(1):17-22.
  19. Targher G. Elevated serum gamma-glutamyltransferase activity is associated with increased risk of mortality, incident type 2 diabetes, cardiovascular events, chronic kidney disease and cancer-a narrative review. Clin Chem Lab Med 2010;48(2): 147-157. https://doi.org/10.1515/CCLM.2010.031
  20. Tan HH, Fiel MI, Sun Q, Guo J, Gordon RE, Chen LC, et al. Kupffer cell activation by ambient air particulate matter exposure may exacerbate non-alcoholic fatty liver disease. J Immunotoxicol 2009;6(4):266-275. https://doi.org/10.3109/15476910903241704
  21. Markevych I, Wolf K, Hampel R, Breitner S, Schneider A, von Klot S, et al. Air pollution and liver enzymes. Epidemiology 2013; 24(6):934-935. https://doi.org/10.1097/EDE.0b013e3182a77600
  22. Radak Z, Chung HY, Goto S. Exercise and hormesis: oxidative stress-related adaptation for successful aging. Biogerontology 2005;6(1):71-75. https://doi.org/10.1007/s10522-004-7386-7
  23. Sid B, Verrax J, Calderon PB. Role of oxidative stress in the pathogenesis of alcohol-induced liver disease. Free Radic Res 2013;47(11):894-904. https://doi.org/10.3109/10715762.2013.819428
  24. Radak Z, Chung HY, Naito H, Takahashi R, Jung KJ, Kim HJ, et al. Age-associated increase in oxidative stress and nuclear factor kappaB activation are attenuated in rat liver by regular exercise. FASEB J 2004;18(6):749-750. https://doi.org/10.1096/fj.03-0509fje
  25. Kessova IG, Ho YS, Thung S, Cederbaum AI. Alcohol-induced liver injury in mice lacking Cu, Zn-superoxide dismutase. Hepatology 2003;38(5):1136-1145. https://doi.org/10.1053/jhep.2003.50450
  26. Cederbaum AI, Lu Y, Wu D. Role of oxidative stress in alcohol-induced liver injury. Arch Toxicol 2009;83(6):519-548. https://doi.org/10.1007/s00204-009-0432-0
  27. Robins JM, Rotnitzky A, Zhao LP. Analysis of semiparametric regression models for repeated outcomes in the presence of missing data. J Am Stat Assoc 1995;90(429):106-121. https://doi.org/10.1080/01621459.1995.10476493
  28. Romieu I, Castro-Giner F, Kunzli N, Sunyer J. Air pollution, oxidative stress and dietary supplementation: a review. Eur Respir J 2008;31(1):179-197. https://doi.org/10.1183/09031936.00128106
  29. Monami M, Bardini G, Lamanna C, Pala L, Cresci B, Francesconi P, et al. Liver enzymes and risk of diabetes and cardiovascular disease: results of the Firenze Bagno a Ripoli (FIBAR) study. Metabolism 2008;57(3):387-392. https://doi.org/10.1016/j.metabol.2007.10.015
  30. Strasak AM, Kelleher CC, Klenk J, Brant LJ, Ruttmann E, Rapp K, et al. Longitudinal change in serum gamma-glutamyltransferase and cardiovascular disease mortality: a prospective population-based study in 76,113 Austrian adults. Arterioscler Thromb Vasc Biol 2008;28(10):1857-1865. https://doi.org/10.1161/ATVBAHA.108.170597
  31. Yun KE, Shin CY, Yoon YS, Park HS. Elevated alanine aminotransferase levels predict mortality from cardiovascular disease and diabetes in Koreans. Atherosclerosis 2009;205(2): 533-537. https://doi.org/10.1016/j.atherosclerosis.2008.12.012
  32. Kim HC, Choi KS, Jang YH, Shin HW, Kim DJ. Normal serum aminotransferase levels and the metabolic syndrome: Korean National Health and Nutrition Examination Surveys. Yonsei Med J 2006;47(4):542-550. https://doi.org/10.3349/ymj.2006.47.4.542
  33. Patel DA, Srinivasan SR, Xu JH, Chen W, Berenson GS. Persistent elevation of liver function enzymes within the reference range is associated with increased cardiovascular risk in young adults: the Bogalusa Heart Study. Metabolism 2007;56(6):792-798. https://doi.org/10.1016/j.metabol.2007.01.010
  34. Doi Y, Kubo M, Yonemoto K, Ninomiya T, Iwase M, Tanizaki Y, et al. Liver enzymes as a predictor for incident diabetes in a Japanese population: the Hisayama study. Obesity (Silver Spring) 2007;15(7):1841-1850. https://doi.org/10.1038/oby.2007.218
  35. Monami M, Balzi D, Lamanna C, Melani C, Cocca C, Lotti E, et al. Prognostic value of serum liver enzymes levels in type 2 diabetic patients. Diabetes Metab Res Rev 2007;23(8):625-630. https://doi.org/10.1002/dmrr.744
  36. Meng X, Wang C, Cao D, Wong CM, Kan H. Short-term effect of ambient air pollution on COPD mortality in four Chinese cities. Atmos Environ 2013;77:149–154. https://doi.org/10.1016/j.atmosenv.2013.05.001
  37. Yu BP, Chung HY. Adaptive mechanisms to oxidative stress during aging. Mech Ageing Dev 2006;127(5):436-443. https://doi.org/10.1016/j.mad.2006.01.023
  38. Radak Z, Chung HY, Koltai E, Taylor AW, Goto S. Exercise, oxidative stress and hormesis. Ageing Res Rev 2008;7(1):34-42. https://doi.org/10.1016/j.arr.2007.04.004
  39. Bailey SM, Cunningham CC. Contribution of mitochondria to oxidative stress associated with alcoholic liver disease. Free Radic Biol Med 2002;32(1):11-16. https://doi.org/10.1016/S0891-5849(01)00769-9

Cited by

  1. Residential Proximity to Major Roadways, Fine Particulate Matter, and Hepatic Steatosis : The Framingham Heart Study vol.186, pp.7, 2015, https://doi.org/10.1093/aje/kwx127
  2. Effects of sub-chronic exposure to atmospheric PM2.5on fibrosis, inflammation, endoplasmic reticulum stress and apoptosis in the livers of rats vol.7, pp.2, 2015, https://doi.org/10.1039/c7tx00262a
  3. Association of Ambient Air Pollution with Increased Liver Enzymes in Korean Adults vol.16, pp.7, 2015, https://doi.org/10.3390/ijerph16071213
  4. Long-term exposure to ambient fine particulate matter and liver enzymes in adults: a cross-sectional study in Taiwan vol.76, pp.7, 2019, https://doi.org/10.1136/oemed-2019-105695
  5. Associations between perceived environmental pollution and health-related quality of life in a Chinese adult population vol.18, pp.1, 2020, https://doi.org/10.1186/s12955-020-01442-9
  6. Multi-dimensional community characteristics in linking particulate matter pollution and cause-specific mortality: 72 communities of South Korea vol.196, pp.None, 2021, https://doi.org/10.1016/j.envres.2021.110989
  7. Prenatal and childhood exposure to air pollution and traffic and the risk of liver injury in European children vol.5, pp.3, 2015, https://doi.org/10.1097/ee9.0000000000000153