DOI QR코드

DOI QR Code

Cigarette Smoking and Serum Bilirubin Subtypes in Healthy Korean Men: The Korea Medical Institute Study

  • Jo, Jae-Seong (Institute for Health Promotion, Department of Epidemiology and Health Promotion, Yonsei University Graduate School of Public Health) ;
  • Kimm, Hee-Jin (Institute for Health Promotion, Department of Epidemiology and Health Promotion, Yonsei University Graduate School of Public Health) ;
  • Yun, Ji-Eun (Institute for Health Promotion, Department of Epidemiology and Health Promotion, Yonsei University Graduate School of Public Health) ;
  • Lee, Kyu-Jang (Korea Medical Institute) ;
  • Jee, Sun-Ha (Institute for Health Promotion, Department of Epidemiology and Health Promotion, Yonsei University Graduate School of Public Health)
  • 투고 : 2011.08.14
  • 심사 : 2011.10.17
  • 발행 : 2012.03.31

초록

Objectives: Cigarette smoking is a modifiable risk factor for cardiovascular disease. Bilirubin is a potent antioxidant and its concentration decreases in smokers. However, studies about the association between cigarette smoking and bilirubin are scarce and most are limited to total bilirubin. Additionally, bilirubin is highly related to hemoglobin. Therefore, this study evaluates the association between bilirubin subtypes and cigarette smoking in healthy Korean men independently of hemoglobin. Methods: This study included 48 040 Korean men aged 30 to 87 years who visited the Korea Medical Institute for routine health examinations from January to December, 2007. The association of smoking with total, direct, and indirect bilirubin was assessed by logistic regression analysis taking into consideration differences in subjects and smoking characteristics. Results: Current smokers had lower bilirubin concentrations than never-smokers and ex-smokers. Smoking amount and duration were inversely significantly associated with total, direct, and indirect bilirubin. In a multivariable adjusted model, compared to never-smokers, the odds ratios (ORs) and 95% confidence intervals (CIs) of current smokers with the highest number of pack-years were 1.7 (1.6 to 1.9) for total, 1.5 (1.4 to 1.6) for direct, and 1.7 (1.6 to 1.9) for indirect bilirubin. After further adjustment for hemoglobin, this association became stronger (OR [95% CI], 2.1 [1.9 to 2.2] for total; 1.9 [1.8 to 2.0] for direct; 2.0 [1.9 to 2.2] for indirect bilirubin). Conclusions: In this study, bilirubin subtypes are inversely associated with smoking status, smoking amount, and smoking duration in healthy Korean men independently of hemoglobin. Further studies are needed to investigate this association in healthy Korean women.

키워드

참고문헌

  1. Erhardt L. Cigarette smoking: an undertreated risk factor for cardiovascular disease. Atherosclerosis 2009;205(1):23-32.
  2. World Health Organization. Tobacco control. Geneva: World Health Organization; 1999.
  3. Korean Ministry of Health and Welfare. The Korea National Health and Nutrition Examination Survey. Seoul: Korean Ministry of Health and Welfare; 2007.
  4. Stocker R, Glazer AN, Ames BN. Antioxidant activity of albumin-bound bilirubin. Proc Natl Acad Sci U S A 1987;84(16):5918-5922.
  5. Stocker R, Yamamoto Y, McDonagh AF, Glazer AN, Ames BN. Bilirubin is an antioxidant of possible physiological importance. Science 1987;235(4792):1043-1046.
  6. Wu TW, Wu J, Li RK, Mickle D, Carey D. Albumin-bound bilirubins protect human ventricular myocytes against oxyradical damage. Biochem Cell Biol 1991;69(10-11):683-688.
  7. Schwertner HA, Vitek L. Gilbert syndrome, UGT1A1*28 allele, and cardiovascular disease risk: possible protective effects and therapeutic applications of bilirubin. Atherosclerosis 2008;198(1):1-11.
  8. Kimm H, Yun JE, Jo J, Jee SH. Low serum bilirubin level as an independent predictor of stroke incidence: a prospective study in Korean men and women. Stroke 2009;40(11):3422-3427.
  9. Lin LY, Kuo HK, Hwang JJ, Lai LP, Chiang FT, Tseng CD, et al. Serum bilirubin is inversely associated with insulin resistance and metabolic syndrome among children and adolescents. Atherosclerosis 2009;203(2):563-568.
  10. Jo J, Yun JE, Lee H, Kimm H, Jee SH. Total, direct, and indirect serum bilirubin concentrations and metabolic syndrome among the Korean population. Endocrine 2011;39(2):182-189.
  11. Chan-Yeung M, Ferreira P, Frohlich J, Schulzer M, Tan F. The effects of age, smoking, and alcohol on routine laboratory tests. Am J Clin Pathol 1981;75(3):320-326.
  12. Hopkins PN, Wu LL, Hunt SC, James BC, Vincent GM, Williams RR. Higher serum bilirubin is associated with decreased risk for early familial coronary artery disease. Arterioscler Thromb Vasc Biol 1996;16(2):250-255.
  13. Schwertner HA. Association of smoking and low serum bilirubin antioxidant concentrations. Atherosclerosis 1998;136(2):383-387.
  14. Van Hoydonck PG, Temme EH, Schouten EG. Serum bilirubin concentration in a Belgian population: the association with smoking status and type of cigarettes. Int J Epidemiol 2001;30(6):1465-1472.
  15. Micozzi MS, Albanes D, Stevens RG. Relation of body size and composition to clinical biochemical and hematologic indices in US men and women. Am J Clin Nutr 1989;50(6):1276-1281.
  16. Milman N, Byg KE, Mulvad G, Pedersen HS, Bjerregaard P. Haemoglobin concentrations appear to be lower in indigenous Greenlanders than in Danes: assessment of haemoglobin in 234 Greenlanders and in 2804 Danes. Eur J Haematol 2001;67(1):23-29.
  17. Caliskan M, Erdogan D, Gullu H, Tok D, Bilgi M, Muderrisoglu H. Low serum bilirubin concentrations are associated with impaired aortic elastic properties, but not impaired left ventricular diastolic function. Int J Clin Pract 2007;61(2):218-224.
  18. Pineda S, Bang OY, Saver JL, Starkman S, Yun SW, Liebeskind DS, et al. Association of serum bilirubin with ischemic stroke outcomes. J Stroke Cerebrovasc Dis 2008;17(3):147-152.
  19. Hwang HJ, Kim SH. Inverse relationship between fasting direct bilirubin and metabolic syndrome in Korean adults. Clin Chim Acta 2010;411(19-20):1496-1501.
  20. Nakagami T, Toyomura K, Kinoshita T, Morisawa S. A beneficial role of bile pigments as an endogenous tissue protector: anti-complement effects of biliverdin and conjugated bilirubin. Biochim Biophys Acta 1993;1158(2):189-193.
  21. Mamtani M, Patel A, Renge R, Kulkarni H. Prognostic value of direct bilirubin in neonatal hyperbilirubinemia. Indian J Pediatr 2007;74(9):819-822.
  22. Shiomi S, Habu D, Kuroki T, Ishida S, Tatsumi N. Clinical usefulness of conjugated bilirubin levels in patients with acute liver diseases. J Gastroenterol 1999;34(1):88-93.
  23. Li B, Wang Z, Fang JJ, Xu CY, Chen WX. Evaluation of prognostic markers in severe drug-induced liver disease. World J Gastroenterol 2007;13(4):628-632.
  24. Frei B, Stocker R, Ames BN. Antioxidant defenses and lipid peroxidation in human blood plasma. Proc Natl Acad Sci U S A 1988;85(24):9748-9752.
  25. Hidalgo FJ, Zamora R, Dillard CJ, Tappel AL. Can serum bilirubin be an index of in vivo oxidative stress? Med Hypotheses 1990;33(3):207-211.
  26. Yamaguchi T, Horio F, Hashizume T, Tanaka M, Ikeda S, Kakinuma A, et al. Bilirubin is oxidized in rats treated with endotoxin and acts as a physiological antioxidant synergistically with ascorbic acid in vivo. Biochem Biophys Res Commun 1995;214(1):11-19.
  27. Yamaguchi T, Hashizume T, Tanaka M, Nakayama M, Sugimoto A, Ikeda S, et al. Bilirubin oxidation provoked by endotoxin treatment is suppressed by feeding ascorbic acid in rat mutant unable to synthesize ascorbic acid. Eur J Biochem 1997;15:233-240.
  28. Yamaguchi T, Hashizume T, Tanaka M, Nakayama M, Sugimoto A, Ikeda S, et al. Bilirubin oxidation provoked by endotoxin treatment is suppressed by feeding ascorbic acid in a rat mutant unable to synthesize ascorbic acid. Eur J Biochem 1997;245(2):233-240.
  29. Minetti M, Mallozzi C, Di Stasi AM, Pietraforte D. Bilirubin is an effective antioxidant of peroxynitritemediated protein oxidation in human blood plasma. Arch Biochem Biophys 1998;352(2):165-174.
  30. Wu TW, Fung KP, Yang CC. Unconjugated bilirubin inhibits the oxidation of human low density lipoprotein better than Trolox. Life Sci 1994;54(25):P477-P481.
  31. Wu TW, Fung KP, Wu J, Yang CC, Weisel RD. Antioxidation of human low density lipoprotein by unconjugated and conjugated bilirubins. Biochem Pharmacol 1996;51(6):859-862.
  32. Neuzil J, Stocker R. Free and albumin-bound bilirubin are efficient co-antioxidants for alpha-tocopherol, inhibiting plasma and low density lipoprotein lipid peroxidation. J Biol Chem 1994;269(24):16712-16719.
  33. Hulea SA, Wasowicz E, Kummerow FA. Inhibition of metal-catalyzed oxidation of low-density lipoprotein by free and albumin-bound bilirubin. Biochim Biophys Acta 1995;1259(1):29-38.
  34. Sull JW, Kim HJ, Yun JE, Park EJ, Kim G, Jee SH. Serum adiponectin is associated with smoking status in healthy Korean men. Endocr J 2009;56(1):73-78.
  35. Frei B, Forte TM, Ames BN, Cross CE. Gas phase oxidants of cigarette smoke induce lipid peroxidation and changes in lipoprotein properties in human blood plasma. Protective effects of ascorbic acid. Biochem J 1991;277(Pt 1):133-1338.
  36. Frei B. Reactive oxygen species and antioxidant vitamins: mechanisms of action. Am J Med 1994;97(3A):5S-13S.
  37. Scheffler E, Wiest E, Woehrle J, Otto I, Schulz I, Huber L, et al. Smoking influences the atherogenic potential of lowdensity lipoprotein. Clin Investig 1992;70(3-4):263-268.
  38. Burchell B, Hume R. Molecular genetic basis of Gilbert's syndrome. J Gastroenterol Hepatol 1999;14(10):960-966.
  39. Yoon SJ, Lee HS, Lee SW, Yun JE, Kim SY, Cho ER, et al. The association between adiponectin and diabetes in the Korean population. Metabolism 2008;57(6):853-857.

피인용 문헌

  1. The Association Between Heterozygosity forUGT1A1*6,UGT1A1*28, and Variation in the Serum Total-Bilirubin Level in Healthy Young Japanese Adults vol.17, pp.6, 2012, https://doi.org/10.1089/gtmb.2012.0402
  2. Smoking Cessation Is Followed by Increases in Serum Bilirubin, an Endogenous Antioxidant Associated With Lower Risk of Lung Cancer and Cardiovascular Disease vol.16, pp.8, 2012, https://doi.org/10.1093/ntr/ntu067
  3. The Relationship between Total Bilirubin Levels and Total Mortality in Older Adults: The United States National Health and Nutrition Examination Survey (NHANES) 1999-2004 vol.9, pp.4, 2012, https://doi.org/10.1371/journal.pone.0094479
  4. Combined Effects of Smoking and Bilirubin Levels on the Risk of Lung Cancer in Korea: The Severance Cohort Study vol.9, pp.8, 2014, https://doi.org/10.1371/journal.pone.0103972
  5. Serum bilirubin concentration is modified by UGT1A1 Haplotypes and influences risk of Type-2 diabetes in the Norfolk Island genetic isolate vol.16, pp.None, 2015, https://doi.org/10.1186/s12863-015-0291-z
  6. Cigarette Smoking Habit and Subjective Quality of Sleep vol.3, pp.1, 2015, https://doi.org/10.5812/scimetr.18454
  7. Active and Passive Smoking and Serum Total Bilirubin in a Rural Korean Population vol.18, pp.5, 2012, https://doi.org/10.1093/ntr/ntv251
  8. Cigarette smoking behaviour and blood metabolomics vol.45, pp.5, 2012, https://doi.org/10.1093/ije/dyv330
  9. Direct Bilirubin Levels and Risk of Metabolic Syndrome in Healthy Chinese Men vol.2017, pp.None, 2012, https://doi.org/10.1155/2017/9621615
  10. Association between elevated serum bilirubin levels with preserved lung function under conditions of exposure to air pollution vol.21, pp.1, 2012, https://doi.org/10.1186/s12890-021-01488-5