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The Association Between Smoking Tobacco After a Diagnosis of Diabetes and the Prevalence of Diabetic Nephropathy in the Korean Male Population

  • Yeom, Hyungseon (Department of Preventive Medicine, Yonsei University College of Medicine) ;
  • Lee, Jung Hyun (Department of Preventive Medicine, Graduate School of Public Health, Yonsei University) ;
  • Kim, Hyeon Chang (Department of Preventive Medicine, Yonsei University College of Medicine) ;
  • Suh, Il (Department of Preventive Medicine, Yonsei University College of Medicine)
  • Received : 2015.11.11
  • Accepted : 2016.03.13
  • Published : 2016.03.31

Abstract

Objectives: Smoking is known to be associated with nephropathy in patients with diabetes. The distinct effects of smoking before and after diabetes has been diagnosed, however, are not well characterized. We evaluated the association of cigarette smoking before and after a diagnosis of diabetes with the presence of diabetic nephropathy. Methods: We analyzed data from the 2011-2013 editions of the Korea National Health and Nutrition Examination Survey. A total of 629 male patients diagnosed with diabetes were classified as non-smokers (90 patients), former smokers (225 patients), or continuing smokers (314 patients). A "former smoker" was a patient who smoked only before receiving his diagnosis of diabetes. A "continuing smoker" was a patient who smoked at any time after his diabetes had been diagnosed. Diabetic nephropathy was defined as the presence of albuminuria (spot urine albumin/creatinine ratio ${\geq}30mg/g$) or low estimated glomerular filtration rate ($<60mL/min/1.73m^2$). Multiple logistic regression models were used to assess the independent association after adjusting for age, duration of diabetes, hemoglobin A1c, body mass index, systolic blood pressure, medication for hypertension, and medication for dyslipidemia. Female patients were excluded from the study due to the small proportion of females in the survey who smoked. Results: Compared to non-smokers, continuing smokers had significantly higher odds ratio ([OR], 2.17; 95% confidence interval [CI], 1.23 to 3.83) of suffering from diabetic nephropathy. The corresponding OR (95% CI) for former smokers was 1.26 (0.70 to 2.29). Conclusions: Smoking after diagnosis of diabetes is significantly associated with the presence of diabetic nephropathy in the Korean male population.

Keywords

References

  1. Ahn JH, Yu JH, Ko SH, Kwon HS, Kim DJ, Kim JH, et al. Prevalence and determinants of diabetic nephropathy in Korea: Korea National Health and Nutrition Examination Survey. Diabetes Metab J 2014;38(2):109-119. https://doi.org/10.4093/dmj.2014.38.2.109
  2. de Boer IH, Katz R, Cao JJ, Fried LF, Kestenbaum B, Mukamal K, et al. Cystatin C, albuminuria, and mortality among older adults with diabetes. Diabetes Care 2009;32(10):1833-1838. https://doi.org/10.2337/dc09-0191
  3. Gerstein HC, Mann JF, Yi Q, Zinman B, Dinneen SF, Hoogwerf B, et al. Albuminuria and risk of cardiovascular events, death, and heart failure in diabetic and nondiabetic individuals. JAMA 2001;286(4):421-426. https://doi.org/10.1001/jama.286.4.421
  4. Molitch ME, DeFronzo RA, Franz MJ, Keane WF, Mogensen CE, Parving HH, et al. Nephropathy in diabetes. Diabetes Care 2004;27 Suppl 1:S79-S83. https://doi.org/10.2337/diacare.27.2007.S79
  5. Jin DC. Major changes and improvements of dialysis therapy in Korea: review of end-stage renal disease registry. Korean J Intern Med 2015;30(1):17-22. https://doi.org/10.3904/kjim.2015.30.1.17
  6. Kim TH, Chun KH, Kim HJ, Han SJ, Kim DJ, Kwak J, et al. Direct medical costs for patients with type 2 diabetes and related complications: a prospective cohort study based on the Korean National Diabetes Program. J Korean Med Sci 2012;27(8): 876-882. https://doi.org/10.3346/jkms.2012.27.8.876
  7. Raptis AE, Viberti G. Pathogenesis of diabetic nephropathy. Exp Clin Endocrinol Diabetes 2001;109 Suppl 2:S424-S437. https://doi.org/10.1055/s-2001-18600
  8. Chuahirun T, Khanna A, Kimball K, Wesson DE. Cigarette smoking and increased urine albumin excretion are interrelated predictors of nephropathy progression in type 2 diabetes. Am J Kidney Dis 2003;41(1):13-21. https://doi.org/10.1053/ajkd.2003.50009
  9. Feodoroff M, Harjutsalo V, Forsblom C, Thorn L, Wadén J, Tolonen N, et al. Smoking and progression of diabetic nephropathy in patients with type 1 diabetes. Acta Diabetol 2015. doi:10.1007/s00592-015-0822-0.
  10. Sawicki PT, Didjurgeit U, Muhlhauser I, Bender R, Heinemann L, Berger M. Smoking is associated with progression of diabetic nephropathy. Diabetes Care 1994;17(2):126-131. https://doi.org/10.2337/diacare.17.2.126
  11. Gregg EW, Li Y, Wang J, Burrows NR, Ali MK, Rolka D, et al. Changes in diabetes-related complications in the United States, 1990-2010. N Engl J Med 2014;370(16):1514-1523. https://doi.org/10.1056/NEJMoa1310799
  12. Chuahirun T, Simoni J, Hudson C, Seipel T, Khanna A, Harrist RB, et al. Cigarette smoking exacerbates and its cessation ameliorates renal injury in type 2 diabetes. Am J Med Sci 2004;327(2):57-67. https://doi.org/10.1097/00000441-200402000-00001
  13. Phisitkul K, Hegazy K, Chuahirun T, Hudson C, Simoni J, Rajab H, et al. Continued smoking exacerbates but cessation ameliorates progression of early type 2 diabetic nephropathy. Am J Med Sci 2008;335(4):284-291. https://doi.org/10.1097/MAJ.0b013e318156b799
  14. Pinto-Sietsma SJ, Mulder J, Janssen WM, Hillege HL, de Zeeuw D, de Jong PE. Smoking is related to albuminuria and abnormal renal function in nondiabetic persons. Ann Intern Med 2000;133(8):585-591. https://doi.org/10.7326/0003-4819-133-8-200010170-00008
  15. Gupta RK, Gupta R, Maheshwari VD, Mawliya M. Impact of smoking on microalbuminuria and urinary albumin creatinine ratio in non-diabetic normotensive smokers. Indian J Nephrol 2014;24(2):92-96. https://doi.org/10.4103/0971-4065.127893
  16. Kweon S, Kim Y, Jang MJ, Kim Y, Kim K, Choi S, et al. Data resource profile: the Korea National Health and Nutrition Examination Survey (KNHANES). Int J Epidemiol 2014;43(1):69-77. https://doi.org/10.1093/ije/dyt228
  17. Jung-Choi KH, Khang YH, Cho HJ. Hidden female smokers in Asia: a comparison of self-reported with cotinine-verified smoking prevalence rates in representative national data from an Asian population. Tob Control 2012;21(6):536-542. https://doi.org/10.1136/tobaccocontrol-2011-050012
  18. Levey AS, de Jong PE, Coresh J, El Nahas M, Astor BC, Matsushita K, et al. The definition, classification, and prognosis of chronic kidney disease: a KDIGO Controversies Conference report. Kidney Int 2011;80(1):17-28. https://doi.org/10.1038/ki.2010.483
  19. Baggio B, Budakovic A, Dalla Vestra M, Saller A, Bruseghin M, Fioretto P. Effects of cigarette smoking on glomerular structure and function in type 2 diabetic patients. J Am Soc Nephrol 2002;13(11):2730-2736. https://doi.org/10.1097/01.ASN.0000032422.81130.68
  20. Cirillo M, Senigalliesi L, Laurenzi M, Alfieri R, Stamler J, Stamler R, et al. Microalbuminuria in nondiabetic adults: relation of blood pressure, body mass index, plasma cholesterol levels, and smoking: the Gubbio Population Study. Arch Intern Med 1998;158(17):1933-1939. https://doi.org/10.1001/archinte.158.17.1933
  21. Tozawa M, Iseki K, Iseki C, Oshiro S, Ikemiya Y, Takishita S. Influence of smoking and obesity on the development of proteinuria. Kidney Int 2002;62(3):956-962. https://doi.org/10.1046/j.1523-1755.2002.00506.x
  22. Voulgari C, Katsilambros N, Tentolouris N. Smoking cessation predicts amelioration of microalbuminuria in newly diagnosed type 2 diabetes mellitus: a 1-year prospective study. Metabolism 2011;60(10):1456-1464. https://doi.org/10.1016/j.metabol.2011.02.014
  23. Hallan SI, Orth SR. Smoking is a risk factor in the progression to kidney failure. Kidney Int 2011;80(5):516-523. https://doi.org/10.1038/ki.2011.157
  24. Luo J, Rossouw J, Tong E, Giovino GA, Lee CC, Chen C, et al. Smoking and diabetes: does the increased risk ever go away? Am J Epidemiol 2013;178(6):937-945. https://doi.org/10.1093/aje/kwt071
  25. Chakkarwar VA. Smoking in diabetic nephropathy: sparks in the fuel tank? World J Diabetes 2012;3(12):186-195. https://doi.org/10.4239/wjd.v3.i12.186
  26. Giacco F, Brownlee M. Oxidative stress and diabetic complications. Circ Res 2010;107(9):1058-1070. https://doi.org/10.1161/CIRCRESAHA.110.223545
  27. Craig WY, Palomaki GE, Haddow JE. Cigarette smoking and serum lipid and lipoprotein concentrations: an analysis of published data. BMJ 1989;298(6676):784-788. https://doi.org/10.1136/bmj.298.6676.784
  28. Freeman DJ, Caslake MJ, Griffin BA, Hinnie J, Tan CE, Watson TD, et al. The effect of smoking on post-heparin lipoprotein and hepatic lipase, cholesteryl ester transfer protein and lecithin:cholesterol acyl transferase activities in human plasma. Eur J Clin Invest 1998;28(7):584-591. https://doi.org/10.1046/j.1365-2362.1998.00328.x
  29. Esmatjes E, Flores L, Lario S, Claria J, Cases A, Inigo P, et al. Smoking increases serum levels of transforming growth factor-beta in diabetic patients. Diabetes Care 1999;22(11):1915-1916. https://doi.org/10.2337/diacare.22.11.1915
  30. Gulliford MC. Low rates of detection and treatment of hypertension among current cigarette smokers. J Hum Hypertens 2001;15(11):771-773. https://doi.org/10.1038/sj.jhh.1001275
  31. John U, Meyer C, Hanke M, Völzke H, Schumann A. Relation between awareness of circulatory disorders and smoking in a general population health examination. BMC Public Health 2006;6:48. https://doi.org/10.1186/1471-2458-6-48
  32. Muggeo M. Accelerated complications in type 2 diabetes mellitus: the need for greater awareness and earlier detection. Diabet Med 1998;15 Suppl 4:S60-S62. https://doi.org/10.1002/(SICI)1096-9136(1998120)15:4+3.3.CO;2-A
  33. Ekberg G, Grefberg N, Larsson LO, Vaara I. Cigarette smoking and glomerular filtration rate in insulin-treated diabetics without manifest nephropathy. J Intern Med 1990;228(3):211-217. https://doi.org/10.1111/j.1365-2796.1990.tb00220.x
  34. Orth SR. Effects of smoking on systemic and intrarenal hemodynamics: influence on renal function. J Am Soc Nephrol 2004;15 Suppl 1:S58-S63. https://doi.org/10.1097/01.ASN.0000093461.36097.D5
  35. Kim Y, Park S, Kim NS, Lee BK. Inappropriate survey design analysis of the Korean National Health and Nutrition Examination Survey may produce biased results. J Prev Med Public Health 2013;46(2):96-104. https://doi.org/10.3961/jpmph.2013.46.2.96
  36. American Diabetes Association. Executive summary: standards of medical care in diabetes--2011. Diabetes Care 2011;34 Suppl 1:S4-S10. https://doi.org/10.2337/dc11-S004
  37. Chuang LM, Tsai ST, Huang BY, Tai TY; Diabcare-Asia 1998 Study Group. The status of diabetes control in Asia--a cross-sectional survey of 24 317 patients with diabetes mellitus in 1998. Diabet Med 2002;19(12):978-985. https://doi.org/10.1046/j.1464-5491.2002.00833.x

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