Smoking and diabetes: Is the association mediated by adiponectin, leptin, or C-reactive protein?

Journal of Epidemiology

Volumn 25, Issue 2, 2015, Pages 99-109

  Hilawe, Esayas Haregot ^a,b   Yatsuya, Hiroshi ^a,c   Li, Yuanying ^c   Uemura, Mayu ^a   Wang, Chaochen ^a   Chiang, Chifa ^a   Toyoshima, Hideaki ^d   Tamakoshi, Koji ^a   Zhang, Yan ^a   Kawazoe, Nobuo ^a   Aoyama, Atsuko ^a  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b MEKELLE UNIVERSITY   (Ethiopia)

^c FUJITA HEALTH UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d ANJO KOSEI HOSPITAL   (Japan)

Author keywords

Adiponectin; C reactive protein; Leptin; Mediation analysis; Smoking; Type 2 diabetes mellitus

Indexed keywords

ADIPONECTIN; BIOLOGICAL MARKER; C REACTIVE PROTEIN; LEPTIN;

ADULT; AGED; BLOOD; COHORT ANALYSIS; DIABETES MELLITUS, TYPE 2; FEMALE; HUMAN; JAPAN; MALE; MIDDLE AGED; SMOKING;

ADIPONECTIN; ADULT; AGED; BIOMARKERS; C-REACTIVE PROTEIN; COHORT STUDIES; DIABETES MELLITUS, TYPE 2; FEMALE; HUMANS; JAPAN; LEPTIN; MALE; MIDDLE AGED; SMOKING;

EID: 84923872990     PISSN: 09175040     EISSN: 13499092     Source Type: Journal    
DOI: 10.2188/jea.JE20140055     Document Type: Article

References (72)

1. Willi C, Bodenmann P, Ghali WA, Faris PD, Cornuz J. Active smoking and the risk of type 2 Diabetes: a systematic review and meta-analysis. JAMA. 2007;298(22):2654-64.
2. US Department of Health and Human Services. The health consequences of smoking-50 years of progress: A report of the Surgeon General. Atlanta, GA. 2014.
3. Fagard RH, Nilsson PM. Smoking and diabetes-the double health hazard! Prim Care Diabetes. 2009 Nov;3(4):205-9.
4. Kadowaki T, Yamauchi T, Kubota N, Hara K, Ueki K, Tobe K. Adiponectin and adiponectin receptors in insulin resistance, diabetes, and the metabolic syndrome. J Clin Invest. 2006; 116(7):1784-92.
5. Tilg H, Moschen AR. Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nat Rev Immunol. 2006 Oct;6(10):772-83.
6. Takefuji S, Yatsuya H, Tamakoshi K, Otsuka R, Wada K, Matsushita K, et al. Smoking status and adiponectin in healthy Japanese men and women. Prev Med. 2007 Dec;45(6):471-5.
7. 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 Jan;56(1):73-8.
8. Thamer C, Stefan N, Stumvoll M, Häring H, Fritsche A. Reduced adiponectin serum levels in smokers. Atherosclerosis. 2005 Apr;179(2):421-2.
9. Iwashima Y, Katsuya T, Ishikawa K, Kida I, Ohishi M, Horio T, et al. Association of hypoadiponectinemia with smoking habit in men. Hypertension. 2005 Jun;45(6):1094-100.
10. Kotani K, Hazama A, Hagimoto A, Saika K, Shigeta M, Katanoda K, et al. Adiponectin and smoking status: a systematic review. J Atheroscler Thromb. 2012 Jan;19(9):787-94.
11. Duncan BB, Schmidt MI, Pankow JS, Bang H, Couper D, Ballantyne CM, et al. Adiponectin and the development of type 2 diabetes: The atherosclerosis risk in communities study. Diabetes. 2004;53(9):2473-8.
12. Li S, Shin HJ, Ding EL, van Dam RM. Adiponectin levels and risk of type 2 diabetes: a systemic review and meta-analysis. JAMA. 2009;302(2):179-88.
13. Jee SH, Ahn CW, Park JS, Park CG, Kim HS, Lee SH, et al. Serum adiponectin and type 2 diabetes: a 6-year follow-up cohort study. Diabetes Metab. J. 2013 Aug;37(4):252-61.
14. Li Y, Yatsuya H, Iso H, Toyoshima H, Tamakoshi K. Inverse relationship of serum adiponectin concentration with type 2 diabetes mellitus incidence in middle-aged Japanese workers: six-year follow-up. Diabetes Metab Res Rev. 2012;28(4): 349-56.
15. Koc B, Bulucu F, Karadurmus N, Sahin M. Lower leptin levels in young non-obese male smokers than non-smokers. Ups J Med Sci. 2009 Jan;114(3):165-9.
16. Nagayasu S, Suzuki S, Yamashita A, Taniguchi A, Fukushima M, Nakai Y, et al. Smoking and adipose tissue inflammation suppress leptin expression in Japanese obese males: potential mechanism of resistance to weight loss among Japanese obese smokers. Tob Induc Dis. 2012 Jan;10(3).
17. Reseland JE, Mundal HH, Hollung K, Haugen F, Zahid N, Anderssen SA, et al. Cigarette smoking may reduce plasma leptin concentration via catecholamines. Prostaglandins Leukot Essent Fatty Acids. 2005 Jul;73(1):43-9.
18. Hotta Y, Yatsuya H, Toyoshima H, Matsushita K, Mitsuhashi H, Takefuji S, et al. Low leptin but high insulin resistance of smokers in Japanese men. Diabetes Res Clin Pract. 2008 Sep;81(3):358-64.
19. Perkins KA, Fonte C. Effects of smoking status and smoking cessation on leptin levels. Nicotine Tob Res. 2002 Nov;4(4): 459-66.
20. Eliasson B, Smith U. Leptin levels in smokers and long-term users of nicotine gum. Eur J Clin Invest. 1999 Feb;29(2):145-52.
21. Al-Daghri NM, Al-Attas OS, Hussain T, Sabico S, Bamakhramah A. Altered levels of adipocytokines in type 2 diabetic cigarette smokers. Diabetes Res Clin Pract. 2009 Feb;83(2):e37-9.
22. McNeely MJ, Boyko EJ, Weigle DS, Shofer JB, Chessler SD, Leonnetti DL, et al. Association between baseline plasma leptin levels and subsequent development of diabetes in Japanese Americans. Diabetes Care. 1999;22(1):65-70.
23. Thorand B, Zierer A, Baumert J, Meisinger C, Herder C, Koenig W. Associations between leptin and the leptin/adiponectin ratio and incident type 2 diabetes in middle-aged men and women: results from the MONICA/KORA Augsburg study 1984-2002. Diabet Med. 2010 Sep;27(9):1004-11.
24. Welsh P, Murray HM, Buckley BM, de Craen AJ, Ford I, Jukema JW, et al. Leptin predicts diabetes but not cardiovascular disease results from a large prospective study in an elderly population. Diabetes Care. 2009;32(2):308-10.
25. Ley SH, Harris SB, Connelly PW, Mamakeesick M, Gittelsohn J, Hegele RA, et al. Adipokines and incident type 2 diabetes in an Aboriginal Canadian [corrected] population: the Sandy Lake Health and Diabetes Project. Diabetes Care. 2008;31(7):1410-5.
26. Marques-Vidal P, Schmid R, Bochud M, Bastardot F, von Känel R, Paccaud F, et al. Adipocytokines, hepatic and inflammatory biomarkers and incidence of type 2 diabetes: The CoLaus study. PLoS One. 2012 Jan;7(12):e51768.
27. Sun Q, van Dam RM, Meigs JB, Franco OH, Mantzoros CS, Hu FB. Leptin and soluble leptin receptor levels in plasma and risk of type 2 diabetes in US women a prospective study. Diabetes. 2010;59(3):611-8.
28. Donath MY, Shoelson SE. Type 2 diabetes as an inflammatory disease. Nat Rev Immunol. 2011 Feb;11(2):98-107.
29. Levitzky YS, Guo CY, Rong J, Larson MG, Walter RE, Keaney JF Jr, et al. Relation of smoking status to a panel of inflammatory markers: the Framingham offspring. Atherosclerosis. 2008 Nov;201(1):217-24.
30. Lao XQ, Jiang CQ, Zhang WS, Adab P, Lam TH, Cheng KK, et al. Smoking, smoking cessation and inflammatory markers in older Chinese men: The Guangzhou Biobank Cohort Study. Atherosclerosis. 2009 Mar;203(1):304-10.
31. O'Loughlin J, Lambert M, Karp I, McGrath J, Gray-Donald K, Barnett TA, et al. Association between cigarette smoking and C-reactive protein in a representative, population-based sample of adolescents. Nicotine Tob Res. 2008 Mar;10(3):525-32.
32. Hastie CE, Haw S, Pell JP. Impact of smoking cessation and lifetime exposure on C-reactive protein. Nicotine Tob Res. 2008 Apr;10(4):637-42.
33. Wannamethee SG, Lowe GD, Shaper AG, Rumley A, Lennon L, Whincup PH. Associations between cigarette smoking, pipe/cigar smoking, and smoking cessation, and haemostatic and inflammatory markers for cardiovascular disease. Eur Heart J. 2005 Sep;26(17):1765-73.
34. Wang X, Bao W, Liu J, Ouyang YY, Wang D, Rong S, et al. Inflammatory markers and risk of type 2 diabetes: a systematic review and meta-analysis. Diabetes Care. 2013 Jan;36(1): 166-75.
35. Ong KL, Tso AW, Xu A, Law LS, Li M, Wat NM, et al. Evaluation of the combined use of adiponectin and C-reactive protein levels as biomarkers for predicting the deterioration in glycaemia after a median of 5.4 years. Diabetologia. 2011 Oct;54(10):2552-60.
36. Doi Y, Kiyohara Y, Kubo M, Ninomiya T, Wakugawa Y, Yonemoto K, et al. Elevated C-reactive protein is a predictor of the development of diabetes in a general Japanese population: the Hisayama study. Diabetes Care. 2005;28(10):2497-500.
37. Krakoff J, Funahashi T, Stehouwer CD, Schalkwijk CG, Tanaka S, Matsuzawa Y, et al. Inflammatory markers, adiponectin, and risk of type 2 diabetes in the Pima Indian. Diabetes Care. 2003;26(6):1745-51.
38. Lee CC, Adler AI, Sandhu MS, Sharp SJ, Forouhi NG, Erqou S, et al. Association of C-reactive protein with type 2 diabetes: prospective analysis and meta-analysis. Diabetologia. 2009 Jun;52(6):1040-7.
39. Wada K, Yatsuya H, Ouyang P, Otsuka R, Mitsuhashi H, Takefuji S, et al. Self-reported medical history was generally accurate among Japanese workplace population. J Clin Epidemiol. 2009 Mar;62(3):306-13.
40. Science and Technology Agency. Standard tables of food composition in Japan. 5th rev en. Tokyo: Printing Bureau of the Ministry of Finance; 2005.
41. Hayes AF. Introduction to mediation, moderation, and conditional process analysis: A regression-based approach. New York: Guilford Press; 2013.
42. Hayes AF, Preacher KJ. Statistical mediation analysis with a multicategorical independent variable. Br J Math Stat Psychol. 2013;Nov 5(Epub ahead of print).
43. Preacher KJ, Hayes AF. Asymptotic and resampling strategies for assessing and comparing indirect effects in multiple mediator models. Behav Res Methods. 2008 Aug;40(3):879-91.
44. Cho NH, Chan JC, Jang HC, Lim S, Kim HL, Choi SH. Cigarette smoking is an independent risk factor for type 2 diabetes: a four-year community-based prospective study. Clin Endocrinol (Oxf). 2009 Nov;71(5):679-85.
45. 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 Jun 30;178(6):937-45.
46. Manson JE, Ajani UA, Liu S, Nathan DM, Hennekens CH. A prospective study of cigarette smoking and the incidence of diabetes mellitus among US male physicians. Am J Med. 2000 Nov;109(7):538-42.
47. Meisinger C, Döring A, Thorand B, Löwel H. Association of cigarette smoking and tar and nicotine intake with development of type 2 diabetes mellitus in men and women from the general population: the MONICA/KORA Augsburg Cohort Study. Diabetologia. 2006 Aug;49(8):1770-6.
48. Nakanishi N, Nakamura K, Matsuo Y, Suzuki K, Tatara K. Cigarette smoking and risk for impaired fasting glucose and type 2 diabetes in middle-aged Japanese men. Ann Intern Med. 2000;133(3):183-91.
49. Sairenchi T, Iso H, Nishimura A, Hosoda T, Irie F, Saito Y, et al. Cigarette smoking and risk of type 2 diabetes mellitus among middle-aged and elderly Japanese men and women. Am J Epidemiol. 2004 Jul 15;160(2):158-62.
50. Will JC, Galuska DA, Ford ES, Mokdad A, Calle EE. Cigarette smoking and diabetes mellitus: evidence of a positive association from a large prospective cohort study. Int J Epidemiol. 2001 Jun;30(3):540-6.
51. Yeh HC, Duncan BB, Schmidt MI, Wang NY, Brancati FL. Smoking, smoking cessation, and risk for type 2 diabetes mellitus: a cohort study. Ann Intern Med. 2010 Jun 1;152(1):10-7.
52. Wannamethee SG, Shaper AG, Perry IJ; British Regional Heart Study. Smoking as a modifiable risk factor for type 2 diabetes in middle-aged men. Diabetes Care. 2001 Sep;24(9):1590-5.
53. Rimm EB, Chan J, Stampfer MJ, Colditz GA, Willett WC. Prospective study of cigarette smoking, alcohol use, and the risk of diabetes in men. BMJ. 1995;310(6979):555-9.
54. Beziaud F, Halimi JM, Lecomte P, Vol S, Tichet J. Cigarette smoking and diabetes mellitus. Diabetes Metab. 2004 Apr;30(2): 161-6.
55. Kawakami N, Takatsuka N, Shimizu H, Ishibashi H. Effects of smoking on the incidence of non-insulin-dependent diabetes mellitus: replication and extension in a Japanese cohort of male employees. Am J Epidemiol. 1997;145(2):103-9.
56. Otsuka F, Kojima S, Maruyoshi H, Kojima S, Matsuzawa Y, Funahashi T, et al. Smoking cessation is associated with increased plasma adiponectin levels in men. J Cardiol. 2009 Apr;53(2):219-25.
57. Efstathiou SP, Skeva II, Dimas C, Panagiotou A, Parisi K, Tzanoumis L, et al. Smoking cessation increases serum adiponectin levels in an apparently healthy Greek population. Atherosclerosis. 2009 Aug;205(2):632-6.
58. Bogan JS, Lodish HF. Two compartments for insulin-stimulated exocytosis in 3T3-L1 adipocytes defined by endogenous ACRP30 and GLUT4. J Cell Biol. 1999 Aug 9;146(3):609-20.
59. Conti-Fine BM, Navaneetham D, Lei S, Maus AD. Neuronal nicotinic receptors in non-neuronal cells: new mediators of tobacco toxicity? Eur J Pharmacol. 2000 Mar 30;393(1-3): 279-94.
60. Churg A, Dai J, Tai H, Xie C, Wright JL. Tumor necrosis factoralpha is central to acute cigarette smoke-induced inflammation and connective tissue breakdown. Am J Respir Crit Care Med. 2002 Sep 15;166(6):849-54.
61. Maeda N, Takahashi M, Funahashi T, Kihara S, Nishizawa H, Kishida K, et al. PPAR-gamma ligands increase expression and plasma concentrations of adiponectin, an adipose-derived protein. Diabetes. 2001 Sep;50(9):2094-9.
62. Yamauchi T, Kamon J, Minokoshi Y, Ito Y, Waki H, Uchida S, et al. Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat Med. 2002 Nov;8(11):1288-95.
63. Yamauchi T, Kamon J, Waki H, Imai Y, Shimozawa N, Hioki K, et al. Globular adiponectin protected ob/ob mice from diabetes and ApoE-deficient mice from atherosclerosis. J Biol Chem. 2003 Jan 24;278(4):2461-8.
64. Stern N, Osher E, Greenman Y. Hypoadiponectinemia as a marker of adipocyte dysfunction-Part I: the biology of adiponectin. J Cardiometab Syndr. 2007 Jan;2(3):174-82.
65. Rom O, Avezov K, Aizenbud D, Reznick AZ. Cigarette smoking and inflammation revisited. Respir Physiol Neurobiol. 2013 Jun 1;187(1):5-10.
66. Schmidt MI, Duncan BB, Vigo A, Pankow JS, Couper D, Ballantyne CM, et al. Leptin and incident type 2 diabetes: risk or protection? Diabetologia. 2006 Sep;49(9):2086-96.
67. Matsubara M, Maruoka S, Katayose S. Inverse relationship between plasma adiponectin and leptin concentrations in normalweight and obese women. Eur J Endocrinol. 2002 Aug;147(2): 173-80.
68. Matsushita K, Yatsuya H, Tamakoshi K, Wada K, Otsuka R, Zhang H, et al. Inverse association between adiponectin and C-reactive protein in substantially healthy Japanese men. Atherosclerosis. 2006 Sep;188(1):184-9.
69. Zhu N, Pankow JS, Ballantyne CM, Couper D, Hoogeveen RC, Pereira M, et al. High-molecular-weight adiponectin and the risk of type 2 diabetes in the ARIC study. J Clin Endocrinol Metab. 2010 Nov;95(11):5097-104.
70. Fisher FM, Trujillo ME, Hanif W, Barnett AH, McTernan PG, Scherer PE, et al. Serum high molecular weight complex of adiponectin correlates better with glucose tolerance than total serum adiponectin in Indo-Asian males. Diabetologia. 2005 Jun;48(6):1084-7.
71. Gu W, Li Y. The therapeutic potential of the adiponectin pathway. BioDrugs. 2012 Feb 1;26(1):1-8.
72. Yamauchi T, Kadowaki T. Physiological and pathophysiological roles of adiponectin and adiponectin receptors in the integrated regulation of metabolic and cardiovascular diseases. Int. J. Obes. (Lond). 2008 Dec;32 Suppl 7:S13-8.