Current smoking status may be associated with overt albuminuria in female patients with type 1 diabetes mellitus: a cross-sectional study
More details
Hide details
Department of Internal Medicine, Division of Endocrinology and Metabolism, Jichi Medical University, Tochigi, Japan
Department of Clinical Laboratory Medicine, Jichi Medical University, Tochigi, Japan
Submission date: 2012-02-29
Acceptance date: 2012-08-06
Publication date: 2012-08-10
Corresponding author
Kenta Okada   

Department of Internal Medicine, Division of Endocrinology and Metabolism, Jichi Medical University, Tochigi 320-0498, Japan
Tobacco Induced Diseases 2012;10(August):12
There are very few clinical reports that have compared the association between cigarette smoking and microangiopathy in Asian patients with type 1 diabetes mellitus (T1DM). The objective of this study was to assess the relationships between urinary protein concentrations and smoking and gender-based risk factors among patients with T1DM.

A cross-sectional study of 259 patients with T1DM (men/women = 90/169; mean age, 50.7 years) who visited our hospital for more than 1 year between October 2010 and April 2011 was conducted. Participants completed a questionnaire about their smoking habits. Patient characteristics included gender, age, body mass index, blood pressure, hemoglobin A1c, lipid parameters, and microangiopathy. Diabetic nephropathy (DN) was categorized as normoalbuminuria (NA), microalbuminuria (MA), or overt albuminuria (OA) on the basis of the following urinary albumin/creatinine ratio (ACR) levels: NA, ACR levels less than 30 mg/g creatinine (Cr); MA, ACR levels between 30 and 299 mg/g Cr; and OA, ACR levels over 300 mg/g Cr.

The percentages of current nonsmokers and current smokers with T1DM were 73.0% (n = 189) and 27.0% (n = 70), respectively. In addition, the percentage of males was higher than that of females (52.2% versus 13.6%) in the current smoking population. The percentage of DN was 61.8% (n = 160) in patients with NA, 21.6% (n = 56) in patients with MA, and 16.6% (n = 43) in patients with OA. The percentage of males among OA patients was also higher than that of females (24.4% versus 12.4%). However, current smoking status was associated with OA in females with T1DM only [unadjusted odds ratio (OR), 4.13; 95% confidence interval (CI), 1.45–11.73, P < 0.01; multivariate-adjusted OR, 5.41; 95% CI, 1.69–17.30, P < 0.01].

Based on our results in this cross-sectional study of Asian patients with T1DM, smoking might be a risk factor for OA among female patients. Further research is needed of these gender-specific results.

Karvonen M, Viik-Kajander M, Moltchanova E, Libman I, LaPorte R, Tuomilehto J: Incidence of childhood type 1 diabetes worldwide. Diabetes Mondiale (DiaMond) Project Group. Diabetes Care. 2000, 23: 1516-1526. 10.2337/diacare.23.10.1516.
EURODIAB ACE Study Group: Variation and trends in incidence of childhood diabetes in Europe. Lancet. 2000, 355: 873-876.
Japan IDDM Epidemiology Study Group: Lack of regional variation in IDDM risk in Japan. Diabetes Care. 1993, 16: 796-800.
Chase HP, Garg SK, Marshall G, Berg CL, Harris S, Jackson WE, Hamman RE: Cigarette smoking increases the risk of albuminuria among subjects with type 1 diabetes. JAMA. 1991, 265: 614-617. 10.1001/jama.1991.03460050068022.
Sawicki PT, Didjurgeit U, Mühlhauser I, Bender R, Heinemann L, Berger M: Smoking is associated with progression of diabetic nephropathy. Diabetes Care. 1994, 17: 126-131. 10.2337/diacare.17.2.126.
Raile K, Galler A, Hofer S, Herbst A, Dunstheimer D, Busch P, Holl RW: Diabetic nephropathy in 27,805 children, adolescents, and adults with type 1 diabetes: effect of diabetes duration, A1C, hypertension, dyslipidemia, diabetes onset, and sex. Diabetes Care. 2007, 30: 2523-2528. 10.2337/dc07-0282.
Scott LJ, Warram JH, Hanna LS, Laffel LM, Ryan L, Krolewski AS: A nonlinear effect of hyperglycemia and current cigarette smoking are major determinants of the onset of microalbuminuria in type 1 diabetes. Diabetes. 2001, 50: 2842-2849. 10.2337/diabetes.50.12.2842.
Mosca L, Linfante AH, Benjamin EJ, Berra K, Hayes SN, Walsh BW, Fabunmi RP, Kwan J, Mills T, Simpson SL: National study of physician awareness and adherence to cardiovascular disease prevention guidelines. Circulation. 2005, 111: 499-510. 10.1161/01.CIR.0000154568.43333.82.
Chaturvedi N, Stephenson JM, Fuller JH: The relationship between smoking and microvascular complications in the EURODIAB IDDM Complications Study. Diabetes Care. 1995, 18: 785-792. 10.2337/diacare.18.6.785.
American Diabetes Association: Diagnosis and classification of diabetes mellitus. Diabetes Care. 2010, 33: S62-S69.
Seino Y, Nanjo K, Tajima N, Kadowaki T, Kashiwagi A, Araki E, Ito C, Inagaki N, Iwamoto Y, Kasuga M, Hanafusa T, Haneda M, Ueki K: Report of the committee on the classification and diagnostic criteria of diabetes mellitus. Diabetol Int. 2010, 1: 2-20. 10.1007/s13340-010-0006-7.
Hirano T, Sakaue T, Misaki A, Murayama S, Takahashi T, Okada K, Takeuchi H, Yoshino G, Adachi M: Very low-density lipoprotein-apoprotein CI is increased in diabetic nephropathy: comparison with apoprotein CIII. Kidney Int. 2003, 63: 2171-2177. 10.1046/j.1523-1755.2003.00019.x.
Resnick HE, Foster GL, Bardsley J, Ratner RE: Achievement of American Diabetes Association clinical practice recommendations among U.S. adults with diabetes, 1999–2002: the National Health and Nutrition Examination Survey. Diabetes Care. 2006, 29: 531-537. 10.2337/diacare.29.03.06.dc05-1254.
Haire-Joshu D, Glasgow RE, Tibbs TL: American Diabetes Association: Smoking and diabetes. Diabetes Care. 2004, 27: S74-S75.
Nilsson PM, Gudbjörnsdottir S, Eliasson B, Cederholm J: Steering Committee of the Swedish National Diabetes Register: Smoking is associated with increased HbA1c values and microalbuminuria in patients with diabetes–data from the National Diabetes Register in Sweden. Diabetes Metab. 2004, 30: 261-268. 10.1016/S1262-3636(07)70117-9.
Orth SR, Ritz E, Schrier RW: The renal risks of smoking. Kidney Int. 1997, 51: 1669-1677. 10.1038/ki.1997.232.
Nilsson TK, Lithner F: Glycaemic control, smoking habits and diabetes duration affect the extrinsic fibrinolytic system in type I diabetic patients but microangiopathy does not. Acta Med Scand. 1988, 224: 123-129.
Mühlhauser I: Smoking and diabetes. Diabet Med. 1990, 7: 10-15. 10.1111/j.1464-5491.1990.tb01299.x.
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: 211-217. 10.1111/j.1365-2796.1990.tb00220.x.
Cadnapaphornchai P, Boykin JL, Berl T, McDonald KM, Schrier RW: Mechanism of effect of nicotine on renal water excretion. Am J Physiol. 1974, 227: 1216-1220.
Hultberg B, Isaksson A, Brattström L, Israelsson B: Elevated urinary excretion of beta-hexosaminidase in smokers. Eur J Clin Chem Clin Biochem. 1992, 30: 131-133.
Baron JA, La Vecchia C, Levi F: The antiestrogenic effect of cigarette smoking in women. Am J Obstet Gynecol. 1990, 162: 502-514.
MacMahon B, Trichopoulos D, Cole P, Brown J: Cigarette smoking and urinary estrogens. N Engl J Med. 1982, 307: 1062-1065. 10.1056/NEJM198210213071707.
Meek MD, Finch GL: Diluted mainstream cigarette smoke condensates activate estrogen receptor and aryl hydrocarbon receptor-mediated gene transcription. Environ Res. 1999, 80: 9-17. 10.1006/enrs.1998.3872.
Tankó LB, Christiansen C: An update on the antiestrogenic effect of smoking: a literature review with implications for researchers and practitioners. Menopause. 2004, 11: 104-109. 10.1097/01.GME.0000079740.18541.DB.
Michnovicz JJ, Hershcopf RJ, Naganuma H, Bradlow HL, Fishman J: Increased 2-hydroxylation of estradiol as a possible mechanism for the anti-estrogenic effect of cigarette smoking. N Engl J Med. 1986, 315: 1305-1309. 10.1056/NEJM198611203152101.
Navab M, Reddy S, Van Lenten BJ, Anantharamaiah GM, Fogelman AM: Role of dysfunctional HDL in atherosclerosis. J Lipid Res. 2009, 50: S145-S149.
Vaziri ND, Navab M, Fogelman AM: HDL metabolism and activity in chronic kidney disease. Nat Rev Nephrol. 2010, 6: 287-296. 10.1038/nrneph.2010.36.
Yokoyama H, Okudaira M, Otani T, Takaike H, Miura J, Saeki A, Uchigata Y, Omori Y: Existence of early-onset NIDDM Japanese demonstrating severe diabetic complications. Diabetes Care. 1997, 20: 844-847. 10.2337/diacare.20.5.844.
Parving HH: Diabetic nephropathy: prevention and treatment. Kidney Int. 2001, 60: 2041-2055. 10.1046/j.1523-1755.2001.00020.x.
Rossing P, Hougaard P, Parving HH: Risk factors for development of incipient and overt diabetic nephropathy in type 1 diabetic patients: a 10-year prospective observational study. Diabetes Care. 2002, 25: 859-864. 10.2337/diacare.25.5.859.
Plasma Lipoprotein-Associated Phospholipase A2 Levels Correlated with the Cardio-Ankle Vascular Index in Long-Term Type 2 Diabetes Mellitus Patients
Kazuhiko Kotani
International Journal of Molecular Sciences
Neurophysiological evaluation in newly diagnosed Diabetes Mellitus type 1
Dragana Matanovic, Srdjan Popovic, Biljana Parapid, Ivana Petronic, Dejan Nikolic
Open Medicine
Incidence and Risk Factors Involved in the Development of Nephropathy in Patients with Type 1 Diabetes Mellitus: Follow Up Since Onset
Maria José Goñi, Luis Forga, Berta Ibañez, Koldo Cambra, David Mozas, Emma Anda
Canadian Journal of Diabetes
The association between cigarette smoking and diabetic nephropathy in Chinese male patients
Qianqian Han, Shanshan Wang, Junlin Zhang, Rui Zhang, Ruikun Guo, Yiting Wang, Hanyu Li, Huan Xu, Fang Liu
Acta Diabetologica
Smoking and the risk of diabetic nephropathy in patients with type 1 and type 2 diabetes: a meta-analysis of observational studies
Ning Jiang, Feng Huang, Xiurong Zhang