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Erschienen in: Acta Diabetologica 11/2018

31.07.2018 | Original Article

The association between cigarette smoking and diabetic nephropathy in Chinese male patients

verfasst von: Qianqian Han, Shanshan Wang, Junlin Zhang, Rui Zhang, Ruikun Guo, Yiting Wang, Hanyu Li, Huan Xu, Fang Liu

Erschienen in: Acta Diabetologica | Ausgabe 11/2018

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Abstract

Aims

To investigate the association between cigarette smoking and the clinicopathological features and renal prognosis of type 2 diabetic mellitus (T2DM) patients with diabetic nephropathy (DN).

Methods

A total of 223 T2DM male patients with biopsy-proven DN who received follow-up for at least 1 year were recruited. The patients were divided into two groups based on smoking status: smoking group and non-smoking group. Clinicopathologic differences were analyzed between the two groups. In addition, smokers were divided into two groups of binary analysis based on smoking amounts and two groups of former smokers and current smokers, and subgroups analysis based on age and DR, respectively. The influence of smoking on estimated glomerular filtration rate (eGFR) was estimated using logistic regression analysis and Cox regression on renal outcomes. Renal outcomes were defined by progression to end-stage renal disease (ESRD) or doubling of serum creatinine (D-SCr) level.

Results

Compared with nonsmokers, smoking patients had more moderate decline eGFR (p = 0.032) and tubular atrophy and interstitial fibrosis (p = 0.033). The adjusted logistic regression analysis suggested cigarette smoking was negatively associated with more severe decline eGFR (p = 0.015), especially for patients with DR (p = 0.010) and patients of age ≤ 50 years (p = 0.012) in the subgroup analysis. In the prognosis analysis, no obvious significant risk factor was shown about smoking. Interestingly, it was observed that former smokers had lower levels of plasma glucose and triglycerides than current smokers (both p < 0.05), while smokers with small smoking amounts had lower levels of triglycerides than those with large smoking amounts (p < 0.05).

Conclusion

Cigarette smoking patients with T2DM and DN had more moderate decline eGFR, especially for DN patients with DR, and milder IFTA lesions, although an obviously significant risk factor was not shown about smoking for DN.
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Literatur
1.
Zurück zum Zitat Cho NH, Shaw JE, Karuranga S et al (2018) IDF diabetes atlas: global estimates of diabetes prevalence for 2017 and projections for 2045. Diabetes Res Clin Pract 138:271–281CrossRef Cho NH, Shaw JE, Karuranga S et al (2018) IDF diabetes atlas: global estimates of diabetes prevalence for 2017 and projections for 2045. Diabetes Res Clin Pract 138:271–281CrossRef
2.
Zurück zum Zitat Wang L, Gao P, Zhang M et al (2017) Prevalence and ethnic pattern of diabetes and prediabetes in China in 2013. JAMA 317:2515–2523CrossRef Wang L, Gao P, Zhang M et al (2017) Prevalence and ethnic pattern of diabetes and prediabetes in China in 2013. JAMA 317:2515–2523CrossRef
3.
Zurück zum Zitat Menke A, Casagrande S, Geiss L, Cowie CC (2015) Prevalence of and trends in diabetes among adults in the United States, 1988–2012. JAMA 314:1021–1029CrossRef Menke A, Casagrande S, Geiss L, Cowie CC (2015) Prevalence of and trends in diabetes among adults in the United States, 1988–2012. JAMA 314:1021–1029CrossRef
4.
Zurück zum Zitat Alicic RZ, Rooney MT, Tuttle KR (2017) Diabetic kidney disease: challenges, progress, and possibilities. Clin J Am Soc Nephrol 12(12):2032–2045CrossRef Alicic RZ, Rooney MT, Tuttle KR (2017) Diabetic kidney disease: challenges, progress, and possibilities. Clin J Am Soc Nephrol 12(12):2032–2045CrossRef
5.
Zurück zum Zitat Saran R, Li Y, Robinson B et al: US renal data system 2015 annual data report: epidemiology of kidney disease in the United States. Am J Kidney Dis 2016; 67(3 Suppl 1):Svii,1–305 Saran R, Li Y, Robinson B et al: US renal data system 2015 annual data report: epidemiology of kidney disease in the United States. Am J Kidney Dis 2016; 67(3 Suppl 1):Svii,1–305
6.
Zurück zum Zitat O’Shaughnessy MM, Hogan SL, Poulton CJ et al (2017) Temporal and demographic trends in glomerular disease epidemiology in the Southeastern United States, 1986–2015. Clin J Am Soc Nephrol 12(4):614–623CrossRef O’Shaughnessy MM, Hogan SL, Poulton CJ et al (2017) Temporal and demographic trends in glomerular disease epidemiology in the Southeastern United States, 1986–2015. Clin J Am Soc Nephrol 12(4):614–623CrossRef
7.
Zurück zum Zitat Okada K, Osuga J, Kotani K et al (2012) Current smoking status may be associated with overt albuminuria in female patients with type 1 diabetes mellitus: a cross-sectional study. Tob Induc Dis 10(1):12–12CrossRef Okada K, Osuga J, Kotani K et al (2012) Current smoking status may be associated with overt albuminuria in female patients with type 1 diabetes mellitus: a cross-sectional study. Tob Induc Dis 10(1):12–12CrossRef
8.
Zurück zum Zitat Hsu CC, Hwang S, Tai TY et al (2009) Cigarette smoking and proteinuria in Taiwanese men with Type 2 diabetes mellitus. Diabet Med 27(3):295–302CrossRef Hsu CC, Hwang S, Tai TY et al (2009) Cigarette smoking and proteinuria in Taiwanese men with Type 2 diabetes mellitus. Diabet Med 27(3):295–302CrossRef
9.
Zurück zum Zitat Maeda I, Hayashi T, Sato KK et al (2011) Cigarette smoking and the association with glomerular hyperfiltration and proteinuria in healthy middle-aged men. Clin J Am Soc Nephrol 6(10):2462–2469CrossRef Maeda I, Hayashi T, Sato KK et al (2011) Cigarette smoking and the association with glomerular hyperfiltration and proteinuria in healthy middle-aged men. Clin J Am Soc Nephrol 6(10):2462–2469CrossRef
10.
Zurück zum Zitat Halimi JM, Giraudeau B, Vol S et al (2000) Effects of current smoking and smoking discontinuation on renal function and proteinuria in the general population. Kidney Int 58(3):1285–1292CrossRef Halimi JM, Giraudeau B, Vol S et al (2000) Effects of current smoking and smoking discontinuation on renal function and proteinuria in the general population. Kidney Int 58(3):1285–1292CrossRef
11.
Zurück zum Zitat Baggio B, Budakovic A, Dalla Vestra M et al (2002) Effects of cigarette smoking on glomerular structure and function in type 2 diabetic patients. J Am Soc Nephrol 13(11):2730–2736CrossRef Baggio B, Budakovic A, Dalla Vestra M et al (2002) Effects of cigarette smoking on glomerular structure and function in type 2 diabetic patients. J Am Soc Nephrol 13(11):2730–2736CrossRef
12.
Zurück zum Zitat Li L, Zhang X, Li Z et al (2017) Renal pathological implications in type 2 diabetes mellitus patients with renal involvement. J Diabetes Compl 31(1):114–121CrossRef Li L, Zhang X, Li Z et al (2017) Renal pathological implications in type 2 diabetes mellitus patients with renal involvement. J Diabetes Compl 31(1):114–121CrossRef
13.
Zurück zum Zitat Anguiano Gómez L, Lei Y, Kumar Devarapu S, Anders HJ (2017) The diabetes pandemic suggests unmet needs for ‘CKD with diabetes’ in addition to ‘diabetic nephropathy’-implications for pre-clinical research and drug testing. Nephrol Dial Transpl. https://doi.org/10.1093/ndt/gfx219 CrossRef Anguiano Gómez L, Lei Y, Kumar Devarapu S, Anders HJ (2017) The diabetes pandemic suggests unmet needs for ‘CKD with diabetes’ in addition to ‘diabetic nephropathy’-implications for pre-clinical research and drug testing. Nephrol Dial Transpl. https://​doi.​org/​10.​1093/​ndt/​gfx219 CrossRef
14.
Zurück zum Zitat Mannam P, Rauniyar N, Lam TT et al (2016) MKK3 influences mitophagy and is involved in cigarette smoke-induced inflammation. Free Radic Biol Med 101:102–115CrossRef Mannam P, Rauniyar N, Lam TT et al (2016) MKK3 influences mitophagy and is involved in cigarette smoke-induced inflammation. Free Radic Biol Med 101:102–115CrossRef
15.
Zurück zum Zitat Furuichi K, Yuzawa Y, Shimizu M et al (2018) Nationwide multicentre kidney biopsy study of Japanese patients with type 2 diabetes. Nephrol Dial Transpl 33(1):138–148CrossRef Furuichi K, Yuzawa Y, Shimizu M et al (2018) Nationwide multicentre kidney biopsy study of Japanese patients with type 2 diabetes. Nephrol Dial Transpl 33(1):138–148CrossRef
16.
Zurück zum Zitat Zhang J, Wang Y, Li L et al (2018) Diabetic retinopathy may predict the renal outcomes of patients with diabetic nephropathy. Ren Fail 40(1):243–251CrossRef Zhang J, Wang Y, Li L et al (2018) Diabetic retinopathy may predict the renal outcomes of patients with diabetic nephropathy. Ren Fail 40(1):243–251CrossRef
17.
Zurück zum Zitat Tervaert TWC, Mooyaart AL, Amann K et al (2010) Pathologic classification of diabetic nephropathy. J Am Soc Nephrol 21(4):556–563CrossRef Tervaert TWC, Mooyaart AL, Amann K et al (2010) Pathologic classification of diabetic nephropathy. J Am Soc Nephrol 21(4):556–563CrossRef
18.
Zurück zum Zitat Miyatake N, Moriyasu H, Sakano N et al (2010) Influence of cigarette smoking on estimated glomerular filtration rate (eGFR) in Japanese male workers. Acta Med Okayama 64(6):385–390PubMed Miyatake N, Moriyasu H, Sakano N et al (2010) Influence of cigarette smoking on estimated glomerular filtration rate (eGFR) in Japanese male workers. Acta Med Okayama 64(6):385–390PubMed
19.
Zurück zum Zitat Coresh J, Astor BC, Greene T et al (2003) Prevalence of chronic kidney disease and decreased kidney function in the adult US population: third national health and nutrition examination survey. Am J Kidney Dis 41(1):1–12CrossRef Coresh J, Astor BC, Greene T et al (2003) Prevalence of chronic kidney disease and decreased kidney function in the adult US population: third national health and nutrition examination survey. Am J Kidney Dis 41(1):1–12CrossRef
20.
Zurück zum Zitat Nosadini R, Tonolo G (2004) Relationship between blood glucose control, pathogenesis and progression of diabetic nephropathy. J Am Soc Nephrol 15(90010):1–5CrossRef Nosadini R, Tonolo G (2004) Relationship between blood glucose control, pathogenesis and progression of diabetic nephropathy. J Am Soc Nephrol 15(90010):1–5CrossRef
21.
Zurück zum Zitat Benowitz NL, Jacob (1984) P 3rd: daily intake of nicotine during cigarette smoking. Clin Pharmacol Ther 35(4):499–504CrossRef Benowitz NL, Jacob (1984) P 3rd: daily intake of nicotine during cigarette smoking. Clin Pharmacol Ther 35(4):499–504CrossRef
22.
Zurück zum Zitat Kozlowski LT, Mehta NY, Sweeney CT et al (1998) Filter ventilation and nicotine content of tobacco in cigarettes from Canada, the United Kingdom, and the United States. Tob Control 7(4):369–375CrossRef Kozlowski LT, Mehta NY, Sweeney CT et al (1998) Filter ventilation and nicotine content of tobacco in cigarettes from Canada, the United Kingdom, and the United States. Tob Control 7(4):369–375CrossRef
23.
Zurück zum Zitat Armitage A, Dollery C, Houseman T et al (1978) Absorption of nicotine from small cigars. Clin Pharmacol Ther 23(2):143–151CrossRef Armitage A, Dollery C, Houseman T et al (1978) Absorption of nicotine from small cigars. Clin Pharmacol Ther 23(2):143–151CrossRef
24.
Zurück zum Zitat Pankow JF (2001) A consideration of the role of gas/particle partitioning in the deposition of nicotine and other tobacco smoke compounds in the respiratory tract. Chem Res Toxicol 14(11):1465–1481CrossRef Pankow JF (2001) A consideration of the role of gas/particle partitioning in the deposition of nicotine and other tobacco smoke compounds in the respiratory tract. Chem Res Toxicol 14(11):1465–1481CrossRef
25.
Zurück zum Zitat Patterson F, Benowitz N, Shields P et al (2003) Individual differences in nicotine intake per cigarette. Cancer Epidemiol Biomark Prev 12(5):468–471 Patterson F, Benowitz N, Shields P et al (2003) Individual differences in nicotine intake per cigarette. Cancer Epidemiol Biomark Prev 12(5):468–471
26.
Zurück zum Zitat Benowitz NL, Jacob P 3rd (1985) Nicotine renal excretion rate influences nicotine intake during cigarette smoking. J Pharmacol Exp Ther 234(1):153–155PubMed Benowitz NL, Jacob P 3rd (1985) Nicotine renal excretion rate influences nicotine intake during cigarette smoking. J Pharmacol Exp Ther 234(1):153–155PubMed
27.
Zurück zum Zitat Willi C, Bodenmann P, Ghali WA et al (2007) Active smoking and the risk of type 2 diabetes—a systematic review and meta-analysis. JAMA 298:2654–2664CrossRef Willi C, Bodenmann P, Ghali WA et al (2007) Active smoking and the risk of type 2 diabetes—a systematic review and meta-analysis. JAMA 298:2654–2664CrossRef
28.
Zurück zum Zitat Tomaszewski M, Charchar FJ, Maric C et al (2007) Glomerular hyperfiltration: a new marker of metabolic risk. Kidney Int 71:816–821CrossRef Tomaszewski M, Charchar FJ, Maric C et al (2007) Glomerular hyperfiltration: a new marker of metabolic risk. Kidney Int 71:816–821CrossRef
29.
Zurück zum Zitat Benjamin LE (2001) Glucose, VEGF-A, and diabetic complications. Am J Pathol 158:1199–1206CrossRef Benjamin LE (2001) Glucose, VEGF-A, and diabetic complications. Am J Pathol 158:1199–1206CrossRef
30.
Zurück zum Zitat Ritz E, Benck U, Franek E et al (1998) Effects of smoking on renal hemodynamics in healthy volunteers and in patients with glomerular disease. J Am Soc Nephrol 9:1798–1804PubMed Ritz E, Benck U, Franek E et al (1998) Effects of smoking on renal hemodynamics in healthy volunteers and in patients with glomerular disease. J Am Soc Nephrol 9:1798–1804PubMed
31.
Zurück zum Zitat Hansen HP, Rossing K, Jacobsen P et al (1996) The acute effect of smoking on systemic haemodynamics, kidney and endothelial functions in insulin-dependent diabetic patients with microalbuminuria. Scand J Clin Lab Invest 56:393–399CrossRef Hansen HP, Rossing K, Jacobsen P et al (1996) The acute effect of smoking on systemic haemodynamics, kidney and endothelial functions in insulin-dependent diabetic patients with microalbuminuria. Scand J Clin Lab Invest 56:393–399CrossRef
32.
Zurück zum Zitat Halimi JM, Philippon C, Mimran A (1998) Contrasting renal effects of nicotine in smokers and non-smokers. Nephrol Dial Transpl 13:940–944CrossRef Halimi JM, Philippon C, Mimran A (1998) Contrasting renal effects of nicotine in smokers and non-smokers. Nephrol Dial Transpl 13:940–944CrossRef
33.
Zurück zum Zitat Pawlik WW, Jacobson ED, Banks RO (1985) Actions of nicotine on renal function in dogs. Proc Soc Exp Biol Med 178:585–590CrossRef Pawlik WW, Jacobson ED, Banks RO (1985) Actions of nicotine on renal function in dogs. Proc Soc Exp Biol Med 178:585–590CrossRef
34.
Zurück zum Zitat Tamaoki L, Oshiro-Monreal FM, Helou CM (2009) Effects of nicotine exposure on renal function of normal and hypercholesterolemic rats. Am J Nephrol 30:377–382CrossRef Tamaoki L, Oshiro-Monreal FM, Helou CM (2009) Effects of nicotine exposure on renal function of normal and hypercholesterolemic rats. Am J Nephrol 30:377–382CrossRef
35.
Zurück zum Zitat Macklin KD, Maus AD, Pereira EF et al (1998) Human vascular endothelial cells express functional nicotinic acetylcholine receptors. J Pharmacol Exp Ther 287:435–439PubMed Macklin KD, Maus AD, Pereira EF et al (1998) Human vascular endothelial cells express functional nicotinic acetylcholine receptors. J Pharmacol Exp Ther 287:435–439PubMed
36.
Zurück zum Zitat Nasr SH, D’Agati VD (2007) Nodular glomerulosclerosis in the nondiabetic smoker. J Am Soc Nephrol 18:2032–2036CrossRef Nasr SH, D’Agati VD (2007) Nodular glomerulosclerosis in the nondiabetic smoker. J Am Soc Nephrol 18:2032–2036CrossRef
37.
Zurück zum Zitat Heeschen C, Jang JJ, Weis M et al (2001) Nicotine stimulates angiogenesis and promotes tumor growth and atherosclerosis. Nat Med 7:833–839CrossRef Heeschen C, Jang JJ, Weis M et al (2001) Nicotine stimulates angiogenesis and promotes tumor growth and atherosclerosis. Nat Med 7:833–839CrossRef
38.
Zurück zum Zitat Wang H, Yu M, Ochani M et al (2003) Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 421:384–388CrossRef Wang H, Yu M, Ochani M et al (2003) Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 421:384–388CrossRef
39.
Zurück zum Zitat Halimi JM, Giraudeau B, Vol S et al (2000) : Effects of current smoking and smoking discontinuation on renal function and proteinuria in the general population. Kidney Int 58:1285–1292CrossRef Halimi JM, Giraudeau B, Vol S et al (2000) : Effects of current smoking and smoking discontinuation on renal function and proteinuria in the general population. Kidney Int 58:1285–1292CrossRef
40.
Zurück zum Zitat Rossing P, Hougaard P, Parving HH (2002) Risk factors for development of incipient and overt diabetic nephropathy in type 1 diabetic patients: a 10-year prospective observational study. Diabetes Care 25:859–864CrossRef Rossing P, Hougaard P, Parving HH (2002) Risk factors for development of incipient and overt diabetic nephropathy in type 1 diabetic patients: a 10-year prospective observational study. Diabetes Care 25:859–864CrossRef
41.
Zurück zum Zitat Ejerblad E, Fored CM, Lindblad P et al (2004) Association between smoking and chronic renal failure in a nationwide population based case—control study. J Am Soc Nephrol 15:2178–2185 9CrossRef Ejerblad E, Fored CM, Lindblad P et al (2004) Association between smoking and chronic renal failure in a nationwide population based case—control study. J Am Soc Nephrol 15:2178–2185 9CrossRef
42.
Zurück zum Zitat Hallan SI, Orth SR (2011) Smoking is a risk factor in the progression to kidney failure. Kidney Int 80:516–523CrossRef Hallan SI, Orth SR (2011) Smoking is a risk factor in the progression to kidney failure. Kidney Int 80:516–523CrossRef
43.
Zurück zum Zitat Jain G, Jaimes EA (2013) Nicotine signaling and progression of chronic kidney disease in smokers. Biochem Pharmacol 15(8):1215–1223 86(CrossRef Jain G, Jaimes EA (2013) Nicotine signaling and progression of chronic kidney disease in smokers. Biochem Pharmacol 15(8):1215–1223 86(CrossRef
44.
Zurück zum Zitat Lhotta K, Rumpelt HJ, König P et al (2002) Cigarette smoking and vascular pathology in renal biopsies. Kidney Int 61(2):648–654CrossRef Lhotta K, Rumpelt HJ, König P et al (2002) Cigarette smoking and vascular pathology in renal biopsies. Kidney Int 61(2):648–654CrossRef
45.
Zurück zum Zitat Leone A, Landini L (2013) Vascular pathology from smoking: look at the microcirculation! Curr Vasc Pharmacol 11(4):524–530CrossRef Leone A, Landini L (2013) Vascular pathology from smoking: look at the microcirculation! Curr Vasc Pharmacol 11(4):524–530CrossRef
46.
Zurück zum Zitat Orth SR, Hallan SI (2008) Smoking: a risk factor for progression of chronic kidney disease and for cardiovascular morbidity and mortality in renal patients—absence of evidence or evidence of absence? Clin J Am Soc Nephrol 3:226–236CrossRef Orth SR, Hallan SI (2008) Smoking: a risk factor for progression of chronic kidney disease and for cardiovascular morbidity and mortality in renal patients—absence of evidence or evidence of absence? Clin J Am Soc Nephrol 3:226–236CrossRef
47.
Zurück zum Zitat Agarwal PK, van den Born J, van Goor H et al (2012) Renoprotective effects of long-term oral nicotine in a rat model of spontaneous proteinuria. Am J Physiol Renal Physiol 302:F895–F904CrossRef Agarwal PK, van den Born J, van Goor H et al (2012) Renoprotective effects of long-term oral nicotine in a rat model of spontaneous proteinuria. Am J Physiol Renal Physiol 302:F895–F904CrossRef
Metadaten
Titel
The association between cigarette smoking and diabetic nephropathy in Chinese male patients
verfasst von
Qianqian Han
Shanshan Wang
Junlin Zhang
Rui Zhang
Ruikun Guo
Yiting Wang
Hanyu Li
Huan Xu
Fang Liu
Publikationsdatum
31.07.2018
Verlag
Springer Milan
Erschienen in
Acta Diabetologica / Ausgabe 11/2018
Print ISSN: 0940-5429
Elektronische ISSN: 1432-5233
DOI
https://doi.org/10.1007/s00592-018-1197-9

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