INTRODUCTION

Diabetic nephropathy is the leading cause of end-stage renal disease and is also responsible for cardiovascular mortality [1-3]. About 30% of patients with diabetes eventually develop diabetic nephropathy [1,4]. In Korea, diabetic nephropathy is becoming a substantial health care problem as the number of patients with diabetes is continuously increasing [5,6].

Albuminuria and a decline in the glomerular filtration rate (GFR) are commonly used for early detection of diabetic nephropathy. Increased urinary albumin is the earliest clinical feature of diabetic nephropathy. Gradual declines in GFR follow functional and structural changes of glomeruli [4,7].

Smoking has been reported to be associated with the progression of diabetic nephropathy. In prospective studies, progression to diabetic nephropathy was more frequent in smokers than non-smokers [8-10]. These studies classified subjects as non-smokers, former smokers and current smokers and found the hazard highest for current smokers. These findings suggest that continued smoking is related to the development of diabetic nephropathy.

Many studies have also evaluated the association between smoking cessation and diabetic nephropathy. A recent decline in diabetes-related complications, including end-stage renal disease, was linked to management and improvement of risk factors including smoking cessation [11]. Other prospective studies have reported that smoking cessation slowed the progression of diabetic nephropathy [12,13].

Smoking has a known association with nephropathy in the non-diabetic population. Subjects classified as smokers at the time of study had a significantly higher prevalence of albuminuria and abnormal renal function [14,15]. Therefore, smoking, whether before or after being diagnosed with diabetes, might be expected to increase an individual’s risk of developing diabetic nephropathy. Previous studies, however, did not distinguish between the effect of smoking before and the effect of smoking after diagnosis. This study aims to make that distinction by considering the association between the presence of diabetic nephropathy and various smoking behaviors, specifically never smoking, smoking only before diagnosis, and smoking at any point in time after receiving a diagnosis of diabetes.

METHODS

We used data from the Korea National Health and Nutrition Examination Survey (KNHANES), a cross-sectional nationwide survey designed to assess the health and nutritional status of the Korean population [16]. The KNHANES selects a representative sample from the population and conducts personal interviews, physical examinations, and clinical and laboratory tests. Because the measurement of urinary albumin was introduced to the KNHANES in 2011, we used data from the 2011-2013 surveys. Females were excluded from our study because the reported prevalence of smoking among females in the survey was low. Moreover, research indicates that self-reports of smoking made by Asian females in similar surveys were unreliable [17]. Among the 9862 male participants during the three years, 708 subjects were reported to be diagnosed with diabetes by a physician. We excluded 79 subjects whose smoking status or other key variables were missing, leaving 629 male patients with diabetes in our data set. The KNHANES data were publicly available for research, so separate ethical approval by our institutional review board was not required.

Participants were classified as non-smokers, former smokers and current smokers based upon a smoking history taken as part of the survey. Within the class “former smokers”, we estimated the date of smoking cessation using details included in the smoking history. Questions pertaining to smoking cessation changed during our study period, so we applied different methods when estimating smoking cessation dates from different subsets of the survey data. With survey data from 2011 to 2012, we added smoking duration to the age of smoking initiation. With data from 2013, we subtracted the duration of smoking cessation from current age. By comparing the age of smoking cessation and the age of diabetes diagnosis, we divided former smokers, as defined in the survey, into two groups. “Former smokers”, as we define them, were those who smoked before the diagnosis of diabetes, but never after. “Continuing smokers” were those who smoked at any time after diagnosis of diabetes. By this definition, we included those reported to be current smokers in the KNHANES in our class “continuing smokers”. Finally, KNHANES participants classified “non-smoker” were included in the class “non-smokers” in our study.

We adopted the definition and classification of chronic kidney diseases recommended by the National Kidney Foundation Kidney Disease Outcomes Quality Initiative to define diabetic nephropathy [18]. Diabetic nephropathy was defined as the presence of albuminuria or test results that show a low GFR. Presence of albuminuria was defined as a spot urine albumin/creatinine ratio (ACR) ≥30 mg/g, including microalbuminuria (30 - 299 mg/g) and macroalbuminuria (≥300 mg/g). The Modification of Diet in Renal Disease formula was used to estimate the GFR: estimated GFR (mL/min/1.73 m²) = 186.3×(serum creatinine)^-1.154×(age)^-0.203 × 0.742 (if female). Low GFR was defined to be estimated GFR <60 mL/min/1.73 m².

We assessed known risk factors for diabetic nephropathy. They include age, duration of diabetes, hypertension, dyslipidemia, body mass index, systolic blood pressure, hemoglobin A1c (HbA1c), serum total cholesterol, and triglycerides. Duration of diabetes was calculated by taking the difference between the year of diabetes diagnosis and current age. Medication for hypertension or for dyslipidemia was self-reported. Body mass index was calculated by dividing weight in kilograms by squared height in meters. Because most of the participants reported that they used anti-diabetic medications to treat their diabetes, we used HbA1c <7.0% as our indicator of adequate glycemic control. Dyslipidemia was defined as serum total cholesterol ≥240 mg/dL, or serum triglyceride ≥ 200 mg/dL, or taking medication for dyslipidemia.

To begin our analysis, we classified subjects by our criteria for diabetic nephropathy. The 416 subjects that did not meet our criteria were labeled “normal”. The 213 subjects that met our criteria were assigned the label “diabetic nephropathy”. We then compared characteristics of the two groups and the prevalence of risk factors in the two groups. We performed Student’s t-tests when response values were continuous and chi-square tests when values were categorical. Multiple logistic regression analysis was used to investigate the independent association between smoking before and after diagnosis of diabetes and the presence of diabetic nephropathy after adjusting for age, duration of diabetes, body mass index, HbA1c, systolic blood pressure, medication for hypertension, and the presence of dyslipidemia. We separately analyzed the association with each of our criteria for diabetic nephropathy: albuminuria and low GFR. In the analysis of albuminuria, a multinomial regression model was used. Albuminuria was subdivided into normoalbuminuria (ACR <30 mg/g), microalbuminuria (ACR=30-299 mg/g), and macroalbuminuria (ACR ≥300 mg/g). GFR <60 mL/min/1.73 m² was considered low. We repeated the analysis, regressing diabetic nephropathy against smoking history according to the life time smoking history (non-smokers, former smokers, and current smokers) and further dividing life time former smokers by their smoking duration (<20 years and ≥20 years). The p-value <0.05 was considered statistically significant. All statistical analyses were performed using SAS version 9.4 (SAS Institute Inc., Cary, NC, USA).

RESULTS

The group of patients in our study, 629 male diagnosed with diabetes, is described by the basic characteristics recorded in Table 1. A large majority (85.7%) of patients smoked at some point in their lives. Among smokers, more than half (58.2%) continued smoking at some point after receiving their diagnosis of diabetes. Nearly 28% of all participants had albuminuria and slightly more than 12% had low GFR.

The overall prevalence of diabetic nephropathy was 33.9% (n=213) (Table 2). Compared to patients without diabetic nephropathy, patients with diabetic nephropathy were significantly older, had suffered diabetes for a longer period of time, had higher systolic blood pressure, were more likely to exhibit inadequate glycemic control, and were more likely to take medication for hypertension. Smoking behavior after diagnosis of diabetes was significantly different, with a higher proportion of continuing smokers who smoked at any time after diagnosis of diabetes (56.8% vs. 46.4%; p=0.009) in the group of patients with diabetic nephropathy. There were no significant differences in body mass index and the presence of dyslipidemia between the two groups.

We then made these comparisons in a different way, comparing these characteristics and risks across groups defined by each of the two criteria for diabetic nephropathy, albuminuria and low GFR. When grouped by albuminuria, there were significant differences in age, duration of diabetes, systolic blood pressure, HbA1c, medication for hypertension and smoking behavior after diagnosis of diabetes. When grouped by low GFR, there were significant differences in age, duration of diabetes, and medication for hypertension between the two groups.

Table 3 shows the association between smoking behavior after diagnosis of diabetes and the presence of diabetic nephropathy. The unadjusted odds ratio (OR) and 95% confidence intervals (CI) show that older age, longer duration of diabetes, higher systolic blood pressure, higher HbA1c, and taking medication for hypertension were significantly associated with the presence of diabetic nephropathy. After adjusting for all other variables, duration of diabetes and medication for hypertension became insignificant. The unadjusted OR (95% CI) for former smokers who had smoked only before their diagnosis of diabetes was 1.29 (0.74 to 2.24), and the adjusted OR was 1.23 (0.68 to 2.21). The unadjusted OR (95% CI) of continuing smokers who smoked at any time after diagnosis was 1.83 (1.08 to 3.09). The OR remained significant after adjusting for all covariates (adjusted OR, 2.12; 95% CI, 1.20 to 3.73).

Table 4 shows the association of smoking behavior after a diagnosis of diabetes with selected levels of albuminuria and with low GFR. The adjusted OR (95% CI) of smoking at any time after diabetes diagnosis, relative to normoalbuminuria, were 1.93 (1.01 to 3.69) for microalbuminuria and 3.60 (1.09 to 11.85) for macroalbuminuria. The corresponding OR (95% CI) for low GFR was 1.18 (0.54 to 2.55).

In the analysis classifying life time former smokers by their smoking duration, the adjusted OR (95% CI) for former smokers who smoked <20 years, former smokers who smoked ≥ 20 years, and current smokers were 1.15 (0.58 to 2.28), 1.54 (0.85 to 2.80) and 2.42 (1.33 to 4.39), respectively (Supplemental Table 1).

DISCUSSION

In this study we evaluated the association between smoking behavior and the presence of diabetic nephropathy, classifying smoking behavior relative to the date of diabetes diagnosis. Cigarette smoking, especially smoking that continued after a diagnosis of diabetes was independently associated with the presence of diabetic nephropathy.

In the literature, smoking was related with adverse outcomes on glomerular structure and function for patients with diabetes. Compared with nonsmoking patients with diabetes, smoking patients with diabetes had higher albumin excretion rates and thicker glomerular basement membranes [19]. The incidence or progression rate of diabetic nephropathy was higher in smokers than non-smokers [9,10]. In these studies the risk of nephropathy was highest for current smokers, followed by former smokers and non-smokers. This finding suggests that smoking, particularly continuous smoking, is associated with diabetic nephropathy.

Smoking also increases the risk of albuminuria or renal dysfunction in the non-diabetic population. According to some cross-sectional studies of non-diabetic persons, smoking was related with the presence of albuminuria or low GFR [14,20]. Smoking was also associated with increased prevalence of proteinuria in repeated health screening examinations [21]. In some of these studies, daily amounts of smoking showed a dose-response relationship with albuminuria [14,21]. Smoking exposure seems to be related with diabetic nephropathy, regardless of the point in time that the exposure occurred, before or after the onset of diabetes. In our results, the OR for former smokers who smoked only before diagnosis of diabetes was higher than for non-smokers but lower than for smokers who smoked at any time after receiving their diagnosis of diabetes. Therefore we conclude that smoking exposure, especially when diabetes is prevalent, is associated with diabetic nephropathy.

Some studies have suggested that smoking cessation can delay the progression of diabetic nephropathy. Lower progression to diabetic nephropathy or improvement of the ACR in former smokers had been observed in prospective studies of diabetic subjects who exhibited microalbuminuria [12,13,22]. It has been reported that total smoking pack-years showed a dose response relationship with the prevalence of diabetic nephropathy among former smokers [9,23]. A prospective study that focused on the relationship of smoking pack-years and the incidence of diabetes showed a similar result. In this study, the hazard of diabetes was higher as smoking pack-years increased and when the time since smoking cessation was shorter [24]. This dose-response relationship was partially shown in our analysis. When we stratified former smokers by smoking duration, the OR was higher for the group formed of those who smoked for longer periods of time. We could not expand the analysis to include subjects identified as current smokers in KNHANES, due to incomplete smoking duration information in the survey. We also considered the association of time between smoking cessation and diabetes diagnosis with the presence of diabetic nephropathy among former smokers (data not shown). The regression indicated a higher OR when the time interval was shorter, but the result was not statistically significant. To more fully reveal the effect of smoking, further prospective studies evaluating smoking in conjunction with diabetes and with diabetic complications will be required.

The pathogenesis of diabetic nephropathy from diabetes stems from high blood glucose and blood lipid levels. High blood glucose and lipids increase oxidative stress and induce inflammation of renal structures [25,26]. Smoking is associated with high blood lipids, and independently increases oxidative stress [27-29]. We assume that smoking participates in the development of diabetic nephropathy by mediating its progression along these pathways. Moreover, smokers take actions that exacerbate the impact of smoking. They have been shown to be unaware of the progression of a chronic disease, leading to low levels of treatment for that disease. Even when they are aware of disease, they, frequently, continue smoking. [30,31]. If the same pattern of behavior holds with diabetes, the delay in diagnosis and the delay in treatment increases the likelihood of complications. Microvascular complications may have already progressed by the time they receive a diagnosis of diabetes. If nothing else, delayed diagnosis and treatment results in prolonging the time in which the patient suffers in a hyperglycemic state [32]. Based on the literature and our findings, we conclude that smoking is independently associated with diabetic nephropathy, and that the impact is higher when diabetes is prevalent. We also cautiously interpret the literature and our findings to indicate that smoking cessation in patients with diabetes may delay the progression of diabetic nephropathy or slow the decrease of glomerular function.

When we grouped subjects separately by albuminuria and then by low GFR, rather than by diabetic nephropathy, we found that the prevalence of albuminuria was significantly higher among those that smoked at any point in time after diagnosis of diabetes. This finding was consistent with many other studies which evaluated smoking and albuminuria [8,20]. The distribution of smoking behavior, however, was not significantly different for those with normal and low GFR in our results. We do not know the exact reason for this, but some studies have reported that smoking can be related to either decreased or increased GFR [14,33]. They explained that smoking acutely induces a decrease in renal plasma flow, but that these repeated episodes alter the structure of glomerular vessels and result in hyperfiltration [14,34]. We assume that these conflicting effects of smoking over time have been mixed in our cross-sectional analysis.

There are several limitations to our study. First, we could not establish causal relationships between smoking behavior and diabetic nephropathy due to the cross-sectional study design. We could not determine whether smoking was associated with the early development or progression of diabetic nephropathy. Second, participation in the KNHANES was limited to non-institutionalized, community-dwelling individuals [35]. This may have led to the exclusion of patients with diabetes and advanced stages of diabetic nephropathy. Moreover, our study excluded female participants, and so, its results cannot be generalized to the entire diabetic population. Third, our study was limited to those diagnosed with diabetes by a physician. We required the diagnosis date. The 2011-2013 KNHANES surveys included 755 subjects who were undiagnosed but satisfied the diagnostic criteria for diabetes (fasting blood glucose ≥126 mg/dL or HbA1c ≥6.5%) based on blood tests [36]. While these individuals were not included in our study, we confirmed that they exhibited smoking behavior similar to that of our subjects. Therefore, we assume that the results of a study that included these undiagnosed individuals would be consistent with the results of this current study. Fourth, we used the date of diagnosis rather than diabetes onset in our study. In some cases diabetes could have been present for many years before diagnosis and diabetic nephropathy could have been present when diabetes was diagnosed [4]. However, the date of diagnosis still has a clinical implication. It may have been used to persuade diabetic smokers to quit. Fifth, the effect of covariates might not be well controlled. There were confounding factors which we could not include. KNHANES 2013 lacked information needed to estimate smoking duration for current smokers, and the 2011 and 2012 surveys did not ask participants about their daily tobacco consumption. In addition, we had incomplete data regarding insulin resistance. Serum insulin was not measured in KNHANES after 2011 [22]. Finally, our study did not clearly distinguish between type 1 diabetes and type 2 diabetes. We do know, however, that the proportion of diabetics with type 1 diabetes is small in Korea [37].

In conclusion, smoking after a diagnosis of diabetes is associated with the presence of diabetic nephropathy. Prospective research studies, evaluating the effect of smoking on diabetic nephropathy are required.

ACKNOWLEDGEMENTS

Notes

CONFLICT OF INTEREST

The authors have no conflicts of interest associated with the material presented in this paper.

SUPPLEMENTAL MATERIAL

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):109-119ArticlePubMedPMC
• 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):1833-1838ArticlePubMedPMC
• 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):421-426ArticlePubMed
• 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
• 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):17-22ArticlePubMedPMC
• 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):876-882ArticlePubMedPMC
• 7. Raptis AE, Viberti G. Pathogenesis of diabetic nephropathy. Exp Clin Endocrinol Diabetes 2001;109 Suppl 2: S424-S437Article
• 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):13-21ArticlePubMed
• 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/s00592-015-0822-0Article
• 10. Sawicki PT, Didjurgeit U, Mühlhauser I, Bender R, Heinemann L, Berger M. Smoking is associated with progression of diabetic nephropathy. Diabetes Care 1994;17(2):126-131ArticlePubMed
• 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):1514-1523ArticlePubMed
• 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):57-67ArticlePubMed
• 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):284-291ArticlePubMed
• 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):585-591ArticlePubMed
• 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):92-96ArticlePubMedPMC
• 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):69-77ArticlePubMedPMC
• 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):536-542ArticlePubMed
• 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):17-28ArticlePubMed
• 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):2730-2736ArticlePubMed
• 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):1933-1939ArticlePubMed
• 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):956-962ArticlePubMed
• 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):1456-1464ArticlePubMed
• 23. Hallan SI, Orth SR. Smoking is a risk factor in the progression to kidney failure. Kidney Int 2011;80(5):516-523ArticlePubMed
• 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):937-945ArticlePubMedPMC
• 25. Chakkarwar VA. Smoking in diabetic nephropathy: sparks in the fuel tank? World J Diabetes 2012;3(12):186-195ArticlePubMedPMC
• 26. Giacco F, Brownlee M. Oxidative stress and diabetic complications. Circ Res 2010;107(9):1058-1070ArticlePubMedPMC
• 27. Craig WY, Palomaki GE, Haddow JE. Cigarette smoking and serum lipid and lipoprotein concentrations: an analysis of published data. BMJ 1989;298(6676):784-788ArticlePubMedPMC
• 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):584-591ArticlePubMed
• 29. Esmatjes E, Flores L, Lario S, Clària J, Cases A, Iñigo P, et al. Smoking increases serum levels of transforming growth factor-beta in diabetic patients. Diabetes Care 1999;22(11):1915-1916ArticlePubMed
• 30. Gulliford MC. Low rates of detection and treatment of hypertension among current cigarette smokers. J Hum Hypertens 2001;15(11):771-773ArticlePubMed
• 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: 48ArticlePubMedPMC
• 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-S62Article
• 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):211-217ArticlePubMed
• 34. Orth SR. Effects of smoking on systemic and intrarenal hemodynamics: influence on renal function. J Am Soc Nephrol 2004;15 Suppl 1: S58-S63Article
• 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):96-104ArticlePubMedPMCPDF
• 36. American Diabetes Association. Executive summary: standards of medical care in diabetes--2011. Diabetes Care 2011;34 Suppl 1: S4-S10ArticlePDF
• 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):978-985ArticlePubMed

Figure & Data

References

Citations

Citations to this article as recorded by  

• Framework of Guidelines for Management of CKD in Asia
  Carol Pollock, Ju-young Moon, Le Pham Ngoc Ha, Pongsathorn Gojaseni, Chen Hua Ching, Lynn Gomez, Tak Mao Chan, Ming-Ju Wu, See Cheng Yeo, Pringgodigdo Nugroho, Anil Kumar Bhalla
  Kidney International Reports.2024; 9(4): 752.     CrossRef
• The hidden impact: the rate of nicotine metabolism and kidney health
  Xiaona Wang, Shanshan Su
  Frontiers in Endocrinology.2024;[Epub]     CrossRef
• Relating Onset of Health Conditions to Changes in Tobacco/Nicotine Use — Analyses based on the U.S. PATH Study *
  Peter N. Lee, John S. Fry
  Contributions to Tobacco & Nicotine Research.2023; 32(1): 1.     CrossRef
• Nicotine promotes renal interstitial fibrosis via upregulation of XIAP in an alpha7-nAChR-dependent manner
  Lili Guo, Yue Zhang, Jian Lu, Xiaoyang Li, Chao Zhang, Wenzhu Song, Yafang Dong, Xiangyang Zhou, Rongshan Li
  Molecular and Cellular Endocrinology.2023; 576: 111989.     CrossRef
• Lifestyle factors associated with a rapid decline in the estimated glomerular filtration rate over two years in older adults with type 2 diabetes–Evidence from a large national database in Japan
  Yaya Li, Makoto Fujii, Yuko Ohno, Asuka Ikeda, Kayo Godai, Yuko Nakamura, Yuya Akagi, Daisuke Yabe, Kazuyo Tsushita, Naoki Kashihara, Kei Kamide, Mai Kabayama, Patricia Khashayar
  PLOS ONE.2023; 18(12): e0295235.     CrossRef
• Development of a Risk Model for Predicting Microalbuminuria in the Chinese Population Using Machine Learning Algorithms
  Wei Lin, Songchang Shi, Huibin Huang, Nengying Wang, Junping Wen, Gang Chen
  Frontiers in Medicine.2022;[Epub]     CrossRef
• The Global Burden of Type 2 Diabetes Attributable to Tobacco: A Secondary Analysis From the Global Burden of Disease Study 2019
  Jianjun Bai, Fang Shi, Yudiyang Ma, Donghui Yang, Chuanhua Yu, Jinhong Cao
  Frontiers in Endocrinology.2022;[Epub]     CrossRef
• ASIAN PACIFIC SOCIETY OF NEPHROLOGY CLINICAL PRACTICE GUIDELINE ON DIABETIC KIDNEY DISEASE
  Adrian LIEW, Sunita BAVANANDAN, Narayan PRASAD, Muh Geot WONG, Jer Ming CHANG, Somchai EIAM‐ONG, Chuan‐Ming HAO, Chiao Yuen LIM, Soo Kun LIM, Kook‐Hwan OH, Hirokazu OKADA, Paweena SUSANTITAPHONG, Aida LYDIA, Huong Thi Bich TRAN, Russell VILLANUEVA, See Ch
  Nephrology.2020; 25(S2): 12.     CrossRef
• Impacts of Preoperative Smoking and Smoking Cessation Time on Preoperative Peripheral Blood Inflammatory Indexes and Postoperative Hospitalization Outcome in Male Patients with Lung Cancer and Surgery Treatment
  Xu Longming, Dai Shuiping, Zuo Yunxia
  Chinese Medical Sciences Journal.2020; 35(2): 170.     CrossRef
• Interaction of MTHFR C677T polymorphism with smoking in susceptibility to diabetic nephropathy in Chinese men with type 2 diabetes
  Liang Ma, Yongwei Jiang, Xiaomu Kong, Qian Liu, Hailing Zhao, Tingting Zhao, Yongtong Cao, Ping Li
  Journal of Human Genetics.2019; 64(1): 23.     CrossRef
• Le tabagisme actif : un facteur de risque majeur des maladies non transmissibles humaines dans une enquête hospitalière
  H. Ben Ayed, M. Ben Hmida, M. Ben Jemaa, M. Trigui, J. Jedidi, R. Karray, Y. Mejdoub, M. Kassis, H. Feki, S. Yaich, J. Damak
  Revue des Maladies Respiratoires.2019; 36(2): 171.     CrossRef
• Association of smoking and cardiometabolic parameters with albuminuria in people with type 2 diabetes mellitus: a systematic review and meta-analysis
  Debasish Kar, Clare Gillies, Mintu Nath, Kamlesh Khunti, Melanie J. Davies, Samuel Seidu
  Acta Diabetologica.2019; 56(8): 839.     CrossRef
• The global prevalence of tobacco use in type 2 diabetes mellitus patients: A systematic review and meta-analysis
  Peter Roderick, Victoria Turner, Anne Readshaw, Omara Dogar, Kamran Siddiqi
  Diabetes Research and Clinical Practice.2019; 154: 52.     CrossRef
• Cigarette smoking and risk of albuminuria in patients with type 2 diabetes: a systematic review and meta-analysis of observational studies
  Haili Xu, Jinliu Suo, Jing Lian
  International Urology and Nephrology.2018; 50(5): 911.     CrossRef
• Cigarette smoking and chronic kidney disease in the general population: a systematic review and meta-analysis of prospective cohort studies
  Jia Xia, Lin Wang, Zhiheng Ma, Liping Zhong, Ying Wang, Yachan Gao, Liqun He, Xiao Su
  Nephrology Dialysis Transplantation.2017; 32(3): 475.     CrossRef
• 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
  Oncotarget.2017; 8(54): 93209.     CrossRef
• Association of single-nucleotide polymorphisms in the RAGE gene and its gene- environment interactions with diabetic nephropathy in Chinese patients with type 2 diabetes
  Ying Zhang, Nan Jia, Feng Hu, Naijun Fan, Xiaohua Guo, Han Du, Changlin Mei, Chunfang Gao
  Oncotarget.2017; 8(57): 96885.     CrossRef