Tobacco, Cigarettes, and the Liver: The Smoking Gun
2021; Elsevier BV; Volume: 11; Issue: 6 Linguagem: Inglês
10.1016/j.jceh.2021.07.016
ISSN2213-3453
AutoresMadhumita Premkumar, Anil C. Anand,
Tópico(s)Hepatitis B Virus Studies
ResumoThe association between alcohol and liver disease, including alcoholic hepatitis, cirrhosis, acute-on-chronic liver failure, and hepatocellular carcinoma, has been well described, but the same cannot be said for the association between smoking, water pipe or tobacco chewing. A review of cumulative evidence suggests that smoking is independently a risk factor for liver fibrosis and contributes to carcinogenesis in HCC. Smoking-related fibrosis has been reported in patients with nonalcoholic fatty liver disease, primary biliary cholangitis, alcoholic liver disease and chronic viral hepatitis. Heavy smoking leads to systemic inflammation, oxidative stress, insulin resistance, and results in tissue hypoxia, as well as free radical damage. Other than damaging the liver, patients also suffer from the systemic effects of the 4000 chemicals associated with tobacco, which include nitrosamines, aromatic hydrocarbons, nicotine, nornicotine, and other alkaloids. These include respiratory ailments, cancer of the lungs, oral cavity, esophagus, pancreas and colon, atherosclerotic vascular disease, and stroke. The association between alcohol and liver disease, including alcoholic hepatitis, cirrhosis, acute-on-chronic liver failure, and hepatocellular carcinoma, has been well described, but the same cannot be said for the association between smoking, water pipe or tobacco chewing. A review of cumulative evidence suggests that smoking is independently a risk factor for liver fibrosis and contributes to carcinogenesis in HCC. Smoking-related fibrosis has been reported in patients with nonalcoholic fatty liver disease, primary biliary cholangitis, alcoholic liver disease and chronic viral hepatitis. Heavy smoking leads to systemic inflammation, oxidative stress, insulin resistance, and results in tissue hypoxia, as well as free radical damage. Other than damaging the liver, patients also suffer from the systemic effects of the 4000 chemicals associated with tobacco, which include nitrosamines, aromatic hydrocarbons, nicotine, nornicotine, and other alkaloids. These include respiratory ailments, cancer of the lungs, oral cavity, esophagus, pancreas and colon, atherosclerotic vascular disease, and stroke. About a third of males worldwide smoke tobacco, as per the estimate of the World Health Organization (WHO). Tobacco smoking was the attributable cause of death in 100 million individuals globally over the course of the 20th century.1He J. Gu D. Wu X. et al.Major causes of death among men and women in China.N Engl J Med. 2005; 353 (PMID: 16162883): 1124-1134https://doi.org/10.1056/NEJMsa050467Crossref PubMed Scopus (1039) Google Scholar,2Pham T.M. Fujino Y. Ide R. et al.Mortality attributable to cigarette smoking in a cohort study in Japan.Eur J Epidemiol. 2007; 22 (Epub 2007 Jul 25. PMID: 17653602): 599-605https://doi.org/10.1007/s10654-007-9161-yCrossref PubMed Scopus (14) Google Scholar Thus, tobacco consumption is a leading cause of preventable morbidity and mortality. The available forms of tobacco in India include cigarettes, cigars, indigenous bidi, water pipes, and smokeless tobacco (ST) mixed with additional components like betel quid and gutkha. The relationship of smoking with lung cancer is well described, but the effects of smoking on the liver are less well known. Smoking and tobacco consumption can increase the fibrogenic and carcinogenic effects of alcohol and exacerbate disease progression in nonalcoholic fatty liver disease (NAFLD), primary biliary cholangitis (PBC), and chronic liver disease (CLD) due to hepatitis B virus (HBV) and hepatitis C virus (HCV) infection.3Gershwin M.E. Selmi C. Worman H.J. et al.USA PBC Epidemiology GroupRisk factors and comorbidities in primary biliary cirrhosis: a controlled interview-based study of 1032 patients.Hepatology. 2005; 42 (PMID: 16250040; PMCID: PMC3150736): 1194-1202https://doi.org/10.1002/hep.20907Crossref PubMed Scopus (442) Google Scholar,4El-Zayadi A.R. Heavy smoking and liver.World J Gastroenterol. 2006; 126098e101Crossref Scopus (119) Google Scholar The risk of death increases in proportion to the extent of exposure to cigarette smoke. The latter can be estimated by the age of the first initiation of the tobacco habit, number of cigarettes smoked per day, duration of smoking, and depth of inhalation.5Altamirano J. Bataller R. Cigarette smoking and chronic liver diseases.Gut. 2010; 59: 1159-1162Crossref PubMed Scopus (71) Google Scholar Another matter of concern is second-hand smoking and environmental cigarette smoke exposure to nonsmokers, which has shown an increased risk of cardiovascular disease and asthma. The effects of second-hand smoke on liver disease progression are still unclear, though data suggests that such individuals are at an increased risk.6Janson C. Chinn S. Jarvis D. Zock J.P. Torén K. Burney P. European Community Respiratory Health Survey. Effect of passive smoking on respiratory symptoms, bronchial responsiveness, lung function, and total serum IgE in the European Community Respiratory Health Survey: a cross-sectional study.Lancet. 2001; 358 (Erratum in: Lancet 2002 Jan 26;359(9303):360. PMID: 11784622): 2103-2109https://doi.org/10.1016/S0140-6736(01)07214-2Abstract Full Text Full Text PDF PubMed Scopus (184) Google Scholar In India, ST like gutkha is frequently consumed by men and women alike, which is under-reported in epidemiological data on liver disease. India has 275 million tobacco consumers, which amounts to about 35% of adults as per the Global Adult Tobacco Survey.7World Health OrganizationGlobal Adult Tobacco Survey (GATS) India, 2009-2010. Ministry of Health and Family Welfare, Government of India, New Delhi, India2010https://ntcp.nhp.gov.in/assets/document/surveys-reports-publications/Global-Adult-Tobacco-Survey-India-2009-2010-Report.pdfDate accessed: July 2, 2021Google Scholar,8Sarkar B.K. Reddy K.S. Priorities for tobacco control research in India.Addiction. 2012; 107: 2066-2068Crossref PubMed Scopus (14) Google Scholar This figure includes 164 million ST consumers, 69 million smokers, and 42 million consumers who partake more than one form of tobacco. All the betel quid, paan or gutkha mixtures are classified as group 1 carcinogens by the International Agency for Research on Cancer, as they contain areca nut, betel leaf, etc., and contain a high amount of nicotine.9IARC Working Group on the Evaluation of Carcinogenic Risks to HumansBetel-quid and areca-nut chewing and some areca-nut derived nitrosamines.IARC Monogr Eval Carcinog Risks Hum. 2004; 85 (PMID: 15635762; PMCID: PMC4781453): 1-334PubMed Google Scholar Nearly 4200 chemical constituents are found in ST. The areca nut industry has created two forms of mixtures; the first is betel quid/areca nut aromatic mixtures called "paan masala," and the second is called gutkha if tobacco was added. This mixture contains sundried, roasted, chopped tobacco, areca nut, slaked lime, and catechu.10Sankhla B. Kachhwaha K. Hussain S.Y. Saxena S. Sireesha S.K. Bhargava A. Genotoxic and carcinogenic effect of gutkha: a fast-growing smokeless tobacco.Addict Health. 2018; 10: 52-63https://doi.org/10.22122/ahj.v10i1.537Crossref PubMed Google Scholar Salivary, blood, and urine levels of derivatives of ST products are very much like that of smoking and constitute an equal and underestimated risk to the progression of liver disease and cancer in India. Additional data regarding additive effects of polyphenols, tannins, alkaloids, nicotine, and musk ketones extracted from these products is required due to the wide consumption of ST in India.11Stepanov I. Hecht S.S. Ramakrishnan S. Gupta P.C. Tobacco-specific nitrosamines in smokeless tobacco products marketed in India.Int J Cancer. 2005; 116: 16-19Crossref PubMed Scopus (89) Google Scholar Prior data has shown that consuming tobacco increases the production of interleukins (IL-1, IL-6), tumor necrosis factor (TNF α), angiogenic agents like vascular endothelial growth factor (VEGF), fibrosis mediators (transforming growth factor β), and angiotensin II. Smoking also induces the nicotinamide adenine dinucleotide phosphate (NADPH) oxidase system, impairs antioxidant pathways like glutathione, and leads to free radical lipid peroxidation. This leads further to hepatocellular inflammation, cell damage, hepatic stellate cell activation, mesangial cell activation, leading to the proliferation of fibrotic mediators, matrix metalloproteinases, and extracellular matrix proteins. Another mechanism of fibrosis is iron deposition. Heavy smokers with chronic hepatitis C have polycythemia and iron deposition.12El-Zayadi A.R. Selim O. Hamdy H. et al.Heavy cigarette smoking induces hypoxic polycythemia (erythrocytosis) and hyperuricemia in chronic hepatitis C patients with reversal of clinical symptoms and laboratory parameters with therapeutic phlebotomy.Am J Gastroenterol. 2002; 97: 1264e5Crossref Google Scholar Smoking leads to vascular vasoconstriction, endothelial dysfunction, smooth muscle proliferation, reduced nitric oxide and tissue hypoxia, and hepatocellular injury. Figure 1 shows the mechanism of liver injury and inflammatory pathways linking smoking and organ damage. Smoking has pleiotropic effects through its constituent chemicals that act on the lung, the cardiovascular system through systemic effects of inflammatory pathways like mitogen-activated kinases (MAPK). Nuclear factor-kappa B and signal transducer and activator of transcription (STAT), gene induction, and epigenetic modifiers. The systemic inflammation, increased lipid peroxidation, free radical injury, and endothelial dysfunction contribute to tissue hypoxia, iron accumulation, and liver cell injury that progresses to liver fibrosis over time. Impaired wound healing leads to impaired hepatic regeneration exacerbating fibrosis and predisposing to replication errors and de novo mutations, possibly a link to carcinogenesis. The association of smoking, alcohol, and risk of cirrhosis suggests that environmental influences need to be estimated in studies on disease pathogenesis.13Yamada M. Wong F.L. Fujiwara S. Tatsukawa Y. Suzuki G. Smoking and alcohol habits as risk factors for benign digestive diseases in a Japanese population: the radiation effects research foundation adult health study.Digestion. 2005; 71: 231-237Crossref PubMed Scopus (13) Google Scholar A common abnormality observed in persons who consume tobacco is liver injury, manifested as abnormal liver function tests. It is associated with an elevation of the liver enzyme levels like alkaline phosphatase (ALP) and gamma glutamyl transpeptidase (GGT). Jang et al showed that in a multivariate hazards model adjusted for age, gender, BMI, alcohol, and coffee drinking, current smokers had significantly lower serum levels of total protein and albumin and higher GGT levels compared with never or past smokers. Daily and lifetime smoking affected the serum levels of total protein, albumin, and GGT but did not affect aspartate transaminase (AST) or alanine transaminase (ALT). The effect of smoking on ALP is confounded by the association of osteoporosis and bone turnover origin of this enzyme, especially in older individuals. The consumption of coffee has protective effects on transaminases, while alcohol worsens the GGT level.14Jang E.S. Jeong S.H. Hwang S.H. et al.Effects of coffee, smoking, and alcohol on liver function tests: a comprehensive cross-sectional study.BMC Gastroenterol. 2012; 12 (PMID: 23075166; PMCID: PMC3531257): 145https://doi.org/10.1186/1471-230X-12-145Crossref PubMed Scopus (36) Google Scholar Thus, alcohol, smoking, lifestyle, and coffee and tea intake are all factors, which modify a genetic predisposition to liver disease. Smoking and ST consumption is undoubtedly an underrecognized pathophysiological link in CLD progression.15Khalaf N. White D. Kanwal F. et al.Coffee and caffeine are associated with decreased risk of advanced hepatic fibrosis among patients with hepatitis C.Clin Gastroenterol Hepatol. 2015; 13 (e3): 1521-1531Abstract Full Text Full Text PDF PubMed Scopus (32) Google Scholar,16Alferink L.J.M. Fittipaldi J. Kiefte-de Jong J.C. et al.Coffee and herbal tea consumption is associated with lower liver stiffness in the general population: the Rotterdam study.J Hepatol. 2017; 67 (Epub 2017 Jun 1. PMID: 28578837): 339-348https://doi.org/10.1016/j.jhep.2017.03.013Abstract Full Text Full Text PDF PubMed Scopus (49) Google Scholar Smoking adversely impacts innate and adaptive immunity and can aggravate pathological immune responses while reducing defensive immune mechanisms. Smoking affects cells involved in the innate immune response, including antigen-presenting cells (APCs) like dendritic cells, macrophages, and natural killer cells.12El-Zayadi A.R. Selim O. Hamdy H. et al.Heavy cigarette smoking induces hypoxic polycythemia (erythrocytosis) and hyperuricemia in chronic hepatitis C patients with reversal of clinical symptoms and laboratory parameters with therapeutic phlebotomy.Am J Gastroenterol. 2002; 97: 1264e5Crossref Google Scholar,13Yamada M. Wong F.L. Fujiwara S. Tatsukawa Y. Suzuki G. Smoking and alcohol habits as risk factors for benign digestive diseases in a Japanese population: the radiation effects research foundation adult health study.Digestion. 2005; 71: 231-237Crossref PubMed Scopus (13) Google Scholar The maturation of dendritic cells and NK cells of the innate response are also impaired.17Qiu F. Liang C.L. Liu H. et al.Impacts of cigarette smoking on immune responsiveness: up and down or upside down?.Oncotarget. 2017; 8: 268-284https://doi.org/10.18632/oncotarget.13613Crossref PubMed Scopus (232) Google Scholar Smoking also affects the adaptive immune response mediators, including T helper cells (Th1/Th2/Th17), CD8+ T cells, CD4+ T regulatory (Treg) cells, and memory T/B lymphocytes. The molecular pathways affected include nuclear factor kappa B (NF κB), MAP kinases, and epigenetic responses like DNA methylation, histone modification, etc. (Figure 1). Data suggests that smoking can contribute to autoimmune diseases like rheumatoid arthritis, lupus, Crohn's disease, etc. Broadly, smoking increases the CD8+/CD4+ ratio and enhances Th17 and CD4+FoxP3+ Treg cells effects. Smoking reduces immunosuppressive Tregs in autoimmune disease and increases Treg effects in lung disease, leading to conflicting regulatory effects and predisposing to infections. Smoking impairs the function of memory T and B cells.17Qiu F. Liang C.L. Liu H. et al.Impacts of cigarette smoking on immune responsiveness: up and down or upside down?.Oncotarget. 2017; 8: 268-284https://doi.org/10.18632/oncotarget.13613Crossref PubMed Scopus (232) Google Scholar Smoking results in systemic inflammation and tissue hypoxemia, oxidative stress, and insulin resistance. This is further exacerbated in the presence of metabolic syndrome and increases the risk of diabetes, cardiovascular, and cerebrovascular events. The mechanisms and cellular effects of smoking and NAFLD are shown in Figure 2. An interesting study demonstrating the effects of smoking in an obese rat model of NAFLD was performed by Azzalini et al, who exposed obese Zucker rats to cigarette smoke and observed activation of pathways, inflammatory mediators, immunohistochemistry, and changes in liver histology. Obese rats exhibited features of the metabolic syndrome, including dyslipidemia, insulin resistance, and histological features of NAFLD. Smoking increased the expression of tissue inhibitor of metalloproteinase-1 and procollagen-alpha2 (I) peptide in obese Zucker rats who were exposed to 2 cigarettes/day, 5 days per week, for 4 weeks, but not in the control rats who were not exposed to cigarette smoke. This was mediated by increased gene expression of AKT and extracellular signal-regulated kinase (ERK). This study showed that 4 weeks of exposure to cigarette smoke exacerbated NAFLD, but the duration was not long enough to establish a link with fibrosis or change in body weight or insulin resistance.18Azzalini L. Ferrer E. Ramalho L.N. et al.Cigarette smoking exacerbates nonalcoholic fatty liver disease in obese rats.Hepatology. 2010; 51 (PMID: 20432253): 1567-1576https://doi.org/10.1002/hep.23516Crossref PubMed Scopus (100) Google Scholar Prior systematic reviews have shown that NAFLD patients have a dose-response relationship with smoking, as those with advanced fibrosis reported higher pack-years of cigarette consumption as compared with early or no fibrosis.19Akhavan Rezayat A. Dadgar Moghadam M. Ghasemi Nour M. et al.Association between smoking and non-alcoholic fatty liver disease: a systematic review and meta-analysis.SAGE Open Med. 2018; 6 (PMID: 29399359; PMCID: PMC5788091)2050312117745223https://doi.org/10.1177/2050312117745223Crossref Google Scholar In a large study, 45,409 of 199,468 Korean adults developed NAFLD during 1,070,991 person-years of follow-up. In men, the multivariate-adjusted Hazard Ratio (HR) for incident NAFLD was between 1.25 [95% confidence interval (CI) 1.21–1.29] and 1.36 (955 CI 1.30–1.42), respectively for low dose and high dose exposures as compared to nonsmokers. The risk in women was higher with adjusted HR of 1.25 (95% CI 1.04–1.50), and 1.46 (95% CI 1.17–1.81), respectively for low and high smoking exposures as compared with nonsmokers.20Jung H.S. Chang Y. Kwon M.J. et al.Smoking and the risk of non-alcoholic fatty liver disease: a cohort study.Am J Gastroenterol. 2019; 114 (PMID: 30353055): 453-463https://doi.org/10.1038/s41395-018-0283-5Crossref PubMed Scopus (43) Google Scholar The largest data is from the NASH Clinical Research Network database, which enrolled 1091 patients between 2004 and 2008 in patients with biopsy-proven NASH. On bivariate analysis, associations between advanced fibrosis, age, gender, ethnicities, smoking exposure, and diabetes were noted. Smoking ≥10 pack-years was associated with advanced fibrosis (OR 1.63, P < 0.0001) on multivariate analysis. In patients with diabetes, advanced fibrosis was likely regardless of smoking, while in nondiabetics, smoking ≥10 pack-years was associated with high frequency of advanced fibrosis. Smoking is associated with increased insulin resistance and the risk of type 2 diabetes.21Zein C.O. Unalp A. Colvin R. Liu Y.C. McCullough A.J. Nonalcoholic Steatohepatitis Clinical Research NetworkSmoking and severity of hepatic fibrosis in nonalcoholic fatty liver disease.J Hepatol. 2011; 54 (Epub 2010 Sep 22. PMID: 21126792; PMCID: PMC3060962): 753-759https://doi.org/10.1016/j.jhep.2010.07.040Abstract Full Text Full Text PDF PubMed Scopus (138) Google Scholar The Thai National Health Examination assessed the follow-up of 7529 persons with NAFLD and reported 928 deaths during 64,116 person-years of follow-up. After adjusting for confounders, current smoking (adjusted HR 13.8, 95% CI –1.66 to 1.45) and smoking ≥ 10 pack years (adjusted HR 310, 95% CI 78-1296) were independently associated with death.22Charatcharoenwitthaya P. Karaketklang K. Aekplakorn W. Cigarette smoking increased risk of overall mortality in patients with non-alcoholic fatty liver disease: a nationwide population-based cohort study.Front Med (Lausanne). 2020; 7 (PMID: 33365321; PMCID: PMC7750535): 604919https://doi.org/10.3389/fmed.2020.604919Crossref PubMed Scopus (10) Google Scholar Munsterman et al reported the association of biopsy-proven NAFLD in 56 patients. The NAFLD activity score (NAS) ≥ 5 was not dependent on any prior or current smoking history or dose of smoking, but a significant correlation was noted with liver fibrosis in a dose-dependent manner.23Munsterman I.D. Smits M.M. Andriessen R. et al.Smoking is associated with severity of liver fibrosis but not with histological severity in nonalcoholic fatty liver disease. Results from a cross-sectional study.Scand J Gastroenterol. 2017; 52 (Epub 2017 Apr 27. PMID: 28446050): 881-885https://doi.org/10.1080/00365521.2017.1315169Crossref PubMed Scopus (6) Google Scholar Several studies have corroborated an association between smoking and advanced liver fibrosis (Table 1).24Hamabe A. Uto H. Imamura Y. et al.Impact of cigarette smoking on onset of nonalcoholic fatty liver disease over a 10-year period.J Gastroenterol. 2011; 46 (Epub 2011 Feb 8. PMID: 21302121): 769-778https://doi.org/10.1007/s00535-011-0376-zCrossref PubMed Scopus (89) Google Scholar, 25Liu B. Balkwill A. Roddam A. Brown A. Beral V. Million Women Study CollaboratorsSeparate and joint effects of alcohol and smoking on the risks of cirrhosis and gallbladder disease in middle-aged women.Am J Epidemiol. 2009; 169 (Epub 2008 Nov 25. PMID: 19033524): 153-160https://doi.org/10.1093/aje/kwn280Crossref PubMed Scopus (33) Google Scholar, 26Chavez-Tapia N.C. Lizardi-Cervera J. Perez-Bautista O. Ramos-Ostos M.H. Uribe M. Smoking is not associated with nonalcoholic fatty liver disease.World J Gastroenterol. 2006; 12 (PMID: 16937532; PMCID: PMC4088019): 5196-5200https://doi.org/10.3748/wjg.v12.i32.5196Crossref PubMed Google Scholar, 27Caballería L. Pera G. Auladell M.A. et al.Prevalence and factors associated with the presence of nonalcoholic fatty liver disease in an adult population in Spain.Eur J Gastroenterol Hepatol. 2010; 22 (PMID: 19730384): 24-32https://doi.org/10.1097/MEG.0b013e32832fcdf0Crossref PubMed Scopus (155) Google Scholar, 28Oniki K. Hori M. Saruwatari J. et al.Interactive effects of smoking and glutathione S-transferase polymorphisms on the development of non-alcoholic fatty liver disease.Toxicol Lett. 2013; 220 (Epub 2013 Apr 30. PMID: 23643483): 143-149https://doi.org/10.1016/j.toxlet.2013.04.019Crossref PubMed Scopus (17) Google Scholar, 29Zhang T. Zhang Y. Zhang C. et al.Prediction of metabolic syndrome by non-alcoholic fatty liver disease in northern urban Han Chinese population: a prospective cohort study.PLoS One. 2014; 9 (PMID: 24801211; PMCID: PMC4011868)e96651https://doi.org/10.1371/journal.pone.0096651Crossref PubMed Scopus (18) Google Scholar, 30Koehler E.M. Schouten J.N. Hansen B.E. et al.Prevalence and risk factors of non-alcoholic fatty liver disease in the elderly: results from the Rotterdam study.J Hepatol. 2012; 57 (Epub 2012 Aug 4. PMID: 22871499): 1305-1311https://doi.org/10.1016/j.jhep.2012.07.028Abstract Full Text Full Text PDF PubMed Scopus (158) Google Scholar, 31Chang Y. Jung H.S. Yun K.E. Cho J. Cho Y.K. Ryu S. Cohort study of non-alcoholic fatty liver disease, NAFLD fibrosis score, and the risk of incident diabetes in a Korean population.Am J Gastroenterol. 2013; 108 (Epub 2013 Oct 8. PMID: 24100261): 1861-1868https://doi.org/10.1038/ajg.2013.349Crossref PubMed Scopus (114) Google Scholar, 32Singh S.P. Singh A. Misra D. et al.Risk factors associated with non-alcoholic fatty liver disease in Indians: a case-control study.J Clin Exp Hepatol. 2015; 5 (Epub 2015 Sep 8. PMID: 26900270; PMCID: PMC4723647): 295-302https://doi.org/10.1016/j.jceh.2015.09.001Abstract Full Text Full Text PDF PubMed Scopus (28) Google Scholar, 33Otgonsuren M. Stepanova M. Gerber L. Younossi Z.M. Anthropometric and clinical factors associated with mortality in subjects with nonalcoholic fatty liver disease.Dig Dis Sci. 2013; 58 (Epub 2012 Nov 10. PMID: 23143735): 1132-1140https://doi.org/10.1007/s10620-012-2446-3Crossref PubMed Scopus (40) Google Scholar However, Yilmaz et al refuted the association, but this study had smaller numbers and comorbidities.34Yilmaz Y. Yonal O. Kurt R. Avsar E. Cigarette smoking is not associated with specific histological features or severity of nonalcoholic fatty liver disease.Hepatology. 2010; 52 (author reply 391-2) (PMID: 20578155): 391https://doi.org/10.1002/hep.23718Crossref PubMed Scopus (11) Google ScholarTable 1Studies Showing the Smoking Dose Response Risk of Advanced Fibrosis in Nonalcoholic Fatty Liver Disease [24Hamabe A. Uto H. Imamura Y. et al.Impact of cigarette smoking on onset of nonalcoholic fatty liver disease over a 10-year period.J Gastroenterol. 2011; 46 (Epub 2011 Feb 8. PMID: 21302121): 769-778https://doi.org/10.1007/s00535-011-0376-zCrossref PubMed Scopus (89) Google Scholar, 25Liu B. Balkwill A. Roddam A. Brown A. Beral V. Million Women Study CollaboratorsSeparate and joint effects of alcohol and smoking on the risks of cirrhosis and gallbladder disease in middle-aged women.Am J Epidemiol. 2009; 169 (Epub 2008 Nov 25. PMID: 19033524): 153-160https://doi.org/10.1093/aje/kwn280Crossref PubMed Scopus (33) Google Scholar, 26Chavez-Tapia N.C. Lizardi-Cervera J. Perez-Bautista O. Ramos-Ostos M.H. Uribe M. Smoking is not associated with nonalcoholic fatty liver disease.World J Gastroenterol. 2006; 12 (PMID: 16937532; PMCID: PMC4088019): 5196-5200https://doi.org/10.3748/wjg.v12.i32.5196Crossref PubMed Google Scholar, 27Caballería L. Pera G. Auladell M.A. et al.Prevalence and factors associated with the presence of nonalcoholic fatty liver disease in an adult population in Spain.Eur J Gastroenterol Hepatol. 2010; 22 (PMID: 19730384): 24-32https://doi.org/10.1097/MEG.0b013e32832fcdf0Crossref PubMed Scopus (155) Google Scholar, 28Oniki K. Hori M. Saruwatari J. et al.Interactive effects of smoking and glutathione S-transferase polymorphisms on the development of non-alcoholic fatty liver disease.Toxicol Lett. 2013; 220 (Epub 2013 Apr 30. PMID: 23643483): 143-149https://doi.org/10.1016/j.toxlet.2013.04.019Crossref PubMed Scopus (17) Google Scholar, 29Zhang T. Zhang Y. Zhang C. et al.Prediction of metabolic syndrome by non-alcoholic fatty liver disease in northern urban Han Chinese population: a prospective cohort study.PLoS One. 2014; 9 (PMID: 24801211; PMCID: PMC4011868)e96651https://doi.org/10.1371/journal.pone.0096651Crossref PubMed Scopus (18) Google Scholar, 30Koehler E.M. Schouten J.N. Hansen B.E. et al.Prevalence and risk factors of non-alcoholic fatty liver disease in the elderly: results from the Rotterdam study.J Hepatol. 2012; 57 (Epub 2012 Aug 4. PMID: 22871499): 1305-1311https://doi.org/10.1016/j.jhep.2012.07.028Abstract Full Text Full Text PDF PubMed Scopus (158) Google Scholar, 31Chang Y. Jung H.S. Yun K.E. Cho J. Cho Y.K. Ryu S. Cohort study of non-alcoholic fatty liver disease, NAFLD fibrosis score, and the risk of incident diabetes in a Korean population.Am J Gastroenterol. 2013; 108 (Epub 2013 Oct 8. PMID: 24100261): 1861-1868https://doi.org/10.1038/ajg.2013.349Crossref PubMed Scopus (114) Google Scholar, 32Singh S.P. Singh A. Misra D. et al.Risk factors associated with non-alcoholic fatty liver disease in Indians: a case-control study.J Clin Exp Hepatol. 2015; 5 (Epub 2015 Sep 8. PMID: 26900270; PMCID: PMC4723647): 295-302https://doi.org/10.1016/j.jceh.2015.09.001Abstract Full Text Full Text PDF PubMed Scopus (28) Google Scholar, 33Otgonsuren M. Stepanova M. Gerber L. Younossi Z.M. Anthropometric and clinical factors associated with mortality in subjects with nonalcoholic fatty liver disease.Dig Dis Sci. 2013; 58 (Epub 2012 Nov 10. PMID: 23143735): 1132-1140https://doi.org/10.1007/s10620-012-2446-3Crossref PubMed Scopus (40) Google Scholar].Author, YearCountrySmoking DoseNStudy DesignNAFLDN (%)Non-NAFLDN (%)OR (95% Confidence interval)Hamabe et al, 201124Hamabe A. Uto H. Imamura Y. et al.Impact of cigarette smoking on onset of nonalcoholic fatty liver disease over a 10-year period.J Gastroenterol. 2011; 46 (Epub 2011 Feb 8. PMID: 21302121): 769-778https://doi.org/10.1007/s00535-011-0376-zCrossref PubMed Scopus (89) Google ScholarJapan1553Retrospective cohortAll smokers93 (5.99)216 (13.90)2.9 (2.0–3.6)Light24 (1.55)57 (3.67)0.9 (0.6–1.5)Heavy69 (4.44)159 (10.24)2.7 (2–3.7)Nonsmoker172 (11.1)1072 (69)Liu et al, 201325Liu B. Balkwill A. Roddam A. Brown A. Beral V. Million Women Study CollaboratorsSeparate and joint effects of alcohol and smoking on the risks of cirrhosis and gallbladder disease in middle-aged women.Am J Epidemiol. 2009; 169 (Epub 2008 Nov 25. 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Auladell M.A. et al.Prevalence and factors associated with the presence of nonalcoholic fatty liver disease in an adult population in Spain.Eur J Gastroenterol Hepatol. 2010; 22 (PMID: 19730384): 24-32https://doi.org/10.1097/MEG.0b013e32832fcdf0Crossref PubMed Scopus (155) Google ScholarSpain766Cross sectionalTotal smokers92 (12.0)250 (32.6)0.1 (0.8–1.5)Current smokers39 (5.0)150 (19.5)0.7 (0.4–0.9)Former smokers53 (6.9)100 (13.0)1.6 (0.8–1.8)Nonsmokers106 (13.8)318 (41.5)Oniki et al, 201328Oniki K. Hori M. Saruwatari J. et al.Interactive effects of smoking and glutathione S-transferase polymorphisms on the development of non-alcoholic fatty liver disease.Toxicol Lett. 2013; 220 (Epub 2013 Apr 30. 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