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Published in: BMC Gastroenterology 1/2020

Open Access 01-12-2020 | Obesity | Research article

Combined effects of lifestyle risk factors on fatty liver index

Authors: Ulla Nivukoski, Markus Niemelä, Aini Bloigu, Risto Bloigu, Mauri Aalto, Tiina Laatikainen, Onni Niemelä

Published in: BMC Gastroenterology | Issue 1/2020

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Abstract

Background

Factors of lifestyle may have a major impact on liver-related morbidity and mortality.
We examined independent and joint effects of lifestyle risk factors on fatty liver index (FLI), a biomarker of hepatic steatosis, in a population-based cross-sectional national health survey.

Methods

The study included 12,368 participants (5784 men, 6584 women) aged 25–74 years. Quantitative estimates of alcohol use, smoking, adiposity and physical activity were used to establish a total score of risk factors, with higher scores indicating an unhealthier lifestyle. FLI was calculated based on an algorithm including body mass index, waist circumference, serum gamma-glutamyltransferase and triglycerides.

Results

The occurrence of FLI ≥ 60% indicating fatty liver increased from 2.4% in men with zero risk factors to 81.9% in those with a total risk score of 7–8 (p <  0.0005 for linear trend) and in women from 0 to 73.5% (p <  0.0005). The most striking individual impacts on the likelihood for FLI above 60% were observed for physical inactivity (p <  0.0005 for both genders) and alcohol consumption (p <  0.0005 for men). Interestingly, coffee consumption was also found to increase with increasing risk factor scores (p <  0.0005 for linear trend in both genders).

Conclusions

The data indicates that unfavorable combinations of lifestyle risk factors lead to a high likelihood of hepatic steatosis. Use of FLI as a diagnostic tool may benefit the assessment of interventions aimed at maintaining a healthy lifestyle and prevention of liver-related morbidity.
Literature
1.
go back to reference Li Y, Pan A, Wang DD, Liu X, Dhana K, Franco OH, et al. Impact of healthy lifestyle factors on life expectancies in the US population. Circulation. 2018;138:345–55.PubMedPubMedCentralCrossRef Li Y, Pan A, Wang DD, Liu X, Dhana K, Franco OH, et al. Impact of healthy lifestyle factors on life expectancies in the US population. Circulation. 2018;138:345–55.PubMedPubMedCentralCrossRef
2.
go back to reference Lim SS, Vos T, Flaxman AD, Danaei G, Shibuya K, Adair-Rohani H, et al. A comparative risk assessment of burden of disease and injury attributable to 67 risk factors and risk factor clusters in 21 regions, 1990-2010: a systematic analysis for the global burden of disease study 2010. Lancet. 2012;380:2224–60.PubMedPubMedCentralCrossRef Lim SS, Vos T, Flaxman AD, Danaei G, Shibuya K, Adair-Rohani H, et al. A comparative risk assessment of burden of disease and injury attributable to 67 risk factors and risk factor clusters in 21 regions, 1990-2010: a systematic analysis for the global burden of disease study 2010. Lancet. 2012;380:2224–60.PubMedPubMedCentralCrossRef
3.
go back to reference Manuel DG, Perez R, Sanmartin C, Taljaard M, Hennessy D, Wilson K, et al. Measuring burden of unhealthy behaviours using a multivariable predictive approach: life expectancy lost in Canada attributable to smoking, alcohol, physical inactivity, and diet. PLoS Med. 2016;13:e1002082.PubMedPubMedCentralCrossRef Manuel DG, Perez R, Sanmartin C, Taljaard M, Hennessy D, Wilson K, et al. Measuring burden of unhealthy behaviours using a multivariable predictive approach: life expectancy lost in Canada attributable to smoking, alcohol, physical inactivity, and diet. PLoS Med. 2016;13:e1002082.PubMedPubMedCentralCrossRef
4.
go back to reference Rutten-Jacobs LC, Larsson SC, Malik R, Rannikmae K, Sudlow CL, Dichgans M, et al. Genetic risk, incident stroke, and the benefits of adhering to a healthy lifestyle: cohort study of 306 473 UK biobank participants. BMJ. 2018;363:k4168.PubMedPubMedCentralCrossRef Rutten-Jacobs LC, Larsson SC, Malik R, Rannikmae K, Sudlow CL, Dichgans M, et al. Genetic risk, incident stroke, and the benefits of adhering to a healthy lifestyle: cohort study of 306 473 UK biobank participants. BMJ. 2018;363:k4168.PubMedPubMedCentralCrossRef
5.
go back to reference McGinnis M, Williams-Russo P, Knickman JR. The case for more active policy attention to health promotion. Health Aff. 2002;21:78–93.CrossRef McGinnis M, Williams-Russo P, Knickman JR. The case for more active policy attention to health promotion. Health Aff. 2002;21:78–93.CrossRef
6.
go back to reference Niemelä O, Niemelä M, Bloigu R, Aalto M, Laatikainen T. Where should the safe limits of alcohol consumption stand in light of liver enzyme abnormalities in alcohol consumers? PLoS One. 2017;12:e0188574.PubMedPubMedCentralCrossRef Niemelä O, Niemelä M, Bloigu R, Aalto M, Laatikainen T. Where should the safe limits of alcohol consumption stand in light of liver enzyme abnormalities in alcohol consumers? PLoS One. 2017;12:e0188574.PubMedPubMedCentralCrossRef
7.
go back to reference Tamakoshi A, Tamakoshi K, Lin Y, Yagyu K, Kikuchi S, JACC Study Group. Healthy lifestyle and preventable death: findings from the Japan collaborative cohort (JACC) study. Prev Med. 2009;48:486–92.PubMedCrossRef Tamakoshi A, Tamakoshi K, Lin Y, Yagyu K, Kikuchi S, JACC Study Group. Healthy lifestyle and preventable death: findings from the Japan collaborative cohort (JACC) study. Prev Med. 2009;48:486–92.PubMedCrossRef
8.
go back to reference Teeriniemi AM, Salonurmi T, Jokelainen T, Vähänikkilä H, Alahäivälä T, Karppinen P, et al. A randomized clinical trial of the effectiveness of a web-based health behaviour change support system and group lifestyle counselling on body weight loss in overweight and obese subjects: 2-year outcomes. J Intern Med. 2018;284:534–45.PubMedCrossRef Teeriniemi AM, Salonurmi T, Jokelainen T, Vähänikkilä H, Alahäivälä T, Karppinen P, et al. A randomized clinical trial of the effectiveness of a web-based health behaviour change support system and group lifestyle counselling on body weight loss in overweight and obese subjects: 2-year outcomes. J Intern Med. 2018;284:534–45.PubMedCrossRef
9.
go back to reference Danielsson J, Kangastupa P, Laatikainen T, Aalto M, Niemelä O. Impacts of common factors of life style on serum liver enzymes. World J Gastroenterol. 2014;20:11743–52.PubMedPubMedCentralCrossRef Danielsson J, Kangastupa P, Laatikainen T, Aalto M, Niemelä O. Impacts of common factors of life style on serum liver enzymes. World J Gastroenterol. 2014;20:11743–52.PubMedPubMedCentralCrossRef
10.
go back to reference Kim WR, Flamm SL, Di Bisceglie AM, Bodenheimer HC. Serum activity of alanine aminotransferase (ALT) as an indicator of health and disease. Hepatology. 2008;47:1363–70.PubMedCrossRef Kim WR, Flamm SL, Di Bisceglie AM, Bodenheimer HC. Serum activity of alanine aminotransferase (ALT) as an indicator of health and disease. Hepatology. 2008;47:1363–70.PubMedCrossRef
11.
go back to reference Koehler EM, Schouten JN, Hansen BE, Hofman A, Stricker BH, Janssen HL. External validation of the fatty liver index for identifying nonalcoholic fatty liver disease in a population-based study. Clin Gastroenterol Hepatol. 2013;11:1201–4.PubMedCrossRef Koehler EM, Schouten JN, Hansen BE, Hofman A, Stricker BH, Janssen HL. External validation of the fatty liver index for identifying nonalcoholic fatty liver disease in a population-based study. Clin Gastroenterol Hepatol. 2013;11:1201–4.PubMedCrossRef
12.
go back to reference Lau K, Baumeister SE, Lieb W, Meffert PJ, Lerch MM, Mayerle J, et al. The combined effects of alcohol consumption and body mass index on hepatic steatosis in a general population sample of European men and women. Aliment Pharmacol Ther. 2015;41:467–76.PubMedCrossRef Lau K, Baumeister SE, Lieb W, Meffert PJ, Lerch MM, Mayerle J, et al. The combined effects of alcohol consumption and body mass index on hepatic steatosis in a general population sample of European men and women. Aliment Pharmacol Ther. 2015;41:467–76.PubMedCrossRef
13.
go back to reference Nivukoski U, Niemelä M, Bloigu A, Bloigu R, Aalto M, Laatikainen T, et al. Impacts of unfavourable lifestyle factors on biomarkers of liver function, inflammation and lipid status. PLoS One. 2019;14:e0218463.PubMedPubMedCentralCrossRef Nivukoski U, Niemelä M, Bloigu A, Bloigu R, Aalto M, Laatikainen T, et al. Impacts of unfavourable lifestyle factors on biomarkers of liver function, inflammation and lipid status. PLoS One. 2019;14:e0218463.PubMedPubMedCentralCrossRef
14.
go back to reference Ruhl CE, Everhart JE. Elevated serum alanine aminotransferase and gamma-glutamyltransferase and mortality in the United States population. Gastroenterology. 2009;136:477–85.PubMedCrossRef Ruhl CE, Everhart JE. Elevated serum alanine aminotransferase and gamma-glutamyltransferase and mortality in the United States population. Gastroenterology. 2009;136:477–85.PubMedCrossRef
15.
go back to reference Breitling LP, Raum E, Müller H, Rothenbacher D, Brenner H. Synergism between smoking and alcohol consumption with respect to serum gamma-glutamyltransferase. Hepatology. 2009;49:802–8.PubMedCrossRef Breitling LP, Raum E, Müller H, Rothenbacher D, Brenner H. Synergism between smoking and alcohol consumption with respect to serum gamma-glutamyltransferase. Hepatology. 2009;49:802–8.PubMedCrossRef
16.
go back to reference Park EY, Lim MK, Oh JK, Cho H, Bae MJ, Yun EH, et al. Independent and supra-additive effects of alcohol consumption, cigarette smoking, and metabolic syndrome on the elevation of serum liver enzyme levels. PLoS One. 2013;8:e63439.PubMedPubMedCentralCrossRef Park EY, Lim MK, Oh JK, Cho H, Bae MJ, Yun EH, et al. Independent and supra-additive effects of alcohol consumption, cigarette smoking, and metabolic syndrome on the elevation of serum liver enzyme levels. PLoS One. 2013;8:e63439.PubMedPubMedCentralCrossRef
17.
go back to reference Lee TH, Kim WR, Benson JT, Therneau TM, Melton LJ III. Serum aminotransferase activity and mortality risk in a United States community. Hepatology. 2008;47:880–7.PubMedCrossRef Lee TH, Kim WR, Benson JT, Therneau TM, Melton LJ III. Serum aminotransferase activity and mortality risk in a United States community. Hepatology. 2008;47:880–7.PubMedCrossRef
18.
go back to reference Niemelä O, Nivukoski U, Bloigu A, Bloigu R, Aalto M, Laatikainen T. Laboratory test based assessment of WHO alcohol risk drinking levels. Scand J Clin Lab Invest. 2019;79:58–64.PubMedCrossRef Niemelä O, Nivukoski U, Bloigu A, Bloigu R, Aalto M, Laatikainen T. Laboratory test based assessment of WHO alcohol risk drinking levels. Scand J Clin Lab Invest. 2019;79:58–64.PubMedCrossRef
19.
go back to reference Ruttmann E, Brant LJ, Concin H, Diem G, Rapp K, Ulmer H, et al. Gamma-glutamyltransferase as a risk factor for cardiovascular disease mortality: an epidemiological investigation in a cohort of 163,944 Austrian adults. Circulation. 2005;112:2130–7.PubMedCrossRef Ruttmann E, Brant LJ, Concin H, Diem G, Rapp K, Ulmer H, et al. Gamma-glutamyltransferase as a risk factor for cardiovascular disease mortality: an epidemiological investigation in a cohort of 163,944 Austrian adults. Circulation. 2005;112:2130–7.PubMedCrossRef
20.
go back to reference Bedogni G, Bellentani S, Miglioli L, Masutti F, Passalacqua M, Castiglione A, et al. The fatty liver index: a simple and accurate predictor of hepatic steatosis in the general population. BMC Gastroenterol. 2006;6:33.PubMedPubMedCentralCrossRef Bedogni G, Bellentani S, Miglioli L, Masutti F, Passalacqua M, Castiglione A, et al. The fatty liver index: a simple and accurate predictor of hepatic steatosis in the general population. BMC Gastroenterol. 2006;6:33.PubMedPubMedCentralCrossRef
21.
go back to reference The World Health Organization MONICA Project (Monitoring trends and determinants in cardiovascular disease): a major international collaboration. WHO MONICA Project Principal Investigators. J Clin Epidemiol. 1988;41:105–14.CrossRef The World Health Organization MONICA Project (Monitoring trends and determinants in cardiovascular disease): a major international collaboration. WHO MONICA Project Principal Investigators. J Clin Epidemiol. 1988;41:105–14.CrossRef
22.
go back to reference Kuulasmaa K, Tolonen H, Cepaitis Z, Laatikainen T, Nissinen A, Vartiainen E, et al. European health risk monitoring project. Helsinki: Finnish National Public Health Institute (KTL); 2006. www.thl.fi/ehrm (11.9.2018). Kuulasmaa K, Tolonen H, Cepaitis Z, Laatikainen T, Nissinen A, Vartiainen E, et al. European health risk monitoring project. Helsinki: Finnish National Public Health Institute (KTL); 2006. www.​thl.​fi/​ehrm (11.9.2018).
23.
go back to reference Byrne CD, Patel J, Scorletti E, Targher G. Tests for diagnosing and monitoring non-alcoholic fatty liver disease in adults. BMJ. 2018;362:k2734.PubMedCrossRef Byrne CD, Patel J, Scorletti E, Targher G. Tests for diagnosing and monitoring non-alcoholic fatty liver disease in adults. BMJ. 2018;362:k2734.PubMedCrossRef
24.
go back to reference Iqbal U, Perumpail BJ, Akhtar D, Kim D, Ahmed A. The epidemiology, risk profiling and diagnostic challenges of nonalcoholic fatty liver disease. Medicines (Basel). 2019;6(1):41. Iqbal U, Perumpail BJ, Akhtar D, Kim D, Ahmed A. The epidemiology, risk profiling and diagnostic challenges of nonalcoholic fatty liver disease. Medicines (Basel). 2019;6(1):41.
25.
go back to reference Younossi Z, Anstee QM, Marietti M, Hardy T, Henry L, Eslam M, et al. Global burden of NAFLD and NASH: trends, predictions, risk factors and prevention. Nat Rev Gastroenterol Hepatol. 2018;15:11–20.PubMedCrossRef Younossi Z, Anstee QM, Marietti M, Hardy T, Henry L, Eslam M, et al. Global burden of NAFLD and NASH: trends, predictions, risk factors and prevention. Nat Rev Gastroenterol Hepatol. 2018;15:11–20.PubMedCrossRef
26.
go back to reference Kazemi-Shirazi L, Endler G, Winkler S, Schickbauer T, Wagner O, Marsik C. Gamma glutamyltransferase and long-term survival: is it just the liver? Clin Chem. 2007;53:940–6.PubMedCrossRef Kazemi-Shirazi L, Endler G, Winkler S, Schickbauer T, Wagner O, Marsik C. Gamma glutamyltransferase and long-term survival: is it just the liver? Clin Chem. 2007;53:940–6.PubMedCrossRef
28.
go back to reference Yki-Järvinen H. Non-alcoholic fatty liver disease as a cause and a consequence of metabolic syndrome. Lancet Diabetes Endocrinol. 2014;2:901–10.PubMedCrossRef Yki-Järvinen H. Non-alcoholic fatty liver disease as a cause and a consequence of metabolic syndrome. Lancet Diabetes Endocrinol. 2014;2:901–10.PubMedCrossRef
29.
go back to reference Huang X, Xu M, Chen Y, Peng K, Huang Y, Wang P, et al. Validation of the Fatty Liver Index for Nonalcoholic Fatty Liver Disease in Middle-Aged and Elderly Chinese. Medicine (Baltimore). 2015;94:e1682.CrossRef Huang X, Xu M, Chen Y, Peng K, Huang Y, Wang P, et al. Validation of the Fatty Liver Index for Nonalcoholic Fatty Liver Disease in Middle-Aged and Elderly Chinese. Medicine (Baltimore). 2015;94:e1682.CrossRef
30.
go back to reference Jäger S, Jacobs S, Kröger J, Stefan N, Fritsche A, Weikert C, et al. Association between the fatty liver index and risk of type 2 diabetes in the EPIC-Potsdam study. PLoS One. 2015;10:e0124749.PubMedPubMedCentralCrossRef Jäger S, Jacobs S, Kröger J, Stefan N, Fritsche A, Weikert C, et al. Association between the fatty liver index and risk of type 2 diabetes in the EPIC-Potsdam study. PLoS One. 2015;10:e0124749.PubMedPubMedCentralCrossRef
31.
go back to reference Ruhl CE, Everhart JE. Fatty liver indices in the multiethnic United States National Health and nutrition examination survey. Aliment Pharmacol Ther. 2015;41:65–76.PubMedCrossRef Ruhl CE, Everhart JE. Fatty liver indices in the multiethnic United States National Health and nutrition examination survey. Aliment Pharmacol Ther. 2015;41:65–76.PubMedCrossRef
32.
go back to reference Wood AM, Kaptoge S, Butterworth AS, Willeit P, Warnakula S, Bolton T, et al. Risk thresholds for alcohol consumption: combined analysis of individual-participant data for 599 912 current drinkers in 83 prospective studies. Lancet. 2018;391:1513–23.PubMedPubMedCentralCrossRef Wood AM, Kaptoge S, Butterworth AS, Willeit P, Warnakula S, Bolton T, et al. Risk thresholds for alcohol consumption: combined analysis of individual-participant data for 599 912 current drinkers in 83 prospective studies. Lancet. 2018;391:1513–23.PubMedPubMedCentralCrossRef
33.
34.
go back to reference Abul-Husn NS, Cheng X, Li AH, Xin Y, Schurmann C, Stevis P, et al. A protein-truncating HSD17B13 variant and protection from chronic liver disease. N Engl J Med. 2018;378:1096–106.PubMedPubMedCentralCrossRef Abul-Husn NS, Cheng X, Li AH, Xin Y, Schurmann C, Stevis P, et al. A protein-truncating HSD17B13 variant and protection from chronic liver disease. N Engl J Med. 2018;378:1096–106.PubMedPubMedCentralCrossRef
35.
go back to reference Oh S, Shida T, Yamagishi K, Tanaka K, So R, Tsujimoto T, et al. Moderate to vigorous physical activity volume is an important factor for managing nonalcoholic fatty liver disease: a retrospective study. Hepatology. 2015;61:1205–15.PubMedCrossRef Oh S, Shida T, Yamagishi K, Tanaka K, So R, Tsujimoto T, et al. Moderate to vigorous physical activity volume is an important factor for managing nonalcoholic fatty liver disease: a retrospective study. Hepatology. 2015;61:1205–15.PubMedCrossRef
36.
go back to reference Soldavini J, Kaunitz JD. Pathobiology and potential therapeutic value of intestinal short-chain fatty acids in gut inflammation and obesity. Dig Dis Sci. 2013;58:2756–66.PubMedPubMedCentralCrossRef Soldavini J, Kaunitz JD. Pathobiology and potential therapeutic value of intestinal short-chain fatty acids in gut inflammation and obesity. Dig Dis Sci. 2013;58:2756–66.PubMedPubMedCentralCrossRef
37.
go back to reference Kozakova M, Palombo C, Eng MP, Dekker J, Flyvbjerg A, Mitrakou A, et al. Fatty liver index, gamma-glutamyltransferase, and early carotid plaques. Hepatology. 2012;55:1406–15.PubMedCrossRef Kozakova M, Palombo C, Eng MP, Dekker J, Flyvbjerg A, Mitrakou A, et al. Fatty liver index, gamma-glutamyltransferase, and early carotid plaques. Hepatology. 2012;55:1406–15.PubMedCrossRef
38.
go back to reference Pais R, Giral P, Khan JF, Rosenbaum D, Housset C, Poynard T, et al. Fatty liver is an independent predictor of early carotid atherosclerosis. J Hepatol. 2016;65:95–102.PubMedCrossRef Pais R, Giral P, Khan JF, Rosenbaum D, Housset C, Poynard T, et al. Fatty liver is an independent predictor of early carotid atherosclerosis. J Hepatol. 2016;65:95–102.PubMedCrossRef
39.
go back to reference Koenig W. C-reactive protein and cardiovascular risk: will the controversy end after CANTOS? Clin Chem. 2017;63:1897–8.PubMedCrossRef Koenig W. C-reactive protein and cardiovascular risk: will the controversy end after CANTOS? Clin Chem. 2017;63:1897–8.PubMedCrossRef
40.
go back to reference Libby P, Ridker PM, Hansson GK. Leducq transatlantic network on Atherothrombosis. Inflammation in atherosclerosis: from pathophysiology to practice. J Am Coll Cardiol. 2009;54:2129–38.PubMedPubMedCentralCrossRef Libby P, Ridker PM, Hansson GK. Leducq transatlantic network on Atherothrombosis. Inflammation in atherosclerosis: from pathophysiology to practice. J Am Coll Cardiol. 2009;54:2129–38.PubMedPubMedCentralCrossRef
41.
go back to reference Moradi H, Streja E, Kalantar-Zadeh K. Serum high density lipoprotein cholesterol level and risk of death: let's avoid the extremes. J Thorac Dis. 2017;9:4849–52.PubMedPubMedCentralCrossRef Moradi H, Streja E, Kalantar-Zadeh K. Serum high density lipoprotein cholesterol level and risk of death: let's avoid the extremes. J Thorac Dis. 2017;9:4849–52.PubMedPubMedCentralCrossRef
42.
go back to reference Sundberg CJ. Physical activity: what is already being done and how we can avert 1 million deaths annually in future. Br J Sports Med. 2016;50:319.PubMedCrossRef Sundberg CJ. Physical activity: what is already being done and how we can avert 1 million deaths annually in future. Br J Sports Med. 2016;50:319.PubMedCrossRef
43.
go back to reference Warburton DE, Bredin SS. Reflections on physical activity and health: what should we recommend? Can J Cardiol. 2016;32:495–504.PubMedCrossRef Warburton DE, Bredin SS. Reflections on physical activity and health: what should we recommend? Can J Cardiol. 2016;32:495–504.PubMedCrossRef
44.
go back to reference Chomistek AK, Manson JE, Stefanick ML, Lu B, Sands-Lincoln M, Going SB, et al. Relationship of sedentary behavior and physical activity to incident cardiovascular disease: results from the Women's Health Initiative. J Am Coll Cardiol. 2013;61:2346–54.PubMedPubMedCentralCrossRef Chomistek AK, Manson JE, Stefanick ML, Lu B, Sands-Lincoln M, Going SB, et al. Relationship of sedentary behavior and physical activity to incident cardiovascular disease: results from the Women's Health Initiative. J Am Coll Cardiol. 2013;61:2346–54.PubMedPubMedCentralCrossRef
45.
go back to reference Kyu HH, Bachman VF, Alexander LT, Mumford JE, Afshin A, Estep K, et al. Physical activity and risk of breast cancer, colon cancer, diabetes, ischemic heart disease, and ischemic stroke events: systematic review and dose-response meta-analysis for the global burden of disease study 2013. BMJ. 2016;354:i3857.PubMedPubMedCentralCrossRef Kyu HH, Bachman VF, Alexander LT, Mumford JE, Afshin A, Estep K, et al. Physical activity and risk of breast cancer, colon cancer, diabetes, ischemic heart disease, and ischemic stroke events: systematic review and dose-response meta-analysis for the global burden of disease study 2013. BMJ. 2016;354:i3857.PubMedPubMedCentralCrossRef
46.
go back to reference Romero-Gómez M, Zelber-Sagi S, Trenell M. Treatment of NAFLD with diet, physical activity and exercise. J Hepatol. 2017;67:829–46.PubMedCrossRef Romero-Gómez M, Zelber-Sagi S, Trenell M. Treatment of NAFLD with diet, physical activity and exercise. J Hepatol. 2017;67:829–46.PubMedCrossRef
47.
go back to reference Smith AD, Crippa A, Woodcock J, Brage S. Physical activity and incident type 2 diabetes mellitus: a systematic review and dose-response meta-analysis of prospective cohort studies. Diabetologia. 2016;59:2527–45.PubMedPubMedCentralCrossRef Smith AD, Crippa A, Woodcock J, Brage S. Physical activity and incident type 2 diabetes mellitus: a systematic review and dose-response meta-analysis of prospective cohort studies. Diabetologia. 2016;59:2527–45.PubMedPubMedCentralCrossRef
48.
go back to reference Lawlor DA, Sattar N, Smith GD, Ebrahim S. The associations of physical activity and adiposity with alanine aminotransferase and gamma-glutamyltransferase. Am J Epidemiol. 2005;161:1081–8.PubMedCrossRef Lawlor DA, Sattar N, Smith GD, Ebrahim S. The associations of physical activity and adiposity with alanine aminotransferase and gamma-glutamyltransferase. Am J Epidemiol. 2005;161:1081–8.PubMedCrossRef
49.
go back to reference St George A, Bauman A, Johnston A, Farrell G, Chey T, George J. Independent effects of physical activity in patients with nonalcoholic fatty liver disease. Hepatology. 2009;50:68–76.PubMedCrossRef St George A, Bauman A, Johnston A, Farrell G, Chey T, George J. Independent effects of physical activity in patients with nonalcoholic fatty liver disease. Hepatology. 2009;50:68–76.PubMedCrossRef
51.
go back to reference Berná G, Romero-Gómez M. The role of nutrition in non-alcoholic fatty liver disease: pathophysiology and management. Liver Int. 2020;40(Suppl 1):102–8.PubMedCrossRef Berná G, Romero-Gómez M. The role of nutrition in non-alcoholic fatty liver disease: pathophysiology and management. Liver Int. 2020;40(Suppl 1):102–8.PubMedCrossRef
52.
go back to reference Abenavoli L, Boccuto L, Federico A, Dallio M, Loguercio C, Di Renzo L, et al. Diet and non-alcoholic fatty liver disease: the Mediterranean way. Int J Environ Res Public Health. 2019;16:3011.PubMedCentralCrossRef Abenavoli L, Boccuto L, Federico A, Dallio M, Loguercio C, Di Renzo L, et al. Diet and non-alcoholic fatty liver disease: the Mediterranean way. Int J Environ Res Public Health. 2019;16:3011.PubMedCentralCrossRef
53.
go back to reference Ghouri N, Preiss D, Sattar N. Liver enzymes, nonalcoholic fatty liver disease, and incident cardiovascular disease: a narrative review and clinical perspective of prospective data. Hepatology. 2010;52:1156–61.PubMedCrossRef Ghouri N, Preiss D, Sattar N. Liver enzymes, nonalcoholic fatty liver disease, and incident cardiovascular disease: a narrative review and clinical perspective of prospective data. Hepatology. 2010;52:1156–61.PubMedCrossRef
54.
go back to reference Liu B, Balkwill A, Reeves G, Beral V. Million women study collaborators. Body mass index and risk of liver cirrhosis in middle aged UK women: prospective study. BMJ. 2010;340:c912.PubMedPubMedCentralCrossRef Liu B, Balkwill A, Reeves G, Beral V. Million women study collaborators. Body mass index and risk of liver cirrhosis in middle aged UK women: prospective study. BMJ. 2010;340:c912.PubMedPubMedCentralCrossRef
55.
go back to reference Abenavoli L, Milic N, Di Renzo L, Preveden T, Medic-Stojanoska M, De Lorenzo A. Metabolic aspects of adult patients with nonalcoholic fatty liver disease. World J Gastroenterol. 2016;22(31):7006–16.PubMedPubMedCentralCrossRef Abenavoli L, Milic N, Di Renzo L, Preveden T, Medic-Stojanoska M, De Lorenzo A. Metabolic aspects of adult patients with nonalcoholic fatty liver disease. World J Gastroenterol. 2016;22(31):7006–16.PubMedPubMedCentralCrossRef
56.
go back to reference Tsukamoto H, Horne W, Kamimura S, Niemelä O, Parkkila S, Ylä-Herttuala S, et al. Experimental liver cirrhosis induced by alcohol and iron. J Clin Invest. 1995;96:620–30.PubMedPubMedCentralCrossRef Tsukamoto H, Horne W, Kamimura S, Niemelä O, Parkkila S, Ylä-Herttuala S, et al. Experimental liver cirrhosis induced by alcohol and iron. J Clin Invest. 1995;96:620–30.PubMedPubMedCentralCrossRef
57.
go back to reference Kanerva N, Kaartinen NE, Schwab U, Lahti-Koski M, Männistö S. Adherence to the Baltic Sea diet consumed in the Nordic countries is associated with lower abdominal obesity. Br J Nutr. 2013;109:520–8.PubMedCrossRef Kanerva N, Kaartinen NE, Schwab U, Lahti-Koski M, Männistö S. Adherence to the Baltic Sea diet consumed in the Nordic countries is associated with lower abdominal obesity. Br J Nutr. 2013;109:520–8.PubMedCrossRef
58.
go back to reference Danielsson J, Kangastupa P, Laatikainen T, Aalto M, Niemelä O. Dose- and gender-dependent interactions between coffee consumption and serum GGT activity in alcohol consumers. Alcohol Alcohol. 2013;48:303–7.PubMedCrossRef Danielsson J, Kangastupa P, Laatikainen T, Aalto M, Niemelä O. Dose- and gender-dependent interactions between coffee consumption and serum GGT activity in alcohol consumers. Alcohol Alcohol. 2013;48:303–7.PubMedCrossRef
59.
go back to reference Gunter MJ, Murphy N, Cross AJ, Dossus L, Dartois L, Fagherazzi G, et al. Coffee drinking and mortality in 10 European countries: a multinational cohort study. Ann Intern Med. 2017;167:236–47.PubMedPubMedCentralCrossRef Gunter MJ, Murphy N, Cross AJ, Dossus L, Dartois L, Fagherazzi G, et al. Coffee drinking and mortality in 10 European countries: a multinational cohort study. Ann Intern Med. 2017;167:236–47.PubMedPubMedCentralCrossRef
60.
go back to reference Vitaglione P, Mazzone G, Lembo V, D'Argenio G, Rossi A, Guido M, et al. Coffee prevents fatty liver disease induced by a high-fat diet by modulating pathways of the gut-liver axis. J Nutr Sci. 2019;8:e15.PubMedPubMedCentralCrossRef Vitaglione P, Mazzone G, Lembo V, D'Argenio G, Rossi A, Guido M, et al. Coffee prevents fatty liver disease induced by a high-fat diet by modulating pathways of the gut-liver axis. J Nutr Sci. 2019;8:e15.PubMedPubMedCentralCrossRef
61.
go back to reference Bjørngaard JH, Nordestgaard AT, Taylor AE, Treur JL, Gabrielsen ME, Munafò MR, et al. Heavier smoking increases coffee consumption: findings from a Mendelian randomization analysis. Int J Epidemiol. 2017;46:1958–67.PubMedPubMedCentralCrossRef Bjørngaard JH, Nordestgaard AT, Taylor AE, Treur JL, Gabrielsen ME, Munafò MR, et al. Heavier smoking increases coffee consumption: findings from a Mendelian randomization analysis. Int J Epidemiol. 2017;46:1958–67.PubMedPubMedCentralCrossRef
62.
go back to reference Marin V, Rosso N, Dal Pen M, Raseni A, Boschelle M, Degrassi C, et al. An animal model for the juvenile non-alcoholic fatty liver disease and non-alcoholic steatohepatitis. PLoS One. 2016;11(7):e0158817.PubMedPubMedCentralCrossRef Marin V, Rosso N, Dal Pen M, Raseni A, Boschelle M, Degrassi C, et al. An animal model for the juvenile non-alcoholic fatty liver disease and non-alcoholic steatohepatitis. PLoS One. 2016;11(7):e0158817.PubMedPubMedCentralCrossRef
63.
go back to reference Stefan S, Schick F, Häring H-U. Causes, characteristics, and consequences of metabolically unhealthy normal weight in humans. Cell Metab. 2017;26:292–300.PubMedCrossRef Stefan S, Schick F, Häring H-U. Causes, characteristics, and consequences of metabolically unhealthy normal weight in humans. Cell Metab. 2017;26:292–300.PubMedCrossRef
64.
go back to reference Huh JH, Kim JY, Choi E, Kim JS, Chang Y, Sung KC. The fatty liver index as a predictor of incident chronic kidney disease in a 10-year prospective cohort study. PLoS One. 2017;12(7):e0180951.PubMedPubMedCentralCrossRef Huh JH, Kim JY, Choi E, Kim JS, Chang Y, Sung KC. The fatty liver index as a predictor of incident chronic kidney disease in a 10-year prospective cohort study. PLoS One. 2017;12(7):e0180951.PubMedPubMedCentralCrossRef
Metadata
Title
Combined effects of lifestyle risk factors on fatty liver index
Authors
Ulla Nivukoski
Markus Niemelä
Aini Bloigu
Risto Bloigu
Mauri Aalto
Tiina Laatikainen
Onni Niemelä
Publication date
01-12-2020
Publisher
BioMed Central
Published in
BMC Gastroenterology / Issue 1/2020
Electronic ISSN: 1471-230X
DOI
https://doi.org/10.1186/s12876-020-01270-7

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