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Published in: BMC Endocrine Disorders 1/2015

Open Access 01-12-2015 | Research article

Subclinical and clinical hypothyroidism and non-alcoholic fatty liver disease: a cross-sectional study of a random population sample aged 18 to 65 years

Authors: Ulla Ludwig, Daniela Holzner, Christian Denzer, Artur Greinert, Mark Martin Haenle, Suemeyra Oeztuerk, Wolfgang Koenig, Bernhard Otto Boehm, Richard Andrew Mason, Wolfgang Kratzer, Tilmann Graeter, the EMIL-Study

Published in: BMC Endocrine Disorders | Issue 1/2015

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Abstract

Background

Non-alcoholic fatty liver disease (NAFLD) is one of the most common disorders of the liver worldwide. Recently, a correlation between thyroid dysfunction and NAFLD has been discussed. Objective of the present study was to investigate the association between thyroid dysfunction and hepatic steatosis.

Methods

Data from 2,445 subjects (51.7 % females) aged 18 to 65 years participating in a population-based cross-sectional study were assessed based on a standardized questionnaire and documentation of physical, biochemical and ultrasonographic findings. After application of exclusion criteria, a total of 1,276 subjects were included in the study collective. The influence of potential factors on the development of hepatic steatosis was assessed using multivariate logistic regression.

Results

The prevalence of hepatic steatosis in the study collective was 27.4 % (n = 349). The serum thyroxin (TT4) concentration in subjects with hepatic steatosis was reduced (p = 0.0004). Adjusting for age, or BMI, there was an increased prevalence of hepatic steatosis in subjects with reduced TT4 concentrations (p = 0.0143; p = <.0001).

Conclusions

The findings of the present study confirm an association between both subclinical and clinical hypothyroidism and hepatic steatosis
Literature
1.
go back to reference Musso G, Gambino R, Cassader M. Non-alcoholic fatty liver disease from pathogenesis to management: an update. Obes Rev. 2010;11:430–45.CrossRefPubMed Musso G, Gambino R, Cassader M. Non-alcoholic fatty liver disease from pathogenesis to management: an update. Obes Rev. 2010;11:430–45.CrossRefPubMed
2.
go back to reference Oh HJ, Kim TH, Sohn YW, Kim YS, Oh YR, Cho EY, et al. Association of serum alanine aminotransferase and gamma-glutamyltransferase levels within the reference range with metabolic syndrome and nonalcoholic fatty liver disease. Korean J Hepatol. 2011;17:27–36.CrossRefPubMedPubMedCentral Oh HJ, Kim TH, Sohn YW, Kim YS, Oh YR, Cho EY, et al. Association of serum alanine aminotransferase and gamma-glutamyltransferase levels within the reference range with metabolic syndrome and nonalcoholic fatty liver disease. Korean J Hepatol. 2011;17:27–36.CrossRefPubMedPubMedCentral
3.
go back to reference Starley BQ, Calcagno CJ, Harrison SA. Nonalcoholic fatty liver disease and hepatocellular carcinoma: a weighty connection. Hepatology. 2010;51:1820–32.CrossRefPubMed Starley BQ, Calcagno CJ, Harrison SA. Nonalcoholic fatty liver disease and hepatocellular carcinoma: a weighty connection. Hepatology. 2010;51:1820–32.CrossRefPubMed
4.
go back to reference Vuppalanchi R, Chalasani N. Nonalcoholic fatty liver disease and nonalcoholic steatohepatitis: Selected practical issues in their evaluation and management. Hepatology. 2009;49:306–17.CrossRefPubMedPubMedCentral Vuppalanchi R, Chalasani N. Nonalcoholic fatty liver disease and nonalcoholic steatohepatitis: Selected practical issues in their evaluation and management. Hepatology. 2009;49:306–17.CrossRefPubMedPubMedCentral
5.
go back to reference Frith J, Day CP, Henderson E, Burt AD, Newton JL. Non-alcoholic fatty liver disease in older people. Gerontology. 2009;55:607–13.CrossRefPubMed Frith J, Day CP, Henderson E, Burt AD, Newton JL. Non-alcoholic fatty liver disease in older people. Gerontology. 2009;55:607–13.CrossRefPubMed
6.
go back to reference Xu C, Xu L, Yu C, Miao M, Li Y. Association between thyroid function and nonalcoholic fatty liver disease in euthyroid elderly Chinese. Clin Endocrinol (Oxf). 2011;75:240–6.CrossRef Xu C, Xu L, Yu C, Miao M, Li Y. Association between thyroid function and nonalcoholic fatty liver disease in euthyroid elderly Chinese. Clin Endocrinol (Oxf). 2011;75:240–6.CrossRef
7.
go back to reference Zelber-Sagi S, Nitzan-Kaluski D, Halpern Z, Oren R. Prevalence of primary non-alcoholic fatty liver disease in a population-based study and its association with biochemical and anthropometric measures. Liver Int. 2006;26:856–63.CrossRefPubMed Zelber-Sagi S, Nitzan-Kaluski D, Halpern Z, Oren R. Prevalence of primary non-alcoholic fatty liver disease in a population-based study and its association with biochemical and anthropometric measures. Liver Int. 2006;26:856–63.CrossRefPubMed
8.
go back to reference Anstee QM, McPherson S, Day CP. How big a problem is non-alcoholic fatty liver disease? BMJ. 2011;343:d3897.CrossRefPubMed Anstee QM, McPherson S, Day CP. How big a problem is non-alcoholic fatty liver disease? BMJ. 2011;343:d3897.CrossRefPubMed
9.
go back to reference Bookman ID, Pham J, Guindi M, Heathcote EJ. Distinguishing nonalcoholic steatohepatitis from fatty liver: serum-free fatty acids, insulin resistance, and serum lipoproteins. Liver Int. 2006;26:566–71.CrossRefPubMed Bookman ID, Pham J, Guindi M, Heathcote EJ. Distinguishing nonalcoholic steatohepatitis from fatty liver: serum-free fatty acids, insulin resistance, and serum lipoproteins. Liver Int. 2006;26:566–71.CrossRefPubMed
10.
go back to reference Papandreou D, Rousso I, Mavromichalis I. Update on non-alcoholic fatty liver disease in children. Clin Nutr. 2007;26:409–15.CrossRefPubMed Papandreou D, Rousso I, Mavromichalis I. Update on non-alcoholic fatty liver disease in children. Clin Nutr. 2007;26:409–15.CrossRefPubMed
12.
go back to reference Kotronen A, Yki-Järvinen H. Fatty liver: a novel component of the metabolic syndrome. Arterioscler Thromb Vasc Biol. 2008;28:27–38.CrossRefPubMed Kotronen A, Yki-Järvinen H. Fatty liver: a novel component of the metabolic syndrome. Arterioscler Thromb Vasc Biol. 2008;28:27–38.CrossRefPubMed
13.
go back to reference Chung GE, Kim D, Kim W, Yim JY, Park MJ, Kim YJ, et al. Non-alcoholic fatty liver disease across the spectrum of hypothyroidism. J Hepatol. 2012;57:150–6.CrossRefPubMed Chung GE, Kim D, Kim W, Yim JY, Park MJ, Kim YJ, et al. Non-alcoholic fatty liver disease across the spectrum of hypothyroidism. J Hepatol. 2012;57:150–6.CrossRefPubMed
14.
go back to reference Liangpunsakul S, Chalasani N. Is hypothyroidism a risk factor for non-alcoholic steatohepatitis? J Clin Gastroenterol. 2003;37:340–3.CrossRefPubMed Liangpunsakul S, Chalasani N. Is hypothyroidism a risk factor for non-alcoholic steatohepatitis? J Clin Gastroenterol. 2003;37:340–3.CrossRefPubMed
15.
go back to reference Pagadala MR, Zein CO, Dasarathy S, Yerian LM, Lopez R, McCullough AJ. Prevalence of hypothyroidism in nonalcoholic fatty liver disease. Dig Dis Sci. 2012;57:528–34.CrossRefPubMed Pagadala MR, Zein CO, Dasarathy S, Yerian LM, Lopez R, McCullough AJ. Prevalence of hypothyroidism in nonalcoholic fatty liver disease. Dig Dis Sci. 2012;57:528–34.CrossRefPubMed
16.
go back to reference Xu L, Ma H, Miao M, Li Y. Impact of subclinical hypothyroidism on the development of non-alcoholic fatty liver disease: A prospective case–control study. J Hepato. 2012;57:1153–4.CrossRef Xu L, Ma H, Miao M, Li Y. Impact of subclinical hypothyroidism on the development of non-alcoholic fatty liver disease: A prospective case–control study. J Hepato. 2012;57:1153–4.CrossRef
17.
go back to reference Loria P, Carulli L, Bertolotti M, Lonardo A. Endocrine and liver interaction: the role of endocrine pathways in NASH. Nat Rev Gastroenterol Hepatol. 2009;6:236–47.CrossRefPubMed Loria P, Carulli L, Bertolotti M, Lonardo A. Endocrine and liver interaction: the role of endocrine pathways in NASH. Nat Rev Gastroenterol Hepatol. 2009;6:236–47.CrossRefPubMed
18.
go back to reference Ineck BA, Ng TM. Effects of subclinical hypothyroidism and its treatment on serum lipids. Ann Pharmacother. 2003;37:725–30.CrossRefPubMed Ineck BA, Ng TM. Effects of subclinical hypothyroidism and its treatment on serum lipids. Ann Pharmacother. 2003;37:725–30.CrossRefPubMed
19.
go back to reference Haenle MM, Brockmann SO, Kron M, Bertling U, Mason RA, Steinbach G, et al. Overweight, physical activity, tobacco and alcohol consumption in a cross-sectional random sample of German adults. BMC Public Health. 2006;6:233.CrossRefPubMedPubMedCentral Haenle MM, Brockmann SO, Kron M, Bertling U, Mason RA, Steinbach G, et al. Overweight, physical activity, tobacco and alcohol consumption in a cross-sectional random sample of German adults. BMC Public Health. 2006;6:233.CrossRefPubMedPubMedCentral
20.
go back to reference Expert Panel on Detection. Evaluation, and treatment of high blood cholesterol in adults: executive summary of the third report of the national cholesterol education program (NCEP) (2001) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (adult treatment panel III). JAMA. 2001;285:2486–97.CrossRef Expert Panel on Detection. Evaluation, and treatment of high blood cholesterol in adults: executive summary of the third report of the national cholesterol education program (NCEP) (2001) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (adult treatment panel III). JAMA. 2001;285:2486–97.CrossRef
21.
go back to reference Saverymuttu SH, Joseph AE, Maxwell JD. Ultrasound scanning in the detection of hepatic fibrosis and steatosis. Br Med J (Clin Res Ed). 1986;292:13–5.CrossRef Saverymuttu SH, Joseph AE, Maxwell JD. Ultrasound scanning in the detection of hepatic fibrosis and steatosis. Br Med J (Clin Res Ed). 1986;292:13–5.CrossRef
22.
go back to reference Hamaguchi M, Kojima T, Itoh Y, Harano Y, Fujii K, Nakajima T, et al. The severity of ultrasonographic findings in nonalcoholic fatty liver disease reflects the metabolic syndrome and visceral fat accumulation. Am J Gastroenterol. 2003;102:2708–15.CrossRef Hamaguchi M, Kojima T, Itoh Y, Harano Y, Fujii K, Nakajima T, et al. The severity of ultrasonographic findings in nonalcoholic fatty liver disease reflects the metabolic syndrome and visceral fat accumulation. Am J Gastroenterol. 2003;102:2708–15.CrossRef
23.
go back to reference Charatcharoenwitthaya P, Lindor KD. Role of radiologic modalities in the management of non-alcoholic steatohepatitis. Clin Liver. 2007;11:37–54.CrossRef Charatcharoenwitthaya P, Lindor KD. Role of radiologic modalities in the management of non-alcoholic steatohepatitis. Clin Liver. 2007;11:37–54.CrossRef
24.
go back to reference Eshraghian A, Dabbaghmanesh MH, Eshraghian H, Fattahi MR, Omrani GR. Nonalcoholic fatty liver disease in a cluster of Iranian population: thyroid status and metabolic risk factors. Arch Iran Med. 2013;16:584–9.PubMed Eshraghian A, Dabbaghmanesh MH, Eshraghian H, Fattahi MR, Omrani GR. Nonalcoholic fatty liver disease in a cluster of Iranian population: thyroid status and metabolic risk factors. Arch Iran Med. 2013;16:584–9.PubMed
25.
go back to reference Mazo DF, Lima VM, Stefano JT, Rabelo F, Faintuch J, Oliveira CP. Gluco-lipidic indices in treated hypothyroidism associated with nonalcoholic fatty liver disease. Arq Gastroenterol. 2011;48:186–9.CrossRefPubMed Mazo DF, Lima VM, Stefano JT, Rabelo F, Faintuch J, Oliveira CP. Gluco-lipidic indices in treated hypothyroidism associated with nonalcoholic fatty liver disease. Arq Gastroenterol. 2011;48:186–9.CrossRefPubMed
26.
go back to reference Gardner CJ, Richardson P, Wong C, Polavarapu N, Kemp GJ, Cuthbertson DJ. Hypothyroidism in a patient with non-alcoholic fatty liver disease. BMJ. 2011;342:c7199.CrossRefPubMed Gardner CJ, Richardson P, Wong C, Polavarapu N, Kemp GJ, Cuthbertson DJ. Hypothyroidism in a patient with non-alcoholic fatty liver disease. BMJ. 2011;342:c7199.CrossRefPubMed
27.
go back to reference Zhang Y, Chang Y, Ryu S, Cho J, Lee WY, Rhee EJ, et al. Thyroid hormones and mortality risk in euthyroid individuals: the Kangbuk Samsung health study. J Clin Endocrinol Metab. 2014;99:2467–76.CrossRefPubMed Zhang Y, Chang Y, Ryu S, Cho J, Lee WY, Rhee EJ, et al. Thyroid hormones and mortality risk in euthyroid individuals: the Kangbuk Samsung health study. J Clin Endocrinol Metab. 2014;99:2467–76.CrossRefPubMed
28.
go back to reference Carulli L, Ballestri S, Lonardo A, Lami F, Violi E, Losi L, et al. Is nonalcoholic steatohepatitis associated with a high-though-normal thyroid stimulating hormone level and lower cholesterol levels? Intern Emerg Med. 2013;8:297–305.CrossRefPubMed Carulli L, Ballestri S, Lonardo A, Lami F, Violi E, Losi L, et al. Is nonalcoholic steatohepatitis associated with a high-though-normal thyroid stimulating hormone level and lower cholesterol levels? Intern Emerg Med. 2013;8:297–305.CrossRefPubMed
29.
go back to reference Moustafa AH, Ali EM, Mohamed TM, Abdou HI. Oxidative stress and thyroid hormones in patients with liver diseases. Eur J Intern Med. 2009;20:703–8.CrossRefPubMed Moustafa AH, Ali EM, Mohamed TM, Abdou HI. Oxidative stress and thyroid hormones in patients with liver diseases. Eur J Intern Med. 2009;20:703–8.CrossRefPubMed
30.
go back to reference Silveira MG1, Mendes FD, Diehl NN, Enders FT, Lindor KD. Thyroid dysfunction in primary biliary cirrhosis, primary sclerosing cholangitis and non-alcoholic fatty liver disease. Liver Int. 2009;29:1094–100.CrossRefPubMed Silveira MG1, Mendes FD, Diehl NN, Enders FT, Lindor KD. Thyroid dysfunction in primary biliary cirrhosis, primary sclerosing cholangitis and non-alcoholic fatty liver disease. Liver Int. 2009;29:1094–100.CrossRefPubMed
31.
go back to reference Ittermann T, Haring R, Wallaschofski H, Baumeister SE, Nauck M, Dörr M, et al. Inverse association between serum free thyroxine levels and hepatic steatosis: results from the Study of Health in Pomerania. Thyroid. 2012;22:568–74.CrossRefPubMedPubMedCentral Ittermann T, Haring R, Wallaschofski H, Baumeister SE, Nauck M, Dörr M, et al. Inverse association between serum free thyroxine levels and hepatic steatosis: results from the Study of Health in Pomerania. Thyroid. 2012;22:568–74.CrossRefPubMedPubMedCentral
32.
go back to reference Park HT, Cho GJ, Ahn KH, Shin JH, Hong SC, Kim T, et al. Thyroid stimulating hormone is associated with metabolic syndrome in euthyroid postmenopausal women. Maturitas. 2009;62:301–5.CrossRefPubMed Park HT, Cho GJ, Ahn KH, Shin JH, Hong SC, Kim T, et al. Thyroid stimulating hormone is associated with metabolic syndrome in euthyroid postmenopausal women. Maturitas. 2009;62:301–5.CrossRefPubMed
33.
go back to reference Roos A, Bakker SJ, Links TP, Gans RO, Wolffenbuttel BH. Thyroid function is associated with components of the metabolic syndrome in euthyroid subjects. J Clin Endocrinol Metab. 2007;92:491–6.CrossRefPubMed Roos A, Bakker SJ, Links TP, Gans RO, Wolffenbuttel BH. Thyroid function is associated with components of the metabolic syndrome in euthyroid subjects. J Clin Endocrinol Metab. 2007;92:491–6.CrossRefPubMed
34.
go back to reference Garduño-Garcia Jde J, Alvirde-Garcia U, López-Carrasco G, Padilla Mendoza ME, Mehta R, Arellano-Campos O, et al. TSH and free thyroxine concentrations are associated with differing metabolic markers in euthyroid subjects. Eur J Endocrinol. 2010;163:273–8.CrossRefPubMed Garduño-Garcia Jde J, Alvirde-Garcia U, López-Carrasco G, Padilla Mendoza ME, Mehta R, Arellano-Campos O, et al. TSH and free thyroxine concentrations are associated with differing metabolic markers in euthyroid subjects. Eur J Endocrinol. 2010;163:273–8.CrossRefPubMed
35.
go back to reference Liu C, Scherbaum WA, Schott M, Schinner S. Subclinical hypothyroidism and the prevalence of the metabolic syndrome. Horm Metab Res. 2011;43:417–21.CrossRefPubMed Liu C, Scherbaum WA, Schott M, Schinner S. Subclinical hypothyroidism and the prevalence of the metabolic syndrome. Horm Metab Res. 2011;43:417–21.CrossRefPubMed
36.
go back to reference Tagami T, Kimura H, Ohtani S, Tanaka T, Tanaka T, Hata S, et al. PHPH study group: multi-center study on the prevalence of hypothyroidism in patients with hypercholesterolemia. Endocr J. 2011;58:449–57.CrossRefPubMed Tagami T, Kimura H, Ohtani S, Tanaka T, Tanaka T, Hata S, et al. PHPH study group: multi-center study on the prevalence of hypothyroidism in patients with hypercholesterolemia. Endocr J. 2011;58:449–57.CrossRefPubMed
Metadata
Title
Subclinical and clinical hypothyroidism and non-alcoholic fatty liver disease: a cross-sectional study of a random population sample aged 18 to 65 years
Authors
Ulla Ludwig
Daniela Holzner
Christian Denzer
Artur Greinert
Mark Martin Haenle
Suemeyra Oeztuerk
Wolfgang Koenig
Bernhard Otto Boehm
Richard Andrew Mason
Wolfgang Kratzer
Tilmann Graeter
the EMIL-Study
Publication date
01-12-2015
Publisher
BioMed Central
Published in
BMC Endocrine Disorders / Issue 1/2015
Electronic ISSN: 1472-6823
DOI
https://doi.org/10.1186/s12902-015-0030-5

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