{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,11,1]],"date-time":"2026-11-01T07:02:24Z","timestamp":1793516544830,"version":"4.5.0"},"reference-count":52,"publisher":"MDPI AG","issue":"19","license":[{"start":{"date-parts":[[2023,9,27]],"date-time":"2023-09-27T00:00:00Z","timestamp":1695772800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Medica Sur Clinic and Foundation"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>The prevalence of hypothyroidism in patients with nonalcoholic fatty liver disease (NAFLD) is high (22.4%). Thyroid hormones (THs) regulate many metabolic activities in the liver by promoting the export and oxidation of lipids, as well as de novo lipogenesis. They also control hepatic insulin sensitivity and suppress hepatic gluconeogenesis. Because of its importance in lipid and carbohydrate metabolism, the involvement of thyroid dysfunction in the pathogenesis of NAFLD seems plausible. The mechanisms implicated in this relationship include high thyroid-stimulating hormone (TSH) levels, low TH levels, and chronic inflammation. The activity of the TH receptor (THR)-\u03b2 in response to THs is essential in the pathogenesis of hypothyroidism-induced NAFLD. Therefore, an orally active selective liver THR-\u03b2 agonist, Resmetirom (MGL-3196), was developed, and has been shown to reduce liver fat content, and as a secondary end point, to improve nonalcoholic steatohepatitis. The treatment of NAFLD with THR-\u03b2 agonists seems quite promising, and other agonists are currently under development and investigation. This review aims to shine a light on the pathophysiological and epidemiological evidence regarding this relationship and the effect that treatment with THs and selective liver THR-\u03b2 agonists have on hepatic lipid metabolism.<\/jats:p>","DOI":"10.3390\/ijms241914605","type":"journal-article","created":{"date-parts":[[2023,9,27]],"date-time":"2023-09-27T03:04:18Z","timestamp":1695783858000},"page":"14605","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":50,"title":["Understanding the Relationship between Nonalcoholic Fatty Liver Disease and Thyroid Disease"],"prefix":"10.3390","volume":"24","author":[{"given":"Paulina","family":"Vidal-Cevallos","sequence":"first","affiliation":[{"name":"Obesity and Digestive Disease Unit, Medica Sur Clinic and Foundation, Av. Puente de Piedra 150, Toriello Guerra, Tlalpan, Mexico City 14050, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0692-8219","authenticated-orcid":false,"given":"Sof\u00eda","family":"Mur\u00faa-Beltr\u00e1n Gall","sequence":"additional","affiliation":[{"name":"Obesity and Digestive Disease Unit, Medica Sur Clinic and Foundation, Av. Puente de Piedra 150, Toriello Guerra, Tlalpan, Mexico City 14050, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Misael","family":"Uribe","sequence":"additional","affiliation":[{"name":"Obesity and Digestive Disease Unit, Medica Sur Clinic and Foundation, Av. Puente de Piedra 150, Toriello Guerra, Tlalpan, Mexico City 14050, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7451-3306","authenticated-orcid":false,"given":"Norberto C.","family":"Ch\u00e1vez-Tapia","sequence":"additional","affiliation":[{"name":"Obesity and Digestive Disease Unit, Medica Sur Clinic and Foundation, Av. Puente de Piedra 150, Toriello Guerra, Tlalpan, Mexico City 14050, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,9,27]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"551","DOI":"10.4254\/wjh.v14.i3.551","article-title":"Prevalence of hypothyroidism and effect of thyroid hormone replacement therapy in patients with non-alcoholic fatty liver disease: A population-based study","volume":"14","author":"Almomani","year":"2022","journal-title":"World J. Hepatol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1007\/s12664-015-0541-z","article-title":"Prevalence of hypothyroidism in nonalcoholic fatty liver disease in patients attending a tertiary hospital in western India","volume":"34","author":"Parikh","year":"2015","journal-title":"Indian J. Gastroenterol."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Ludwig, U., Holzner, D., Denzer, C., Greinert, A., Haenle, M.M., Oeztuerk, S., Koenig, W., Boehm, B.O., Mason, R.A., and Kratzer, W. (2015). Subclinical and clinical hypothyroidism and non-alcoholic fatty liver disease: A cross-sectional study of a random population sample aged 18 to 65 years. BMC Endocr. Disord., 15.","DOI":"10.1186\/s12902-015-0030-5"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1038\/nrendo.2018.18","article-title":"Global epidemiology of hyperthyroidism and hypothyroidism","volume":"14","author":"Taylor","year":"2018","journal-title":"Nat. Rev. Endocrinol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"923","DOI":"10.1210\/jc.2013-2409","article-title":"The incidence and prevalence of thyroid dysfunction in Europe: A meta-analysis","volume":"99","author":"Madariaga","year":"2014","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1388","DOI":"10.1016\/j.jhep.2015.11.004","article-title":"EASL-EASD-EASO Clinical Practice Guidelines for the management of non-alcoholic fatty liver disease","volume":"64","author":"Marchesini","year":"2016","journal-title":"J. Hepatol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"328","DOI":"10.1002\/hep.29367","article-title":"The diagnosis and management of nonalcoholic fatty liver disease: Practice guidance from the American Association for the Study of Liver Diseases","volume":"67","author":"Chalasani","year":"2018","journal-title":"Hepatology"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1038\/nrgastro.2017.109","article-title":"Global burden of NAFLD and NASH: Trends, predictions, risk factors and prevention","volume":"15","author":"Younossi","year":"2018","journal-title":"Nat. Rev. Gastroenterol. Hepatol."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Rinella, M.E., Lazarus, J.V., Ratziu, V., Francque, S.M., Sanyal, A.J., Kanwal, F., Romero, D., Abdelmalek, M.F., Anstee, Q.M., and Arab, J.P. (J. Hepatol., 2023). A multi-society Delphi consensus statement on new fatty liver disease nomenclature, J. Hepatol., in press.","DOI":"10.1097\/HEP.0000000000000520"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"462","DOI":"10.1016\/j.dld.2018.12.014","article-title":"Pathogenesis of hypothyroidism-induced NAFLD: Evidence for a distinct disease entity?","volume":"51","author":"Lonardo","year":"2019","journal-title":"Dig. Liver Dis."},{"key":"ref_11","first-page":"e14858","article-title":"Unraveling the Role of Hypothyroidism in Non-alcoholic Fatty Liver Disease Pathogenesis: Correlations, Conflicts, and the Current Stand","volume":"13","author":"Gor","year":"2021","journal-title":"Cureus"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"R52","DOI":"10.1530\/EC-20-0490","article-title":"Pathophysiology of nash in endocrine diseases","volume":"10","author":"Gariani","year":"2021","journal-title":"Endocr. Connect."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Mavromati, M., and Jornayvaz, F.R. (2021). Review hypothyroidism-associated dyslipidemia: Potential molecular mechanisms leading to NAFLD. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms222312797"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1016\/j.mce.2017.02.015","article-title":"Thyroid stimulating hormone increases hepatic gluconeogenesis via CRTC2","volume":"446","author":"Li","year":"2017","journal-title":"Mol. Cell. Endocrinol."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Mart\u00ednez-Escud\u00e9, A., Pera, G., Costa-Garrido, A., Rodr\u00edguez, L., Arteaga, I., Exp\u00f3sito-Mart\u00ednez, C., Tor\u00e1n-Monserrat, P., and Caballer\u00eda, L. (2021). TSH levels as an independent risk factor for NAFLD and liver fibrosis in the general population. J. Clin. Med., 10.","DOI":"10.3390\/jcm10132907"},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Tanase, D.M., Gosav, E.M., Neculae, E., Costea, C.F., Ciocoiu, M., Hurjui, L.L., Tarniceriu, C.C., and Floria, M. (2020). Hypothyroidism-induced nonalcoholic fatty liver disease (Hin): Mechanisms and emerging therapeutic options. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21165927"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1448","DOI":"10.1530\/EC-18-0499","article-title":"Reduced expression of thyroid hormone receptor \u03b2 in human nonalcoholic steatohepatitis","volume":"7","author":"Krause","year":"2018","journal-title":"Endocr. Connect."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1016\/j.steroids.2006.11.008","article-title":"Molecular modeling of the thyroid hormone interactions with \u03b1v\u03b23 integrin","volume":"72","author":"Cody","year":"2007","journal-title":"Steroids"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1780","DOI":"10.1073\/pnas.0510849103","article-title":"Activation of phosphatidylinositol 3-kinase signaling by a mutant thyroid hormone \u03b2 receptor","volume":"103","author":"Furuya","year":"2006","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"30365","DOI":"10.1074\/jbc.M113.504845","article-title":"FoxO1 deacetylation regulates thyroid hormone-induced transcription of key hepatic gluconeogenic genes","volume":"288","author":"Singh","year":"2013","journal-title":"J. Biol. Chem."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Damiano, F., Rochira, A., Gnoni, A., and Siculella, L. (2017). Action of thyroid hormones, T3 and T2, on hepatic fatty acids: Differences in metabolic effects and molecular mechanisms. Int. J. Mol. Sci., 18.","DOI":"10.3390\/ijms18040744"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"742","DOI":"10.1002\/hep.31296","article-title":"Thyroid Hormone Signaling and the Liver","volume":"72","author":"Ritter","year":"2020","journal-title":"Hepatology"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"770","DOI":"10.1002\/hep.31204","article-title":"Thyroid Hormones and Thyromimetics: A New Approach to Nonalcoholic Steatohepatitis?","volume":"72","author":"Sinha","year":"2020","journal-title":"Hepatology"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1216","DOI":"10.1016\/j.bbalip.2007.05.001","article-title":"Activation of the hepatic LDL receptor promoter by thyroid hormone","volume":"1771","author":"Lopez","year":"2007","journal-title":"Biochim. Biophys. Acta-Mol. Cell Biol. Lipids"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"2408","DOI":"10.1194\/jlr.M051664","article-title":"Thyroid hormone reduces PCSK9 and stimulates bile acid synthesis in humans","volume":"55","author":"Bonde","year":"2014","journal-title":"J. Lipid Res."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"3417","DOI":"10.1210\/en.2009-0059","article-title":"Carbohydrate response element binding protein gene expression is positively regulated by thyroid hormone","volume":"150","author":"Hashimoto","year":"2009","journal-title":"Endocrinology"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"E1741","DOI":"10.1210\/clinem\/dgaa097","article-title":"Resting energy expenditure in obese women with primary hypothyroidism and appropriate levothyroxine replacement therapy","volume":"105","author":"Muraca","year":"2020","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"ref_28","first-page":"629","article-title":"Thyroid dysfunction in obese adults in relation to nonalcoholic fatty liver disease","volume":"31","author":"Mohamed","year":"2020","journal-title":"Egypt. J. Intern. Med."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"335","DOI":"10.3389\/fendo.2017.00335","article-title":"Relationship between Hypothyroidism and Non-Alcoholic Fatty Liver Disease: A Systematic Review and Meta-analysis","volume":"8","author":"He","year":"2017","journal-title":"Front. Endocrinol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"208","DOI":"10.1159\/000454920","article-title":"Nonalcoholic Fatty Liver Disease Is Not Associated with Thyroid Hormone Levels and Hypothyroidism: A Systematic Review and Meta-Analysis","volume":"6","author":"Jaruvongvanich","year":"2017","journal-title":"Eur. Thyroid J."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1270","DOI":"10.1089\/thy.2018.0257","article-title":"Association between Primary Hypothyroidism and Nonalcoholic Fatty Liver Disease: A Systematic Review and Meta-Analysis","volume":"28","author":"Mantovani","year":"2018","journal-title":"Thyroid"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1153","DOI":"10.1016\/j.dld.2018.08.012","article-title":"Association of non-alcoholic fatty liver disease with thyroid function: A systematic review and meta-analysis","volume":"50","author":"Guo","year":"2018","journal-title":"Dig. Liver Dis."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"643582","DOI":"10.3389\/fcell.2021.643582","article-title":"Exploring the Causality Between Hypothyroidism and Non-alcoholic Fatty Liver: A Mendelian Randomization Study","volume":"9","author":"Qiu","year":"2021","journal-title":"Front. Cell Dev. Biol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"2698","DOI":"10.1210\/jc.2018-00475","article-title":"Low-dose levothyroxine reduces intrahepatic lipid content in patients with type 2 diabetes mellitus and NAFLD","volume":"103","author":"Bruinstroop","year":"2018","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"382","DOI":"10.3389\/fendo.2018.00382","article-title":"Thyroid hormones, thyromimetics and their metabolites in the treatment of liver disease","volume":"9","author":"Kowalik","year":"2018","journal-title":"Front. Endocrinol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"5753039","DOI":"10.1155\/2017\/5753039","article-title":"Benefits of levothyroxine replacement therapy on nonalcoholic fatty liver disease in subclinical hypothyroidism patients","volume":"2017","author":"Liu","year":"2017","journal-title":"Int. J. Endocrinol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1656","DOI":"10.1210\/en.2003-0973","article-title":"Effects of the Thyroid Hormone Receptor Agonist GC-1 on Metabolic Rate and Cholesterol in Rats and Primates: Selective Actions Relative to 3,5,3\u2032-Triiodo-L-Thyronine","volume":"145","author":"Grover","year":"2004","journal-title":"Endocrinology"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1677\/joe.1.07066","article-title":"Thyroid hormone receptor \u03b2-specific agonist GC-1 increases energy expenditure and prevents fat-mass accumulation in rats","volume":"193","author":"Villicev","year":"2007","journal-title":"J. Endocrinol."},{"key":"ref_39","first-page":"E89","article-title":"Thyroid hormone receptor-\u03b2 agonists prevent hepatic steatosis in fat-fed rats but impair insulin sensitivity via discrete pathways","volume":"305","author":"Vatner","year":"2013","journal-title":"Am. J. Physiol. Metab."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1016\/S2213-8587(14)70006-3","article-title":"Eprotirome in patients with familial hypercholesterolaemia (the AKKA trial): A randomised, double-blind, placebo-controlled phase 3 study","volume":"2","author":"Sjouke","year":"2014","journal-title":"Lancet Diabetes Endocrinol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1111\/joim.12261","article-title":"Reductions in serum levels of LDL cholesterol, apolipoprotein B, triglycerides and lipoprotein(a) in hypercholesterolaemic patients treated with the liver-selective thyroid hormone receptor agonist eprotirome","volume":"277","author":"Angelin","year":"2015","journal-title":"J. Intern. Med."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"van der Valk, F., Hassing, C., Visser, M., Thakkar, P., Mohanan, A., Pathak, K., Dutt, C., Chauthaiwale, V., Ackermans, M., and Nederveen, A. (2014). The Effect of a Diiodothyronine Mimetic on Insulin Sensitivity in Male Cardiometabolic Patients: A Double-Blind Randomized Controlled Trial. PLoS ONE, 9, Available online: https:\/\/dx.plos.org\/10.1371\/journal.pone.0086890.","DOI":"10.1371\/journal.pone.0086890"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1349","DOI":"10.1210\/jc.2009-1209","article-title":"Effects of the Thyromimetic Agent Diiodothyropropionic Acid on Body Weight, Body Mass Index, and Serum Lipoproteins: A Pilot Prospective, Randomized, Controlled Study","volume":"95","author":"Ladenson","year":"2010","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"ref_44","first-page":"2153","article-title":"Augmented Hepatic and Skeletal Thyromimetic Effects of Tiratricol in Comparison with Levothyroxine 1","volume":"82","author":"Sherman","year":"1997","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"3912","DOI":"10.1021\/jm4019299","article-title":"Discovery of 2-[3,5-Dichloro-4-(5-isopropyl-6-oxo-1,6-dihydropyridazin-3-yloxy)phenyl]-3,5-dioxo-2,3,4,5-tetrahydro[1,2,4]triazine-6-carbonitrile (MGL-3196), a Highly Selective Thyroid Hormone Receptor \u03b2 Agonist in Clinical Trials for the Treatment of Dys","volume":"57","author":"Kelly","year":"2014","journal-title":"J. Med. Chem."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1016\/j.atherosclerosis.2013.07.056","article-title":"Lipid lowering in healthy volunteers treated with multiple doses of MGL-3196, a liver-targeted thyroid hormone receptor-\u03b2 agonist","volume":"230","author":"Taub","year":"2013","journal-title":"Atherosclerosis"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"573","DOI":"10.1002\/hep4.1657","article-title":"Effects of Resmetirom on Noninvasive Endpoints in a 36-Week Phase 2 Active Treatment Extension Study in Patients With NASH","volume":"5","author":"Harrison","year":"2021","journal-title":"Hepatol. Commun."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1354","DOI":"10.1016\/j.cgh.2021.07.039","article-title":"Hepatic Fat Reduction Due to Resmetirom in Patients with Nonalcoholic Steatohepatitis Is Associated With Improvement of Quality of Life","volume":"20","author":"Younossi","year":"2022","journal-title":"Clin. Gastroenterol. Hepatol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1080\/13543784.2020.1708899","article-title":"Thyromimetics as emerging therapeutic agents for nonalcoholic steatohepatitis: Rationale for the development of resmetirom (MGL-3196)","volume":"29","author":"Alkhouri","year":"2020","journal-title":"Expert Opin. Investig. Drugs"},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Wang, B., Wang, B., Yang, Y., Xu, J., Hong, M., Xia, M., Li, X., and Gao, X. (2021). Thyroid function and non-alcoholic fatty liver disease in hyperthyroidism patients. BMC Endocr. Disord., 21.","DOI":"10.1186\/s12902-021-00694-w"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"829","DOI":"10.1002\/ueg2.12124","article-title":"Impact of thyroid disorders on the incidence of non-alcoholic fatty liver disease in Germany","volume":"9","author":"Labenz","year":"2021","journal-title":"United Eur. Gastroenterol. J."},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Caddeo, A., Kowalik, M.A., Serra, M., Runfola, M., Bacci, A., Rapposelli, S., Columbano, A., and Perra, A. (2021). Tg68, a novel thyroid hormone receptor-\u03b2 agonist for the treatment of nafld. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms222313105"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/19\/14605\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T20:59:18Z","timestamp":1760129958000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/19\/14605"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,9,27]]},"references-count":52,"journal-issue":{"issue":"19","published-online":{"date-parts":[[2023,10]]}},"alternative-id":["ijms241914605"],"URL":"https:\/\/doi.org\/10.3390\/ijms241914605","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,9,27]]}}}