{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,15]],"date-time":"2026-10-15T22:37:07Z","timestamp":1792103827162,"version":"4.4.0"},"reference-count":38,"publisher":"Oxford University Press (OUP)","issue":"9","license":[{"start":{"date-parts":[[2020,9,1]],"date-time":"2020-09-01T00:00:00Z","timestamp":1598918400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"DOI":"10.13039\/100000062","name":"National Institute of Diabetes and Digestive and Kidney Diseases","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000062","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["R01-DK94818"],"award-info":[{"award-number":["R01-DK94818"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["NCT01924455"],"award-info":[{"award-number":["NCT01924455"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["K24AA022523"],"award-info":[{"award-number":["K24AA022523"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["K24DA034621"],"award-info":[{"award-number":["K24DA034621"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["K24DK078772"],"award-info":[{"award-number":["K24DK078772"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100005294","name":"Massachusetts General Hospital","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100005294","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2021,11,2]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:sec>\n                  <jats:title>Background<\/jats:title>\n                  <jats:p>Hepatitis B virus (HBV) and fatty liver disease (FLD) are common in human immunodeficiency virus (HIV). Correlates of FLD and its relationship with alanine aminotransferase (ALT) were examined longitudinally in HIV-HBV coinfection.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Methods<\/jats:title>\n                  <jats:p>From 28\/4\/2014\u20137\/11\/2018, 114 HIV-HBV adults had liver biopsy and were followed for a median of 3 years (ancillary study of Hepatitis B Research Network). Steatohepatitis was based on presence of steatosis, ballooning, and perisinusoidal fibrosis. FLD was defined as \u22655% steatosis and\/or steatohepatitis.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Results<\/jats:title>\n                  <jats:p>Median age was 49 years, 93% were male, 51% black, 93% had HIV RNA &amp;lt;400 copies\/mL and 83% HBV DNA &amp;lt;1000 IU\/mL. Thirty percent had FLD (20% steatosis, 10% steatohepatitis). Those with FLD had higher median triglyceride (171 vs 100 mg\/dL, P\u2005&amp;lt;\u2005.01) and small, dense LDL (44 vs 29 mg\/dL, P\u2005&amp;lt;\u2005.01) and lower HDL-2-C (9 vs 12 mg\/dL, P\u2005=\u2005.001). After adjusting for age, sex, and alcohol use, white and other versus black race (ORs, 8.49 and 16.54, respectively), ALT (OR, 3.13\/doubling), hypertension (OR, 10.93), hyperlipidemia (OR, 4.36), and diabetes family history (OR, 5.38) were associated with having FLD (all P &amp;lt; .05). Steatohepatitis or steatosis alone (vs none) was associated with higher ALT over time (1.93 and 1.34 times higher, respectively; P\u2005&amp;lt;\u2005.001), with adjustment for age, sex, and HBV DNA.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Conclusions<\/jats:title>\n                  <jats:p>About 30% with HIV-HBV coinfection had FLD including 10% with steatohepatitis. FLD was associated with non-black race, metabolic risks, an atherogenic lipid profile, and elevated ALT over time. Thus, identification of FLD and management of adverse metabolic profiles are critically important in HIV-HBV coinfection.<\/jats:p>\n                  <jats:p>Clinical Trial Registration. NCT 01924455.<\/jats:p>\n               <\/jats:sec>","DOI":"10.1093\/cid\/ciaa1303","type":"journal-article","created":{"date-parts":[[2020,8,27]],"date-time":"2020-08-27T19:12:34Z","timestamp":1598555554000},"page":"e3275-e3285","source":"Crossref","is-referenced-by-count":20,"title":["Fatty Liver Disease in a Prospective North American Cohort of Adults With Human Immunodeficiency Virus and Hepatitis B Virus Coinfection"],"prefix":"10.1093","volume":"73","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-9178-9139","authenticated-orcid":false,"given":"Mandana","family":"Khalili","sequence":"first","affiliation":[{"name":"University of California San Francisco, San Francisco, California, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wendy C","family":"King","sequence":"additional","affiliation":[{"name":"University of Pittsburgh Graduate School of Public Health, Pittsburgh, Pennsylvania, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David E","family":"Kleiner","sequence":"additional","affiliation":[{"name":"National Institutes of Health, Bethesda, Maryland, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mamta K","family":"Jain","sequence":"additional","affiliation":[{"name":"University of Texas Southwestern Medical Center, Dallas, Texas, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Raymond T","family":"Chung","sequence":"additional","affiliation":[{"name":"Massachusetts General Hospital, Boston, Massachusetts, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mark","family":"Sulkowski","sequence":"additional","affiliation":[{"name":"Johns Hopkins University, Baltimore, Maryland, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mauricio","family":"Lisker-Melman","sequence":"additional","affiliation":[{"name":"Washington University School of Medicine, St Louis, Missouri, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David K","family":"Wong","sequence":"additional","affiliation":[{"name":"University Health Network, Toronto, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marc","family":"Ghany","sequence":"additional","affiliation":[{"name":"National Institutes of Health, Bethesda, Maryland, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Arun","family":"Sanyal","sequence":"additional","affiliation":[{"name":"Virginia Commonwealth University, Richmond, Virginia, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Richard K","family":"Sterling","sequence":"additional","affiliation":[{"name":"Virginia Commonwealth University, Richmond, Virginia, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2020,9,1]]},"reference":[{"key":"2021110300153271400_CIT0001","author":"UNAIDS"},{"key":"2021110300153271400_CIT0002","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1016\/S0140-6736(08)61113-7","article-title":"Life expectancy of individuals on combination antiretroviral therapy in high-income countries: a collaborative analysis of 14 cohort studies","volume":"372","author":"Antiretroviral Therapy Cohort Collaboration","year":"2008","journal-title":"Lancet"},{"key":"2021110300153271400_CIT0003","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.cld.2014.09.001","article-title":"Chronic liver disease in the human immunodeficiency virus patient","volume":"19","author":"Acharya","year":"2015","journal-title":"Clin Liver Dis"},{"key":"2021110300153271400_CIT0004","doi-asserted-by":"crossref","first-page":"1537","DOI":"10.1097\/QAD.0b013e32833a0918","article-title":"Factors associated with specific causes of death amongst HIV-positive individuals in the D:A:D Study","volume":"24","author":"Smith","year":"2010","journal-title":"AIDS"},{"key":"2021110300153271400_CIT0005","doi-asserted-by":"crossref","first-page":"1267","DOI":"10.1097\/QAD.0000000000002233","article-title":"Clinical significance of elevated liver transaminases in HIV-infected patients","volume":"33","author":"Cai","year":"2019","journal-title":"AIDS"},{"key":"2021110300153271400_CIT0006","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1097\/QAI.0000000000000992","article-title":"Poorly controlled HIV infection: an independent risk factor for liver fibrosis","volume":"72","author":"Kim","year":"2016","journal-title":"J Acquir Immune Defic Syndr"},{"key":"2021110300153271400_CIT0007","doi-asserted-by":"crossref","first-page":"502","DOI":"10.1086\/649922","article-title":"Incidence and risk factors for chronic elevation of alanine aminotransferase levels in HIV-infected persons without hepatitis B or C virus co-infection","volume":"50","author":"Kovari","year":"2010","journal-title":"Clin Infect Dis"},{"key":"2021110300153271400_CIT0008","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1002\/hep.26638","article-title":"Human immunodeficiency virus and liver disease forum 2012","volume":"59","author":"Sherman","year":"2014","journal-title":"Hepatology"},{"key":"2021110300153271400_CIT0009","doi-asserted-by":"crossref","first-page":"2500","DOI":"10.3748\/wjg.v17.i20.2500","article-title":"Mechanisms of alcohol-mediated hepatotoxicity in human-immunodeficiency-virus-infected patients","volume":"17","author":"Szabo","year":"2011","journal-title":"World J Gastroenterol"},{"key":"2021110300153271400_CIT0010","doi-asserted-by":"crossref","first-page":"1621","DOI":"10.1097\/QAD.0000000000001504","article-title":"Prevalence and risk factors of nonalcoholic fatty liver disease in HIV-monoinfection","volume":"31","author":"Maurice","year":"2017","journal-title":"AIDS"},{"key":"2021110300153271400_CIT0011","first-page":"75","article-title":"Fatty liver disease in persons with HIV infection","volume":"27","author":"Seth","year":"2019","journal-title":"Top Antivir Med"},{"key":"2021110300153271400_CIT0012","first-page":"1569","article-title":"Nonalcoholic steatohepatitis and hepatic fibrosis in HIV-1-monoinfected adults with elevated aminotransferase levels on antiretroviral therapy","volume":"60","author":"Morse","year":"2015","journal-title":"Clin Infect Dis"},{"key":"2021110300153271400_CIT0013","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1097\/QAD.0000000000001483","article-title":"Metabolic concerns in aging HIV-infected persons: from serum lipid phenotype to fatty liver","volume":"31","author":"Guaraldi","year":"2017","journal-title":"AIDS"},{"key":"2021110300153271400_CIT0014","doi-asserted-by":"crossref","first-page":"266","DOI":"10.1093\/infdis\/jiz096","article-title":"Increased prevalence of hepatic steatosis in young adults with lifelong HIV","volume":"220","author":"Aepfelbacher","year":"2019","journal-title":"J Infect Dis"},{"key":"2021110300153271400_CIT0015","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1111\/j.1468-1293.2010.00904.x","article-title":"Fatty liver disease is associated with underlying cardiovascular disease in HIV-infected persons","volume":"12","author":"Crum-Cianflone","year":"2011","journal-title":"HIV Med"},{"key":"2021110300153271400_CIT0016","doi-asserted-by":"crossref","first-page":"767","DOI":"10.1002\/hep.26741","article-title":"Fibrosis progression in human immunodeficiency virus\/hepatitis C virus coinfected adults: prospective analysis of 435 liver biopsy pairs","volume":"59","author":"Konerman","year":"2014","journal-title":"Hepatology"},{"key":"2021110300153271400_CIT0017","doi-asserted-by":"crossref","first-page":"746","DOI":"10.1038\/s41395-018-0409-9","article-title":"Spectrum of liver disease in hepatitis B virus (HBV) patients co-infected with human immunodeficiency virus (HIV): results of the HBV-HIV cohort study","volume":"114","author":"Sterling","year":"2019","journal-title":"Am J Gastroenterol"},{"key":"2021110300153271400_CIT0018","doi-asserted-by":"crossref","first-page":"643","DOI":"10.1080\/17474124.2019.1614913","article-title":"Nonalcoholic fatty liver disease and steatohepatitis in people living with HIV","volume":"13","author":"Squillace","year":"2019","journal-title":"Expert Rev Gastroenterol Hepatol"},{"key":"2021110300153271400_CIT0019","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1186\/s12876-019-0969-1","article-title":"Comparison of the prevalence, severity, and risk factors for hepatic steatosis in HIV-infected and uninfected people","volume":"19","author":"Torgersen","year":"2019","journal-title":"BMC Gastroenterol"},{"key":"2021110300153271400_CIT0020","doi-asserted-by":"crossref","first-page":"436","DOI":"10.1002\/hep.22665","article-title":"Liver damage underlying unexplained transaminase elevation in human immunodeficiency virus-1 mono-infected patients on antiretroviral therapy","volume":"49","author":"Ingiliz","year":"2009","journal-title":"Hepatology"},{"key":"2021110300153271400_CIT0021","doi-asserted-by":"crossref","first-page":"2310","DOI":"10.1016\/j.cgh.2019.01.027","article-title":"Prevalence and risk factors of significant fibrosis in patients with nonalcoholic fatty liver without Steatohepatitis","volume":"17","author":"Pelusi","year":"2019","journal-title":"Clin Gastroenterol Hepatol"},{"key":"2021110300153271400_CIT0022","first-page":"320","article-title":"Hepatitis B virus infection is not associated with fatty liver disease: evidence from a cohort study and functional analysis","volume":"19","author":"Wang","year":"2019","journal-title":"Mol Med Rep"},{"key":"2021110300153271400_CIT0023","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1111\/apt.15298","article-title":"Moderate to severe hepatic steatosis leads to overestimation of liver stiffness measurement in chronic hepatitis B patients without significant fibrosis","volume":"50","author":"Shen","year":"2019","journal-title":"Aliment Pharmacol Ther"},{"key":"2021110300153271400_CIT0024","doi-asserted-by":"crossref","first-page":"696","DOI":"10.1016\/0168-8278(95)80226-6","article-title":"Histological grading and staging of chronic hepatitis","volume":"22","author":"Ishak","year":"1995","journal-title":"J Hepatol"},{"key":"2021110300153271400_CIT0025","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1055\/s-0032-1306421","article-title":"Nonalcoholic fatty liver disease: pathologic patterns and biopsy evaluation in clinical research","volume":"32","author":"Kleiner","year":"2012","journal-title":"Semin Liver Dis"},{"key":"2021110300153271400_CIT0026","author":"National Institute on Alcohol Abuse and Alcoholism"},{"key":"2021110300153271400_CIT0027","doi-asserted-by":"crossref","first-page":"423","DOI":"10.15288\/jsa.1995.56.423","article-title":"The Alcohol Use Disorders Identification Test (AUDIT): validation of a screening instrument for use in medical settings","volume":"56","author":"Bohn","year":"1995","journal-title":"J Stud Alcohol"},{"key":"2021110300153271400_CIT0028","doi-asserted-by":"crossref","first-page":"1640","DOI":"10.1161\/CIRCULATIONAHA.109.192644","article-title":"Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity","volume":"120","author":"Alberti","year":"2009","journal-title":"Circulation"},{"key":"2021110300153271400_CIT0029","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1002\/hep.23670","article-title":"Comparison of surrogate and direct measurement of insulin resistance in chronic hepatitis C virus infection: impact of obesity and ethnicity","volume":"52","author":"Lam","year":"2010","journal-title":"Hepatology"},{"key":"2021110300153271400_CIT0030","doi-asserted-by":"crossref","first-page":"1311","DOI":"10.1002\/hep.25805","article-title":"Relationship between adipose tissue insulin resistance and liver histology in nonalcoholic steatohepatitis: a pioglitazone versus vitamin E versus placebo for the treatment of nondiabetic patients with nonalcoholic steatohepatitis trial follow-up study","volume":"56","author":"Bell","year":"2012","journal-title":"Hepatology"},{"key":"2021110300153271400_CIT0031","doi-asserted-by":"crossref","first-page":"571","DOI":"10.1097\/00126334-200308150-00004","article-title":"An objective lipodystrophy severity grading scale derived from the lipodystrophy case definition score","volume":"33","author":"Carr","year":"2003","journal-title":"J Acquir Immune Defic Syndr"},{"key":"2021110300153271400_CIT0032","doi-asserted-by":"crossref","first-page":"1012","DOI":"10.1016\/j.jhep.2019.06.031","article-title":"Crosstalk between adipose tissue insulin resistance and liver macrophages in non-alcoholic fatty liver disease","volume":"71","author":"Rosso","year":"2019","journal-title":"J Hepatol"},{"key":"2021110300153271400_CIT0033","doi-asserted-by":"crossref","first-page":"531","DOI":"10.1080\/17474124.2019.1599284","article-title":"Nonalcoholic fatty liver disease and nonalcoholic steatohepatitis in HIV infection: a metabolic approach of an infectious disease","volume":"13","author":"Coronel-Castillo","year":"2019","journal-title":"Expert Rev Gastroenterol Hepatol"},{"key":"2021110300153271400_CIT0034","doi-asserted-by":"crossref","first-page":"13306","DOI":"10.3748\/wjg.v20.i37.13306","article-title":"Nonalcoholic fatty liver disease and vascular disease: state-of-the-art","volume":"20","author":"Fargion","year":"2014","journal-title":"World J Gastroenterol"},{"key":"2021110300153271400_CIT0035","doi-asserted-by":"crossref","first-page":"1050","DOI":"10.1002\/hep4.1387","article-title":"Mortality risk detected by atherosclerotic cardiovascular disease score in patients with nonalcoholic fatty liver disease","volume":"3","author":"Golabi","year":"2019","journal-title":"Hepatol Commun"},{"key":"2021110300153271400_CIT0036","doi-asserted-by":"crossref","first-page":"224","DOI":"10.1097\/QAI.0000000000001996","article-title":"Factors associated with excess myocardial infarction risk in HIV-infected adults: a systematic review and meta-analysis","volume":"81","author":"Rao","year":"2019","journal-title":"J Acquir Immune Defic Syndr"},{"key":"2021110300153271400_CIT0037","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1186\/1476-511X-13-100","article-title":"Nonalcoholic steatohepatitis is associated with an atherogenic lipoprotein subfraction profile","volume":"13","author":"Corey","year":"2014","journal-title":"Lipids Health Dis"},{"key":"2021110300153271400_CIT0038","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1097\/QAD.0b013e328340fde2","article-title":"Clinical and virological outcomes in HIV-infected patients with chronic hepatitis B on long-term nucleos(t)ide analogues","volume":"25","author":"Mart\u00edn-Carbonero","year":"2011","journal-title":"AIDS"}],"container-title":["Clinical Infectious Diseases"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/cid\/advance-article-pdf\/doi\/10.1093\/cid\/ciaa1303\/34474664\/ciaa1303.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/cid\/article-pdf\/73\/9\/e3275\/41060720\/ciaa1303.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/cid\/article-pdf\/73\/9\/e3275\/41060720\/ciaa1303.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,11,3]],"date-time":"2021-11-03T00:17:43Z","timestamp":1635898663000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/cid\/article\/73\/9\/e3275\/5900012"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,9,1]]},"references-count":38,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2020,9,1]]},"published-print":{"date-parts":[[2021,11,2]]}},"URL":"https:\/\/doi.org\/10.1093\/cid\/ciaa1303","relation":{},"ISSN":["1058-4838","1537-6591"],"issn-type":[{"value":"1058-4838","type":"print"},{"value":"1537-6591","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2021,11,1]]},"published":{"date-parts":[[2020,9,1]]}}}