Digestive Disease Interventions 2020; 04(02): 223-234
DOI: 10.1055/s-0040-1713369
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Both Alcoholic and Nonalcoholic Steatohepatitis Is an Emerging Indication for Liver Transplantation in the United States

1   University Transplant Center, UT Health San Antonio, San Antonio, Texas
,
2   Department of Gastroenterology and Hepatology, Cleveland Clinic Foundation, Cleveland, Ohio
,
Eric Lawitz
1   University Transplant Center, UT Health San Antonio, San Antonio, Texas
3   Texas Liver Institute, San Antonio, Texas
,
Kris V. Kowdley
4   Liver Care Network and Organ Care Research, Swedish Medical Center, Seattle, Washington
,
Glenn Halff
1   University Transplant Center, UT Health San Antonio, San Antonio, Texas
,
Francisco Cigarroa
1   University Transplant Center, UT Health San Antonio, San Antonio, Texas
,
Tarunjeet Klair
1   University Transplant Center, UT Health San Antonio, San Antonio, Texas
,
Rocio Lopez
2   Department of Gastroenterology and Hepatology, Cleveland Clinic Foundation, Cleveland, Ohio
,
Mazen Noureddin
5   Department of Gastroenterology and Hepatology, Cedars-Sinai Medical Center, Los Angeles, California
,
Naim Alkhouri
1   University Transplant Center, UT Health San Antonio, San Antonio, Texas
3   Texas Liver Institute, San Antonio, Texas
› Author Affiliations
Funding None.
Further Information

Publication History

21 January 2020

24 April 2020

Publication Date:
03 July 2020 (online)

Abstract

Background Nonalcoholic steatohepatitis (NASH) and alcoholic liver disease (ALD) are now the most common indications for liver transplantation (LT) in the United States. A subset of patients have both alcoholic and nonalcoholic steatohepatitis (BASH). This study characterizes patients with BASH requiring LT and assesses changes in the prevalence of BASH as an indication for LT.

Methods The United Network for Organ Sharing database was analyzed for all patients ≥ 18 years of age who received their first deceased donor LT from 2002 to 2016 for ALD, NASH, or BASH. Baseline demographics, clinical parameters, and LT outcomes were compared between groups.

Results Since 2002, 85,448 patients underwent LT:15,327 had ALD, 9,971 had NASH, and 2,779 had BASH. The prevalence of BASH as an indication for LT increased from 0.5% in 2002 to 5% in 2016. Compared with patients with NASH, those with BASH were significantly more likely to be male (85.6 vs. 57%), younger (mean 56.4 vs. 58.6 years), and Hispanic (22.2 vs. 13.6%) (p < 0.001 for all). While indication for transplant was not significantly associated with transplant outcomes on multivariable analysis, patient and graft survival curves do differ significantly by indication for transplant, with worse outcomes for patients with BASH (patient survival at 5 years: NASH 78.1%, ALD 77.2%, BASH 73.5%, p = 0.013; graft survival at 5 years: NASH 75.3%, ALD 74.0%, BASH 70.8%, p = 0.046).

Conclusions BASH is a rising indication for LT, especially for Hispanic males, due to the increasing prevalence of ALD and NASH in the United States.

Supporting Information

None.


 
  • References

  • 1 Hales CM, Carroll MD, Fryar CD, Ogden CL. Prevalence of obesity among adults and youth: United States, 2015-2016. NCHS Data Brief 2017; ; ( (288) 1-8
  • 2 Dwyer-Lindgren L, Flaxman AD, Ng M, Hansen GM, Murray CJ, Mokdad AH. Drinking patterns in US counties from 2002 to 2012. Am J Public Health 2015; 105 (06) 1120-1127
  • 3 Rinella ME, Loomba R, Caldwell SH. , et al. Controversies in the diagnosis and management of NAFLD and NASH. Gastroenterol Hepatol (N Y) 2014; 10 (04) 219-227
  • 4 Khoudari G, Singh A, Noureddin M. , et al. Characterization of patients with both alcoholic and nonalcoholic fatty liver disease in a large United States cohort. World J Hepatol 2019; 11 (10) 710-718
  • 5 Ong JP, Elariny H, Collantes R. , et al. Predictors of nonalcoholic steatohepatitis and advanced fibrosis in morbidly obese patients. Obes Surg 2005; 15 (03) 310-315
  • 6 Kalbfleisch JD, Prentice RL. The Statistical Analysis of Failure Time Data. 2nd ed. Hoboken, NJ: Wiley; 2002
  • 7 Fryar CD, Carroll MD, Ogden CL. Prevalence of Overweight, Obesity, and Extreme Obesity among Adults Aged 20 and Over: United States, 1960–1962 through 2013–2014. Hyattsville, MD: National Center for Health Statistics; 2016
  • 8 Flegal KM, Kruszon-Moran D, Carroll MD, Fryar CD, Ogden CL. Trends in Obesity Among Adults in the United States, 2005 to 2014. JAMA 2016; 315 (21) 2284-2291
  • 9 Aguilar M, Bhuket T, Torres S, Liu B, Wong RJ. Prevalence of the metabolic syndrome in the United States, 2003-2012. JAMA 2015; 313 (19) 1973-1974
  • 10 Estes C, Razavi H, Loomba R, Younossi Z, Sanyal AJ. Modeling the epidemic of nonalcoholic fatty liver disease demonstrates an exponential increase in burden of disease. Hepatology 2018; 67 (01) 123-133
  • 11 Bellentani S, Saccoccio G, Costa G. , et al; The Dionysos Study Group. Drinking habits as cofactors of risk for alcohol induced liver damage. Gut 1997; 41 (06) 845-850
  • 12 Grant BF, Chou SP, Saha TD. , et al. Prevalence of 12-month alcohol use, high-risk drinking, and DSM-IV alcohol use disorder in the United States, 2001-2002 to 2012-2013: results from the National Epidemiologic Survey on Alcohol and Related Conditions. JAMA Psychiatry 2017; 74 (09) 911-923
  • 13 Tapper EB, Parikh ND. Mortality due to cirrhosis and liver cancer in the United States, 1999-2016: observational study. BMJ 2018; 362: k2817
  • 14 Stepanova M, Wai H, Saab S, Mishra A, Venkatesan C, Younossi ZM. The portrait of an adult liver transplant recipient in the United States from 1987 to 2013. JAMA Intern Med 2014; 174 (08) 1407-1409
  • 15 Hart CL, Morrison DS, Batty GD, Mitchell RJ, Davey Smith G. Effect of body mass index and alcohol consumption on liver disease: analysis of data from two prospective cohort studies. BMJ 2010; 340: c1240
  • 16 Raynard B, Balian A, Fallik D. , et al. Risk factors of fibrosis in alcohol-induced liver disease. Hepatology 2002; 35 (03) 635-638
  • 17 Naveau S, Giraud V, Borotto E, Aubert A, Capron F, Chaput JC. Excess weight risk factor for alcoholic liver disease. Hepatology 1997; 25 (01) 108-111
  • 18 Mehta M, Satsangi S, Duseja A, Taneja S, Dhiman RK, Chawla Y. Can alcoholic liver disease and nonalcoholic fatty liver disease co-exist?. J Clin Exp Hepatol 2017; 7 (02) 121-126
  • 19 Loomba R, Yang HI, Su J. , et al. Synergism between obesity and alcohol in increasing the risk of hepatocellular carcinoma: a prospective cohort study. Am J Epidemiol 2013; 177 (04) 333-342
  • 20 Kimura T, Tanaka N, Fujimori N. , et al. Mild drinking habit is a risk factor for hepatocarcinogenesis in non-alcoholic fatty liver disease with advanced fibrosis. World J Gastroenterol 2018; 24 (13) 1440-1450
  • 21 Fleischman MW, Budoff M, Zeb I, Li D, Foster T. NAFLD prevalence differs among hispanic subgroups: the Multi-Ethnic Study of Atherosclerosis. World J Gastroenterol 2014; 20 (17) 4987-4993
  • 22 Williams CD, Stengel J, Asike MI. , et al. Prevalence of nonalcoholic fatty liver disease and nonalcoholic steatohepatitis among a largely middle-aged population utilizing ultrasound and liver biopsy: a prospective study. Gastroenterology 2011; 140 (01) 124-131
  • 23 Desai AP, Mohan P, Roubal AM, Bettencourt R, Loomba R. Geographic variability in liver disease-related mortality rates in the United States. Am J Med 2018; 131 (07) 728-734
  • 24 Jiao J, Watt GP, Lee M. , et al. Cirrhosis and advanced fibrosis in Hispanics in Texas: the dominant contribution of central obesity. PLoS One 2016; 11 (03) e0150978
  • 25 Chang SH, Wang M, Liu X. , et al. Racial/ethnic disparities in access and outcomes of simultaneous liver-kidney transplant among liver transplant candidates with renal dysfunction in the United States. Transplantation 2019; 103 (08) 1663-1674
  • 26 Kardashian AA, Dodge JL, Roberts J, Brandman D. Weighing the risks: morbid obesity and diabetes are associated with increased risk of death on the liver transplant waiting list. Liver Int 2018; 38 (03) 553-563
  • 27 Setiawan VW, Hernandez BY, Lu SC. , et al. Diabetes and racial/ethnic differences in hepatocellular carcinoma risk: the multiethnic cohort. J Natl Cancer Inst 2014; 106 (12) dju326
  • 28 Sánchez-Jiménez BA, Brizuela-Alcántara D, Ramos-Ostos MH, Alva-López LF, Uribe-Esquivel M, Chávez-Tapia NC. Both alcoholic and non-alcoholic steatohepatitis association with cardiovascular risk and liver fibrosis. Alcohol 2018; 69: 63-67
  • 29 Portillo-Sanchez P, Bril F, Maximos M. , et al. High prevalence of nonalcoholic fatty liver disease in patients with type 2 diabetes mellitus and normal plasma aminotransferase levels. J Clin Endocrinol Metab 2015; 100 (06) 2231-2238
  • 30 Kim SH, Lee JW, Hwang HJ. Associations between combinations of body mass index plus non-alcoholic fatty liver disease and diabetes mellitus among Korean adults. Asia Pac J Clin Nutr 2011; 20 (01) 14-20
  • 31 Jaskiewicz K, Rzepko R, Sledzinski Z. Fibrogenesis in fatty liver associated with obesity and diabetes mellitus type 2. Dig Dis Sci 2008; 53 (03) 785-788