Introduction
Autoimmune liver diseases (AILDs) such as autoimmune hepatitis (AIH), primary biliary cholangitis (PBC), and primary sclerosing cholangitis (PSC) are chronic inflammatory disorders affecting the hepatobiliary system. These diseases account for a small percentage of liver transplants (LT) in the United States, with survival outcomes influenced by various factors including disease burden, medical comorbidities, and socioeconomic variables.
Study Objective
This study aims to analyze the impact of socioeconomic factors on liver transplant outcomes in patients with AILDs, focusing on waitlist removal, post-LT patient survival, and graft survival.
Materials and Methods
Using the United Network for Organ Sharing (UNOS) database, we identified 13,702 patients with AILDs listed for LT between 2002 and 2021. We performed a stepwise multivariate analysis adjusting for transplant recipient gender, race, diabetes mellitus, model for end-stage liver disease (MELD) score, and additional social determinants including education, reliance on public insurance, employment status, and U.S. citizenship.
Results
Our study found that lack of college education and reliance on public insurance increased the risk of waitlist removal and negatively influenced post-LT patient and graft survival. Not working for income had the greatest detrimental impact on both patient and graft survival. Interestingly, not having U.S. citizenship did not affect survival outcomes in AILD patients.
Waitlist Survival
Patients with PBC had a higher risk of waitlist removal due to death or clinical deterioration compared to AIH and PSC patients. Socioeconomic factors such as Hispanic race, lack of college education, public insurance, non-U.S. citizenship, and not working for income were significantly associated with an increased risk of waitlist removal.
Post-Transplant Patient and Graft Survival
Post-transplant patient survival rates at 5 and 10 years were significantly better for those working for income, having private insurance, and possessing a college education. In contrast, Black/African American race, lack of college education, public insurance, and not working for income had a detrimental impact on post-LT patient survival. Similarly, these socioeconomic factors also negatively affected graft survival.
Discussion
Our findings highlight the significant impact of socioeconomic factors on liver transplant outcomes in patients with AILDs. Lack of education and reliance on public insurance were associated with poorer outcomes, likely due to limited access to healthcare resources and financial constraints. The absence of income had the most substantial negative impact on both patient and graft survival, underscoring the importance of addressing these disparities to improve transplant outcomes.
Conclusion
This study underscores the need for tailored pre- and post-transplant care strategies to address the healthcare barriers faced by underserved patients. Future research should focus on developing interventions to mitigate these disparities and enhance the overall success of liver transplants in patients with AILDs.
Authors
Leandro Sierra, Ana Marenco-Flores, Romelia Barba, Daniela Goyes, Bryan Ferrigno, Wilfor Diaz, Esli Medina-Morales, Behnam Saberi, Vilas R Patwardhan, Alan Bonder
References
[1] Gumm A, Perez-Atayde A, Wehrman A. Posttransplant considerations in autoimmune liver disease: recurrence of disease and de novo. Clin Liver Dis (Hoboken) 2022;20(4):130–5.
[2] Kwong AJ, Ebel NH, Kim WR, Lake JR, Smith JM, Schladt DP, et al. OPTN/SRTR 2020 Annual data report: liver. Am J Transplant 2022;22:204–309.
[3] Huang DC, Fricker ZP, Alqahtani S, Tamim H, Saberi B, Bonder A. The influence of equitable access policies and socioeconomic factors on post-liver transplant survival. EClinicalMedicine 2021;41:101137.
[4] Nephew LD, Serper M. Racial, gender, and socioeconomic disparities in liver transplantation. Liver Transpl 2021;27(6):900–12.
[5] Mazumder NR, Simpson D, Atiemo K, Jackson K, Zhao L, Daud A, et al. Black patients with cirrhosis have higher mortality and lower transplant rates: results from a metropolitan cohort study. Hepatology 2021;74(2):926–36.
[6] Levy C, Naik J, Giordano C, Mandalia A, O’Brien C, Bhamidimarri KR, et al. Hispanics with primary biliary cirrhosis are more likely to have features of autoimmune hepatitis and reduced response to ursodeoxycholic acid than non-Hispanics. Clin Gastroenterol Hepatol 2014;12(8):1398–405.
[7] Are VS, Vilar-Gomez E, Gromski MA, Akisik F, Lammert C, Ghabril M, et al. Racial differences in primary sclerosing cholangitis mortality is associated with community socioeconomic status. Liver Int 2021;41(11):2703–11.
[8] Kardashian A, Serper M, Terrault N, Nephew LD. Health disparities in chronic liver disease. Hepatology 2023;77(4):1382–403.
[9] Goyes D, Danford CJ, Nsubuga JP, Bonder A. Waitlist mortality and transplant free survival in Hispanic patients listed for liver transplant using the UNOS database. Ann Hepatol 2021;23:100304.
[10] Zhou K, Dodge JL, Xu E, Emamaullee J, Kahn JA. Excess liver transplant waitlist mortality for patients with primary biliary cholangitis under MELD-Na allocation. Clin Transplant 2022;36(2):e14527.
[11] Singal AK, Fang X, Kaif M, Hasanin M, Mcguire BM, Kuo YF, et al. Primary biliary cirrhosis has high wait-list mortality among patients listed for liver transplantation. Transpl Int 2017;30(5):454–62.
[12] Xu CQ, Yao F, Mohamad Y, Wong R, Kent D, Seetharaman S, et al. Evaluating the associations between the liver frailty index and karnofsky performance status with waitlist mortality. Transpl Direct 2021;7(2):e651.
[13] Trivedi HD, Danford CJ, Goyes D, Bonder A. Osteoporosis in primary biliary cholangitis: prevalence, impact and management challenges. Clin Exp Gastroenterol 2020;13.
[14] Danford CJ, Trivedi HD, Papamichael K, Tapper EB, Bonder A. Osteoporosis in primary biliary cholangitis. World J Gastroenterol 2018;24(31):3513–20.
[15] Inoue T, Maeda K, Satake S, Matsui Y, Arai H. Osteosarcopenia, the co-existence of osteoporosis and sarcopenia, is associated with social frailty in older adults. Aging Clin Exp Res 2022;34(3):535–43.
[16] Suri JS, Danford CJ, Patwardhan V, Bonder A. Mortality on the UNOS waitlist for patients with autoimmune liver disease. J Clin Med 2020;9(2):319.
[17] Jacob DA, Neumann UP, Bahra M, Klupp J, Puhl G, Neuhaus R, et al. Long-term follow-up after recurrence of primary biliary cirrhosis after liver transplantation in 100 patients. Clin Transplant 2006;20(2):211–20.
[18] Eckhoff DE, McGuire BM, Young CJ, Sellers MT, Frenette LR, Hudson SL, et al. Race: a critical factor in organ donation, patient referral and selection, and orthotopic liver transplantation? Liver Transpl Surg 1998;4(6):499–505.
[19] Gutin L, Yao F, Dodge JL, Grab J, Mehta N. Comparison of liver transplant wait-list outcomes among patients with hepatocellular carcinoma with public vs private medical insurance. JAMA Netw Open 2019;2(8):e1910326.
[20] Huang DC, Yu RL, Alqahtani S, Tamim H, Saberi B, Bonder A. Racial, ethnic, and socioeconomic disparities impact post-liver transplant survival in patients with hepatocellular carcinoma. Ann Hepatol 2023:101127.
[21] Sierra L, Barba R, Ferrigno B, Goyes D, Diaz W, Patwardhan VR, et al. Living-donor liver transplant and improved post-transplant survival in patients with primary sclerosing cholangitis. J Clin Med 2023;12(8):2807.
[22] Durand F, Levitsky J, Cauchy F, Gilgenkrantz H, Soubrane O, Francoz C. Age and liver transplantation. J Hepatol 2019;70(4):745–58.
[23] Yoo HY, Thuluvath PJ. Outcome of liver transplantation in adult recipients: influence of neighborhood income, education, and insurance. Liver Transpl 2004;10(2):235–43.
[24] Schwartz A, Schiano T, Kim-Schluger L, Florman S. Geographic disparity: the dilemma of lower socioeconomic status, multiple listing, and death on the liver transplant waiting list. Clin Transplant 2014;28(10):1075–9.
[25] Ochoa-Allemant P, Ezaz G, Trivedi HD, Sanchez-Fernandez L, Bonder A. Long-term outcomes after liver transplantation in the Hispanic population. Liver Int 2019.
[26] Webb GJ, Rana A, Hodson J, Akhtar MZ, Ferguson JW, Neuberger JM, et al. Twenty-year comparative analysis of patients with autoimmune liver diseases on transplant waitlists. Clin Gastroenterol Hepatol 2018;16(2):278–87 e7.
[27] Kemmer N. Ethnic disparities in liver transplantation. Gastroenterol Hepatol (N Y) 2011;7(5):302–7.
[28] Nsubuga JP, Goyes D, Trivedi HD, Medina-Morales E, Patwardhan V, Bonder A. Waitlist mortality and posttransplant outcomes in African Americans with autoimmune liver diseases. J Transplant 2021;2021:6692049.
[29] Wong LL, Hernandez BY, Albright CL. Socioeconomic factors affect disparities in access to liver transplant for hepatocellular cancer. J Transplant 2012;2012:870659.
[30] Kim WR, Mannalithara A, Heimbach JK, Kamath PS, Asrani SK, Biggins SW, et al. MELD 3.0: the model for end-stage liver disease updated for the modern era. Gastroenterology 2021;161(6):1887–95 e4.