Risk of New-Onset Liver Injuries Due to COVID-19 in Preexisting Hepatic Conditions—Review of the Literature
Abstract
:1. Introduction
2. Materials and Methods
3. COVID-19 and Cirrhosis
4. COVID-19 and Cholangitis
5. COVID-19 and NAFLD (Non-Alcoholic Fatty Liver Disease)
6. COVID-19 and Hepatitis B and C Infection
7. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Sanyaolu, A.; Okorie, C.; Marinkovic, A.; Patidar, R.; Younis, K.; Desai, P.; Hosein, Z.; Padda, I.; Mangat, J.; Altaf, M. Comorbidity and its Impact on Patients with COVID-19. SN Compr. Clin. Med. 2020, 2, 1069–1076. [Google Scholar] [CrossRef] [PubMed]
- WHO Coronavirus (COVID-19) Dashboard. Available online: https://covid19.who.int (accessed on 9 October 2022).
- Heydari, K.; Lotfi, P.; Shadmehri, N.; Yousefi, M.; Raei, M.; Houshmand, P.; Zahedi, M.; Alizadeh-Navaei, R.; Bathaeian, S.; Rismantab, S. Clinical and Paraclinical Characteristics of COVID-19 patients: A Systematic Review and Meta-Analysis. Tabari Biomed. Stud. Res. J. 2022, 4, 30–47. [Google Scholar] [CrossRef]
- Zahedi, M.; Yousefi, M.; Abounoori, M.; Malekan, M.; Tajik, F.; Heydari, K.; Mortazavi, P.; Ghahramani, S.; Ghazaeian, M.; Sheydaee, F.; et al. The Interrelationship between Liver Function Test and the Coronavirus Disease 2019: A Systematic Review and Meta-Analysis. Iran. J. Med. Sci. 2021, 46, 237–255. [Google Scholar] [CrossRef] [PubMed]
- Cheemerla, S.; Balakrishnan, M. Global Epidemiology of Chronic Liver Disease. Clin. Liver Dis. 2021, 17, 365–370. [Google Scholar] [CrossRef] [PubMed]
- Global Progress Report on HIV, Viral Hepatitis and Sexually Transmitted Infections. 2021. Available online: https://www.who.int/publications-detail-redirect/9789240027077 (accessed on 9 October 2022).
- Hepatitis, C. Available online: https://www.who.int/news-room/fact-sheets/detail/hepatitis-c (accessed on 9 October 2022).
- Vernon, G.; Baranova, A.; Younossi, Z.M. Systematic review: The epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults. Aliment. Pharmacol. Ther. 2011, 34, 274–285. [Google Scholar] [CrossRef] [PubMed]
- Chen, T.; Wu, D.; Chen, H.; Yan, W.; Yang, D.; Chen, G.; Ma, K.; Xu, D.; Yu, H.; Wang, H.; et al. Clinical characteristics of 113 deceased patients with coronavirus disease 2019: Retrospective study. BMJ 2020, 368, m1091. [Google Scholar] [CrossRef] [Green Version]
- Tian, S.; Xiong, Y.; Liu, H.; Niu, L.; Guo, J.; Liao, M.; Xiao, S.-Y. Pathological study of the 2019 novel coronavirus disease (COVID-19) through postmortem core biopsies. Mod. Pathol. 2020, 33, 1007–1014. [Google Scholar] [CrossRef] [Green Version]
- Malik, P.; Patel, K.; Akrmah, M.; Donthi, D.; Patel, U.; Khader, S.N.; Asiry, S. COVID-19: A Disease with a Potpourri of Histopathologic Findings-a Literature Review and Comparison to the Closely Related SARS and MERS. SN Compr. Clin. Med. 2021, 3, 2407–2434. [Google Scholar] [CrossRef]
- Bradley, B.T.; Maioli, H.; Johnston, R.; Chaudhry, I.; Fink, S.L.; Xu, H.; Najafian, B.; Deutsch, G.; Lacy, J.M.; Williams, T.; et al. Histopathology and ultrastructural findings of fatal COVID-19 infections in Washington State: A case series. Lancet 2020, 396, 320–332. [Google Scholar] [CrossRef]
- Varga, Z.; Flammer, A.J.; Steiger, P.; Haberecker, M.; Andermatt, R.; Zinkernagel, A.S.; Mehra, M.R.; Schuepbach, R.A.; Ruschitzka, F.; Moch, H. Endothelial cell infection and endotheliitis in COVID-19. Lancet 2020, 395, 1417–1418. [Google Scholar] [CrossRef]
- Wang, Y.; Liu, S.; Liu, H.; Li, W.; Lin, F.; Jiang, L.; Li, X.; Xu, P.; Zhang, L.; Zhao, L.; et al. SARS-CoV-2 infection of the liver directly contributes to hepatic impairment in patients with COVID-19. J. Hepatol. 2020, 73, 807–816. [Google Scholar] [CrossRef] [PubMed]
- Kaltschmidt, B.; Fitzek, A.D.E.; Schaedler, J.; Förster, C.; Kaltschmidt, C.; Hansen, T.; Steinfurth, F.; Windmöller, B.A.; Pilger, C.; Kong, C.; et al. Hepatic Vasculopathy and Regenerative Responses of the Liver in Fatal Cases of COVID-19. Clin. Gastroenterol. Hepatol. 2021, 19, 1726–1729.e3. [Google Scholar] [CrossRef] [PubMed]
- Cheung, C.C.L.; Goh, D.; Lim, X.; Tien, T.Z.; Lim, J.C.T.; Lee, J.N.; Tan, B.; Tay, Z.E.A.; Wan, W.Y.; Chen, E.X.; et al. Residual SARS-CoV-2 viral antigens detected in GI and hepatic tissues from five recovered patients with COVID-19. Gut 2022, 71, 226–229. [Google Scholar] [CrossRef] [PubMed]
- Balaphas, A.; Gkoufa, K.; Meyer, J.; Peloso, A.; Bornand, A.; McKee, T.A.; Toso, C.; Popeskou, S.-G. COVID-19 can mimic acute cholecystitis and is associated with the presence of viral RNA in the gallbladder wall. J. Hepatol. 2020, 73, 1566–1568. [Google Scholar] [CrossRef]
- Delorey, T.M.; Ziegler, C.G.K.; Heimberg, G.; Normand, R.; Yang, Y.; Segerstolpe, Å.; Abbondanza, D.; Fleming, S.J.; Subramanian, A.; Montoro, D.T.; et al. COVID-19 tissue atlases reveal SARS-CoV-2 pathology and cellular targets. Nature 2021, 595, 107–113. [Google Scholar] [CrossRef]
- Pedersen, S.F.; Ho, Y.-C. SARS-CoV-2: A storm is raging. J. Clin. Investig. 2020, 130, 2202–2205. [Google Scholar] [CrossRef]
- Pirola, C.J.; Sookoian, S. SARS-CoV-2 virus and liver expression of host receptors: Putative mechanisms of liver involvement in COVID-19. Liver Int. 2020, 40, 2038–2040. [Google Scholar] [CrossRef]
- Senapati, S.; Banerjee, P.; Bhagavatula, S.; Kushwaha, P.P.; Kumar, S. Contributions of human ACE2 and TMPRSS2 in determining host-pathogen interaction of COVID-19. J. Genet. 2021, 100, 12. [Google Scholar] [CrossRef]
- Jackson, C.B.; Farzan, M.; Chen, B.; Choe, H. Mechanisms of SARS-CoV-2 entry into cells. Nat. Rev. Mol. Cell Biol. 2022, 23, 3–20. [Google Scholar] [CrossRef]
- Spearman, C.W.; Aghemo, A.; Valenti, L.; Sonderup, M.W. COVID-19 and the liver: A 2021 update. Liver Int. 2021, 41, 1988–1998. [Google Scholar] [CrossRef]
- Yan, B.; Freiwald, T.; Chauss, D.; Wang, L.; West, E.; Mirabelli, C.; Zhang, C.J.; Nichols, E.-M.; Malik, N.; Gregory, R.; et al. SARS-CoV-2 drives JAK1/2-dependent local complement hyperactivation. Sci. Immunol. 2021, 6, eabg0833. [Google Scholar] [CrossRef]
- Effenberger, M.; Grander, C.; Grabherr, F.; Griesmacher, A.; Ploner, T.; Hartig, F.; Bellmann-Weiler, R.; Joannidis, M.; Zoller, H.; Weiss, G.; et al. Systemic inflammation as fuel for acute liver injury in COVID-19. Dig. Liver Dis. 2021, 53, 158–165. [Google Scholar] [CrossRef]
- Merad, M.; Blish, C.A.; Sallusto, F.; Iwasaki, A. The immunology and immunopathology of COVID-19. Science 2022, 375, 1122–1127. [Google Scholar] [CrossRef]
- Ekpanyapong, S.; Bunchorntavakul, C.; Reddy, K.R. COVID-19 and the Liver: Lessons Learnt from the EAST and the WEST, A Year Later. J. Viral Hepat. 2022, 29, 4–20. [Google Scholar] [CrossRef]
- Li, Y.; Xiao, S. Hepatic involvement in COVID-19 patients: Pathology, pathogenesis, and clinical implications. J. Med. Virol. 2020, 92, 1491–1494. [Google Scholar] [CrossRef]
- Amin, M. COVID-19 and the liver: Overview. Eur. J. Gastroenterol. Hepatol. 2021, 33, 309–311. [Google Scholar] [CrossRef]
- Eastin, C.; Eastin, T. Clinical Characteristics of Coronavirus Disease 2019 in China. J. Emerg. Med. 2020, 58, 711–712. [Google Scholar] [CrossRef]
- Huang, C.; Wang, Y.; Li, X.; Ren, L.; Zhao, J.; Hu, Y.; Zhang, L.; Fan, G.; Xu, J.; Gu, X.; et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 2020, 395, 497–506. [Google Scholar] [CrossRef] [Green Version]
- Wu, Z.; McGoogan, J.M. Characteristics of and Important Lessons From the Coronavirus Disease 2019 (COVID-19) Outbreak in China: Summary of a Report of 72 314 Cases From the Chinese Center for Disease Control and Prevention. JAMA 2020, 323, 1239–1242. [Google Scholar] [CrossRef]
- Huang, J.; Cheng, A.; Kumar, R.; Fang, Y.; Chen, G.; Zhu, Y.; Lin, S. Hypoalbuminemia predicts the outcome of COVID-19 independent of age and co-morbidity. J. Med. Virol. 2020, 92, 2152–2158. [Google Scholar] [CrossRef]
- Xu, Y.; Yang, H.; Wang, J.; Li, X.; Xue, C.; Niu, C.; Liao, P. Serum Albumin Levels are a Predictor of COVID-19 Patient Prognosis: Evidence from a Single Cohort in Chongqing, China. Int. J. Gen. Med. 2021, 14, 2785–2797. [Google Scholar] [CrossRef] [PubMed]
- Ambade, V. Biochemical rationale for hypoalbuminemia in COVID-19 patients. J. Med. Virol. 2021, 93, 1207–1209. [Google Scholar] [CrossRef] [PubMed]
- Johnson, A.; Fatemi, R.; Winlow, W. SARS-CoV-2 Bound Human Serum Albumin and Systemic Septic Shock. Front. Cardiovasc. Med. 2020, 7, 153. [Google Scholar] [CrossRef] [PubMed]
- Liu, J.; Yu, C.; Yang, Q.; Yuan, X.; Yang, F.; Li, P.; Chen, G.; Liang, W.; Yang, Y. The clinical implication of gamma-glutamyl transpeptidase in COVID-19. Liver Res. 2021, 5, 209–216. [Google Scholar] [CrossRef]
- Shao, T.; Tong, Y.; Lu, S.; Jeyarajan, A.J.; Su, F.; Dai, J.; Shi, J.; Huang, J.; Hu, C.; Wu, L.; et al. Gamma-Glutamyltransferase Elevation Is Frequent in Patients With COVID-19: A Clinical Epidemiologic Study. Hepatol. Commun. 2020, 4, 1744–1750. [Google Scholar] [CrossRef]
- Zhu, X.; Wang, J.; Du, J.; Chen, S.; Chen, S.; Li, J.; Shen, B. Changes in Serum Liver Function for Patients with COVID-19: A 1-Year Follow-Up Study. Infect. Drug Resist. 2022, 15, 1857–1870. [Google Scholar] [CrossRef]
- Sharma, A.; Nagalli, S. Chronic Liver Disease; StatPearls Publishing: Treasure Island, FL, USA, 2022. [Google Scholar]
- Martinez, M.A.; Franco, S. Impact of COVID-19 in Liver Disease Progression. Hepatol. Commun. 2021, 5, 1138–1150. [Google Scholar] [CrossRef]
- Marjot, T.; Webb, G.J.; Barritt, A.S.; Moon, A.M.; Stamataki, Z.; Wong, V.W.; Barnes, E. COVID-19 and liver disease: Mechanistic and clinical perspectives. Nat. Rev. Gastroenterol. Hepatol. 2021, 18, 348–364. [Google Scholar] [CrossRef]
- Portincasa, P.; Krawczyk, M.; Machill, A.; Lammert, F.; Di Ciaula, A. Hepatic consequences of COVID-19 infection. Lapping or biting? Eur. J. Intern. Med. 2020, 77, 18–24. [Google Scholar] [CrossRef]
- Marjot, T.; Moon, A.M.; Cook, J.A.; Abd-Elsalam, S.; Aloman, C.; Armstrong, M.J.; Pose, E.; Brenner, E.J.; Cargill, T.; Catana, M.-A.; et al. Outcomes following SARS-CoV-2 infection in patients with chronic liver disease: An international registry study. J. Hepatol. 2021, 74, 567–577. [Google Scholar] [CrossRef]
- Moon, A.M.; Webb, G.J.; Aloman, C.; Armstrong, M.J.; Cargill, T.; Dhanasekaran, R.; Genescà, J.; Gill, U.S.; James, T.W.; Jones, P.D.; et al. High mortality rates for SARS-CoV-2 infection in patients with pre-existing chronic liver disease and cirrhosis: Preliminary results from an international registry. J. Hepatol. 2020, 73, 705–708. [Google Scholar] [CrossRef] [PubMed]
- Sarin, S.K.; Choudhury, A.; Lau, G.K.; Zheng, M.-H.; Ji, D.; Abd-Elsalam, S.; Hwang, J.; Qi, X.; Cua, I.H.; Suh, J.I.; et al. APASL COVID Task Force, APASL COVID Liver Injury Spectrum Study (APCOLIS Study-NCT 04345640). Pre-existing liver disease is associated with poor outcome in patients with SARS CoV2 infection; The APCOLIS Study (APASL COVID-19 Liver Injury Spectrum Study). Hepatol. Int. 2020, 14, 690–700. [Google Scholar] [CrossRef] [PubMed]
- Bajaj, J.S.; Garcia-Tsao, G.; Biggins, S.W.; Kamath, P.S.; Wong, F.; McGeorge, S.; Shaw, J.; Pearson, M.; Chew, M.; Fagan, A.; et al. Comparison of mortality risk in patients with cirrhosis and COVID-19 compared with patients with cirrhosis alone and COVID-19 alone: Multicentre matched cohort. Gut 2021, 70, 531–536. [Google Scholar] [CrossRef] [PubMed]
- Iavarone, M.; D’Ambrosio, R.; Soria, A.; Triolo, M.; Pugliese, N.; Del Poggio, P.; Perricone, G.; Massironi, S.; Spinetti, A.; Buscarini, E.; et al. High rates of 30-day mortality in patients with cirrhosis and COVID-19. J. Hepatol. 2020, 73, 1063–1071. [Google Scholar] [CrossRef]
- Kim, D.; Adeniji, N.; Latt, N.; Kumar, S.; Bloom, P.P.; Aby, E.S.; Perumalswami, P.; Roytman, M.; Li, M.; Vogel, A.S.; et al. Predictors of Outcomes of COVID-19 in Patients With Chronic Liver Disease: US Multi-center Study. Clin. Gastroenterol. Hepatol. 2021, 19, 1469–1479.e19. [Google Scholar] [CrossRef]
- Mallet, V.; Beeker, N.; Bouam, S.; Sogni, P.; Pol, S. Demosthenes research group Prognosis of French COVID-19 patients with chronic liver disease: A national retrospective cohort study for 2020. J. Hepatol. 2021, 75, 848–855. [Google Scholar] [CrossRef]
- Simon, T.G.; Hagström, H.; Sharma, R.; Söderling, J.; Roelstraete, B.; Larsson, E.; Ludvigsson, J.F. Risk of severe COVID-19 and mortality in patients with established chronic liver disease: A nationwide matched cohort study. BMC Gastroenterol. 2021, 21, 439. [Google Scholar] [CrossRef]
- Nagarajan, R.; Krishnamoorthy, Y.; Rajaa, S.; Hariharan, V.S. COVID-19 Severity and Mortality Among Chronic Liver Disease Patients: A Systematic Review and Meta-Analysis. Prev. Chronic Dis. 2022, 19, E53. [Google Scholar] [CrossRef]
- Mendizabal, M.; Ridruejo, E.; Piñero, F.; Anders, M.; Padilla, M.; Toro, L.G.; Torre, A.; Montes, P.; Urzúa, A.; Gonzalez Ballerga, E.; et al. Comparison of different prognostic scores for patients with cirrhosis hospitalized with SARS-CoV-2 infection. Ann. Hepatol. 2021, 25, 100350. [Google Scholar] [CrossRef]
- Sharma, S.; Elhence, A.; Vaishnav, M.; Kumar, R.; Shalimar. COVID-19 in patients with cirrhosis: Understanding adverse impact. Gut 2021, 70, 1409. [Google Scholar] [CrossRef]
- Shalimar; Elhence, A.; Vaishnav, M.; Kumar, R.; Pathak, P.; Soni, K.D.; Aggarwal, R.; Soneja, M.; Jorwal, P.; Kumar, A.; et al. Poor outcomes in patients with cirrhosis and Corona Virus Disease-19. Indian J. Gastroenterol. 2020, 39, 285–291. [Google Scholar] [CrossRef] [PubMed]
- Warner, F.J.; Rajapaksha, H.; Shackel, N.; Herath, C.B. ACE2: From protection of liver disease to propagation of COVID-19. Clin. Sci. 2020, 134, 3137–3158. [Google Scholar] [CrossRef] [PubMed]
- Chai, X.; Hu, L.; Zhang, Y.; Han, W.; Lu, Z.; Ke, A.; Zhou, J.; Shi, G.; Fang, N.; Fan, J.; et al. Specific ACE2 Expression in Cholangiocytes May Cause Liver Damage After 2019-nCoV Infection. bioRxiv 2020. [Google Scholar] [CrossRef] [Green Version]
- Gao, F.; Zheng, K.I.; Fan, Y.-C.; Targher, G.; Byrne, C.D.; Zheng, M.-H. ACE2: A Linkage for the Interplay Between COVID-19 and Decompensated Cirrhosis. Am. J. Gastroenterol. 2020, 115, 1544. [Google Scholar] [CrossRef] [PubMed]
- Li, D.; Ding, X.; Xie, M.; Tian, D.; Xia, L. COVID-19-associated liver injury: From bedside to bench. J. Gastroenterol. 2021, 56, 218–230. [Google Scholar] [CrossRef]
- Su, F. COVID-19 and Cirrhosis: A Combination We Must Strive to Prevent. Gastroenterology 2021, 161, 1371–1373. [Google Scholar] [CrossRef]
- Dufour, J.-F.; Marjot, T.; Becchetti, C.; Tilg, H. COVID-19 and liver disease. Gut 2022, 71, 2350–2362. [Google Scholar] [CrossRef]
- Ruemmele, P.; Hofstaedter, F.; Gelbmann, C.M. Secondary sclerosing cholangitis. Nat. Rev. Gastroenterol. Hepatol. 2009, 6, 287–295. [Google Scholar] [CrossRef]
- Bütikofer, S.; Lenggenhager, D.; Wendel Garcia, P.D.; Maggio, E.M.; Haberecker, M.; Reiner, C.S.; Brüllmann, G.; Buehler, P.K.; Gubler, C.; Müllhaupt, B.; et al. Secondary sclerosing cholangitis as cause of persistent jaundice in patients with severe COVID-19. Liver Int. 2021, 41, 2404–2417. [Google Scholar] [CrossRef]
- Ghafoor, S.; Germann, M.; Jüngst, C.; Müllhaupt, B.; Reiner, C.S.; Stocker, D. Imaging features of COVID-19-associated secondary sclerosing cholangitis on magnetic resonance cholangiopancreatography: A retrospective analysis. Insights Imaging 2022, 13, 128. [Google Scholar] [CrossRef]
- Leonhardt, S.; Veltzke-Schlieker, W.; Adler, A.; Schott, E.; Hetzer, R.; Schaffartzik, W.; Tryba, M.; Neuhaus, P.; Seehofer, D. Trigger mechanisms of secondary sclerosing cholangitis in critically ill patients. Crit. Care 2015, 19, 131. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hunyady, P.; Streller, L.; Rüther, D.F.; Groba, S.R.; Bettinger, D.; Fitting, D.; Hamesch, K.; Marquardt, J.U.; Mücke, V.T.; Finkelmeier, F.; et al. Secondary sclerosing cholangitis following COVID-19 disease: A multicenter retrospective study. Clin. Infect. Dis. 2022, ciac565. [Google Scholar] [CrossRef] [PubMed]
- Wanner, N.; Andrieux, G.; Badia-I-Mompel, P.; Edler, C.; Pfefferle, S.; Lindenmeyer, M.T.; Schmidt-Lauber, C.; Czogalla, J.; Wong, M.N.; Okabayashi, Y.; et al. Molecular consequences of SARS-CoV-2 liver tropism. Nat. Metab. 2022, 4, 310–319. [Google Scholar] [CrossRef] [PubMed]
- Puelles, V.G.; Lütgehetmann, M.; Lindenmeyer, M.T.; Sperhake, J.P.; Wong, M.N.; Allweiss, L.; Chilla, S.; Heinemann, A.; Wanner, N.; Liu, S.; et al. Multiorgan and Renal Tropism of SARS-CoV-2. N. Engl. J. Med. 2020, 383, 590–592. [Google Scholar] [CrossRef] [PubMed]
- Zhao, B.; Ni, C.; Gao, R.; Wang, Y.; Yang, L.; Wei, J.; Lv, T.; Liang, J.; Zhang, Q.; Xu, W.; et al. Recapitulation of SARS-CoV-2 infection and cholangiocyte damage with human liver ductal organoids. Protein Cell 2020, 11, 771–775. [Google Scholar] [CrossRef] [Green Version]
- Xu, Z.; Shi, L.; Wang, Y.; Zhang, J.; Huang, L.; Zhang, C.; Liu, S.; Zhao, P.; Liu, H.; Zhu, L.; et al. Pathological findings of COVID-19 associated with acute respiratory distress syndrome. Lancet Respir. Med. 2020, 8, 420–422. [Google Scholar] [CrossRef]
- Tafreshi, S.; Whiteside, I.; Levine, I.; D’Agostino, C. A case of secondary sclerosing cholangitis due to COVID-19. Clin. Imaging 2021, 80, 239–242. [Google Scholar] [CrossRef]
- Hartl, L.; Haslinger, K.; Angerer, M.; Semmler, G.; Schneeweiss-Gleixner, M.; Jachs, M.; Simbrunner, B.; Bauer, D.J.M.; Eigenbauer, E.; Strassl, R.; et al. Progressive cholestasis and associated sclerosing cholangitis are frequent complications of COVID-19 in patients with chronic liver disease. Hepatology 2022, 76, 1563–1575. [Google Scholar] [CrossRef]
- Lee, A.; Wein, A.N.; Doyle, M.B.M.; Chapman, W.C. Liver transplantation for post-COVID-19 sclerosing cholangitis. BMJ Case Rep. 2021, 14, e244168. [Google Scholar] [CrossRef]
- Roth, N.C.; Kim, A.; Vitkovski, T.; Xia, J.; Ramirez, G.; Bernstein, D.; Crawford, J.M. Post-COVID-19 Cholangiopathy: A Novel Entity. Am. J. Gastroenterol. 2021, 116, 1077–1082. [Google Scholar] [CrossRef]
- Kobeszko, M.; Kumar, N. S1655 COVID-19-Induced Persistent Jaundice With Secondary Sclerosing Cholangitis. Off. J. Am. Coll. Gastroenterol. ACG 2021, 116, S741. [Google Scholar] [CrossRef]
- Bauer, U.; Pavlova, D.; Abbassi, R.; Lahmer, T.; Geisler, F.; Schmid, R.M.; Ehmer, U. Secondary sclerosing cholangitis after COVID-19 pneumonia: A report of two cases and review of the literature. Clin. J. Gastroenterol. 2022, 15, 1124–1129. [Google Scholar] [CrossRef] [PubMed]
- Machado, M.C.C.; Filho, R.K.; el Bacha, I.A.H.; de Oliveira, I.S.; Ribeiro, C.M.D.F.; de Souza, H.P.; Parise, E.R. Post-COVID-19 Secondary Sclerosing Cholangitis: A Rare but Severe Condition with no Treatment Besides Liver Transplantation. Am. J. Case Rep. 2022, 23, e936250. [Google Scholar] [CrossRef]
- Browning, J.D.; Kumar, K.S.; Saboorian, M.H.; Thiele, D.L. Ethnic differences in the prevalence of cryptogenic cirrhosis. Am. J. Gastroenterol. 2004, 99, 292–298. [Google Scholar] [CrossRef] [PubMed]
- Machado, M.V.; Diehl, A.M. Pathogenesis of Nonalcoholic Steatohepatitis. Gastroenterology 2016, 150, 1769–1777. [Google Scholar] [CrossRef] [Green Version]
- Maurice, J.; Manousou, P. Non-alcoholic fatty liver disease. Clin. Med. 2018, 18, 245–250. [Google Scholar] [CrossRef] [Green Version]
- Singh, A.; Hussain, S.; Antony, B. Non-alcoholic fatty liver disease and clinical outcomes in patients with COVID-19: A comprehensive systematic review and meta-analysis. Diabetes Metab. Syndr. 2021, 15, 813–822. [Google Scholar] [CrossRef]
- Sachdeva, S.; Khandait, H.; Kopel, J.; Aloysius, M.M.; Desai, R.; Goyal, H. NAFLD and COVID-19: A Pooled Analysis. SN Compr. Clin. Med. 2020, 2, 2726–2729. [Google Scholar] [CrossRef]
- Forlano, R.; Mullish, B.H.; Mukherjee, S.K.; Nathwani, R.; Harlow, C.; Crook, P.; Judge, R.; Soubieres, A.; Middleton, P.; Daunt, A.; et al. In-hospital mortality is associated with inflammatory response in NAFLD patients admitted for COVID-19. PloS ONE 2020, 15, e0240400. [Google Scholar] [CrossRef]
- Younossi, Z.; Stepanova, M.; Lam, B.; Cable, R.; Felix, S.; Jeffers, T.; Younossi, E.; Pham, H.; Srishord, M.; Austin, P.; et al. Independent Predictors of Mortality Among Patients with Non-alcoholic Fatty Liver Disease (NAFLD) Hospitalized with COVID-19 Infection. Hepatol. Commun. 2021, 6, 3062–3072. [Google Scholar] [CrossRef]
- Mushtaq, K.; Khan, M.U.; Iqbal, F.; Alsoub, D.H.; Chaudhry, H.S.; Ata, F.; Iqbal, P.; Elfert, K.; Balaraju, G.; Almaslamani, M.; et al. NAFLD is a predictor of liver injury in COVID-19 hospitalized patients but not of mortality, disease severity on the presentation or progression—The debate continues. J. Hepatol. 2021, 74, 482–484. [Google Scholar] [CrossRef] [PubMed]
- Mahamid, M.; Nseir, W.; Khoury, T.; Mahamid, B.; Nubania, A.; Sub-Laban, K.; Schifter, J.; Mari, A.; Sbeit, W.; Goldin, E. Nonalcoholic fatty liver disease is associated with COVID-19 severity independently of metabolic syndrome: A retrospective case-control study. Eur. J. Gastroenterol. Hepatol. 2021, 33, 1578–1581. [Google Scholar] [CrossRef] [PubMed]
- Bramante, C.T.; Tignanelli, C.J.; Dutta, N.; Jones, E.; Tamaritz, L.; Clark, J.; Melton-Meaux, G.; Usher, M.; Ikramuddin, S. Non-alcoholic fatty liver disease (NAFLD) and risk of hospitalization for Covid-19. medRxiv 2020. [Google Scholar] [CrossRef]
- Prins, G.H.; Olinga, P. Potential implications of COVID-19 in non-alcoholic fatty liver disease. Liver Int. 2020, 40, 2568. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Finelli, C. Gut Microbiota, NAFLD and COVID-19: A Possible Interaction. Obesities 2022, 2, 215–221. [Google Scholar] [CrossRef]
- Adenote, A.; Dumic, I.; Madrid, C.; Barusya, C.; Nordstrom, C.W.; Rueda Prada, L. NAFLD and Infection, a Nuanced Relationship. Can. J. Gastroenterol. Hepatol. 2021, 2021, 5556354. [Google Scholar] [CrossRef]
- López-González, Á.A.; Altisench Jané, B.; Masmiquel Comas, L.; Arroyo Bote, S.; González San Miguel, H.M.; Ramírez Manent, J.I. Impact of COVID-19 Lockdown on Non-Alcoholic Fatty Liver Disease and Insulin Resistance in Adults: A before and after Pandemic Lockdown Longitudinal Study. Nutrients 2022, 14, 2795. [Google Scholar] [CrossRef]
- Chang, Y.; Jeon, J.; Song, T.-J.; Kim, J. Association between the fatty liver index and the risk of severe complications in COVID-19 patients: A nationwide retrospective cohort study. BMC Infect. Dis. 2022, 22, 384. [Google Scholar] [CrossRef]
- Ji, D.; Qin, E.; Xu, J.; Zhang, D.; Cheng, G.; Wang, Y.; Lau, G. Non-alcoholic fatty liver diseases in patients with COVID-19: A retrospective study. J. Hepatol. 2020, 73, 451–453. [Google Scholar] [CrossRef]
- Fondevila, M.F.; Mercado-Gómez, M.; Rodríguez, A.; Gonzalez-Rellan, M.J.; Iruzubieta, P.; Valentí, V.; Escalada, J.; Schwaninger, M.; Prevot, V.; Dieguez, C.; et al. Obese patients with NASH have increased hepatic expression of SARS-CoV-2 critical entry points. J. Hepatol. 2021, 74, 469–471. [Google Scholar] [CrossRef]
- Sharma, P.; Kumar, A.; Anikhindi, S.; Bansal, N.; Singla, V.; Shivam, K.; Arora, A. Effect of COVID-19 on Pre-existing Liver disease: What Hepatologist Should Know? J. Clin. Exp. Hepatol. 2021, 11, 484–493. [Google Scholar] [CrossRef] [PubMed]
- Suresh Kumar, V.C.; Harne, P.S.; Mukherjee, S.; Gupta, K.; Masood, U.; Sharma, A.V.; Lamichhane, J.; Dhamoon, A.S.; Sapkota, B. Transaminitis is an indicator of mortality in patients with COVID-19: A retrospective cohort study. World J. Hepatol. 2020, 12, 619–627. [Google Scholar] [CrossRef] [PubMed]
- Asemota, J.; Aduli, F. The Impact of Nonalcoholic Fatty Liver Disease on the Outcomes of Coronavirus Disease 2019 Infection. Clin. Liver Dis. 2022, 19, 29–31. [Google Scholar] [CrossRef] [PubMed]
- Backer-Meurke, S.L.; Khanna, D. The Lasting Effects of COVID-19 on The Progression of Non-Alcoholic Fatty Liver Disease. FASEB J. 2022, 36. [Google Scholar] [CrossRef]
- Milovanovic, T.; Pantic, I.; Dragasevic, S.; Lugonja, S.; Dumic, I.; Rajilic-Stojanovic, M. The interrelationship among non-alcoholic fatty liver disease, colonic diverticulosis and metabolic syndrome. J. Gastrointestin. Liver Dis. 2021, 30, 1–9. [Google Scholar] [CrossRef]
- Wilkins, T.; Sams, R.; Carpenter, M. Hepatitis B: Screening, Prevention, Diagnosis, and Treatment. Am. Fam. Physician 2019, 99, 314–323. [Google Scholar]
- Manns, M.P.; Maasoumy, B. Breakthroughs in hepatitis C research: From discovery to cure. Nat. Rev. Gastroenterol. Hepatol. 2022, 19, 533–550. [Google Scholar] [CrossRef]
- Bailey, J.R.; Barnes, E.; Cox, A.L. Approaches, Progress, and Challenges to Hepatitis C Vaccine Development. Gastroenterology 2019, 156, 418–430. [Google Scholar] [CrossRef] [Green Version]
- Global Hepatitis Report. 2017. Available online: https://www.who.int/publications-detail-redirect/9789241565455 (accessed on 10 September 2022).
- Global Health Sector Strategies on, Respectively, HIV, Viral Hepatitis and Sexually Transmitted Infections for the Period 2022–2030. Available online: https://www.who.int/publications-detail-redirect/9789240053779 (accessed on 10 September 2022).
- Yip, T.C.-F.; Gill, M.; Wong, G.L.-H.; Liu, K. Management of hepatitis B virus reactivation due to treatment of COVID-19. Hepatol. Int. 2022, 16, 257–268. [Google Scholar] [CrossRef]
- Choe, J.W.; Jung, Y.K.; Yim, H.J.; Seo, G.H. Clinical Effect of Hepatitis B Virus on COVID-19 Infected Patients: A Nationwide Population-Based Study Using the Health Insurance Review & Assessment Service Database. J. Korean Med. Sci. 2022, 37, e29. [Google Scholar] [CrossRef]
- Alqahtani, S.A.; Buti, M. COVID-19 and hepatitis B infection. Antivir. Ther. 2020, 25, 389–397. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; Lei, J.; Li, Z.; Yan, L. Potential Effects of Coronaviruses on the Liver: An Update. Front. Med. 2021, 8, 651658. [Google Scholar] [CrossRef] [PubMed]
- Yang, S.; Wang, S.; Du, M.; Liu, M.; Liu, Y.; He, Y. Patients with COVID-19 and HBV Coinfection are at Risk of Poor Prognosis. Infect. Dis. Ther. 2022, 11, 1229–1242. [Google Scholar] [CrossRef] [PubMed]
- Chen, L.; Huang, S.; Yang, J.; Cheng, X.; Shang, Z.; Lu, H.; Cheng, J. Clinical characteristics in patients with SARS-CoV-2/HBV co-infection. J. Viral Hepat. 2020, 27, 1504–1507. [Google Scholar] [CrossRef]
- He, Q.; Zhang, G.; Gu, Y.; Wang, J.; Tang, Q.; Jiang, Z.; Shao, C.; Zhang, H.; Chen, Z.; Ma, B.; et al. Clinical Characteristics of COVID-19 Patients With Pre-existing Hepatitis B Virus Infection: A Multicenter Report. Am. J. Gastroenterol. 2021, 116, 420–421. [Google Scholar] [CrossRef]
- Ding, Z.-Y.; Li, G.-X.; Chen, L.; Shu, C.; Song, J.; Wang, W.; Wang, Y.-W.; Chen, Q.; Jin, G.-N.; Liu, T.-T.; et al. Association of liver abnormalities with in-hospital mortality in patients with COVID-19. J. Hepatol. 2021, 74, 1295–1302. [Google Scholar] [CrossRef]
- Lv, X.-H.; Yang, J.-L.; Deng, K. COVID-19 Patients With Hepatitis B Virus Infection. Am. J. Gastroenterol. 2021, 116, 1357–1358. [Google Scholar] [CrossRef]
- Kaufman, H.W.; Bull-Otterson, L.; Meyer, W.A.; Huang, X.; Doshani, M.; Thompson, W.W.; Osinubi, A.; Khan, M.A.; Harris, A.M.; Gupta, N.; et al. Decreases in Hepatitis C Testing and Treatment During the COVID-19 Pandemic. Am. J. Prev. Med. 2021, 61, 369–376. [Google Scholar] [CrossRef]
- Mori, N.; Imamura, M.; Takaki, S.; Araki, T.; Hayes, N.C.; Aisaka, Y.; Chayama, K. Hepatitis C virus (HCV) reactivation caused by steroid therapy for dermatomyositis. Intern. Med. 2014, 53, 2689–2693. [Google Scholar] [CrossRef] [Green Version]
- Lee, H.L.; Bae, S.H.; Jang, B.; Hwang, S.; Yang, H.; Nam, H.C.; Sung, P.S.; Lee, S.W.; Jang, J.W.; Choi, J.Y.; et al. Reactivation of Hepatitis C Virus and Its Clinical Outcomes in Patients Treated with Systemic Chemotherapy or Immunosuppressive Therapy. Gut Liver 2017, 11, 870–877. [Google Scholar] [CrossRef] [Green Version]
- Shokri, S.; Mahmoudvand, S. The possibility of hepatitis C reactivation in COVID-19 patients treated with corticosteroids. Ann. Hepatol. 2022, 27, 100704. [Google Scholar] [CrossRef] [PubMed]
- Afify, S.; Eysa, B.; Hamid, F.A.; Abo-Elazm, O.M.; Edris, M.A.; Maher, R.; Abdelhalim, A.; Abdel Ghaffar, M.M.; Omran, D.A.; Shousha, H.I. Survival and outcomes for co-infection of chronic hepatitis C with and without cirrhosis and COVID-19: A multicenter retrospective study. World J. Gastroenterol. 2021, 27, 7362–7375. [Google Scholar] [CrossRef] [PubMed]
- Ronderos, D.; Omar, A.M.S.; Abbas, H.; Makker, J.; Baiomi, A.; Sun, H.; Mantri, N.; Choi, Y.; Fortuzi, K.; Shin, D.; et al. Chronic hepatitis-C infection in COVID-19 patients is associated with in-hospital mortality. World J. Clin. Cases 2021, 9, 8749–8762. [Google Scholar] [CrossRef] [PubMed]
- Hamid, S.; Alvares da Silva, M.R.; Burak, K.W.; Chen, T.; Drenth, J.P.H.; Esmat, G.; Gaspar, R.; LaBrecque, D.; Lee, A.; Macedo, G.; et al. WGO Guidance for the Care of Patients With COVID-19 and Liver Disease. J. Clin. Gastroenterol. 2021, 55, 1–11. [Google Scholar] [CrossRef] [PubMed]
- Elfiky, A.A. Ribavirin, Remdesivir, Sofosbuvir, Galidesivir, and Tenofovir against SARS-CoV-2 RNA dependent RNA polymerase (RdRp): A molecular docking study. Life Sci. 2020, 253, 117592. [Google Scholar] [CrossRef] [PubMed]
- Gadour, E.; Hassan, Z.; Shrwani, K. P31 Covid-19 induced hepatitis (CIH), definition and diagnostic criteria of a poorly understood new clinical syndrome. Gut 2020, 69, A22. [Google Scholar] [CrossRef]
- Balaja, W.R.; Jacob, S.; Hamidpour, S.; Masoud, A. COVID-19 Presenting as Acute Icteric Hepatitis. Cureus 2021, 13, e16359. [Google Scholar] [CrossRef]
- Wang, Z.-Z.; Li, K.; Maskey, A.R.; Huang, W.; Toutov, A.A.; Yang, N.; Srivastava, K.; Geliebter, J.; Tiwari, R.; Miao, M.; et al. A small molecule compound berberine as an orally active therapeutic candidate against COVID-19 and SARS: A computational and mechanistic study. FASEB J. 2021, 35, e21360. [Google Scholar] [CrossRef]
- Ghareeb, D.A.; Saleh, S.R.; Seadawy, M.G.; Nofal, M.S.; Abdulmalek, S.A.; Hassan, S.F.; Khedr, S.M.; AbdElwahab, M.G.; Sobhy, A.A.; Abdel-Hamid, A.S.A.; et al. Nanoparticles of ZnO/Berberine complex contract COVID-19 and respiratory co-bacterial infection in addition to elimination of hydroxychloroquine toxicity. J. Pharm. Investig. 2021, 51, 735–757. [Google Scholar] [CrossRef]
- Warowicka, A.; Nawrot, R.; Goździcka-Józefiak, A. Antiviral activity of berberine. Arch. Virol. 2020, 165, 1935–1945. [Google Scholar] [CrossRef]
- Hung, T.-C.; Jassey, A.; Liu, C.-H.; Lin, C.-J.; Lin, C.-C.; Wong, S.H.; Wang, J.Y.; Yen, M.-H.; Lin, L.-T. Berberine inhibits hepatitis C virus entry by targeting the viral E2 glycoprotein. Phytomedicine 2019, 53, 62–69. [Google Scholar] [CrossRef] [PubMed]
- Kim, S.-Y.; Kim, H.; Kim, S.-W.; Lee, N.-R.; Yi, C.-M.; Heo, J.; Kim, B.-J.; Kim, N.-J.; Inn, K.-S. An Effective Antiviral Approach Targeting Hepatitis B Virus with NJK14047, a Novel and Selective Biphenyl Amide p38 Mitogen-Activated Protein Kinase Inhibitor. Antimicrob. Agents Chemother. 2017, 61, e00214-17. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jena, A.B.; Kanungo, N.; Chainy, G.B.N.; Devaraji, V.; Das, S.K.; Dandapat, J. A Computational Insight on the Inhibitory Potential of 8-Hydroxydihydrosanguinarine (8-HDS), a Pyridone Containing Analog of Sanguinarine, against SARS CoV2. Chem. Biodivers. 2022, 19, e202200266. [Google Scholar] [CrossRef] [PubMed]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Bucurica, S.; Ionita Radu, F.; Bucurica, A.; Socol, C.; Prodan, I.; Tudor, I.; Sirbu, C.A.; Plesa, F.C.; Jinga, M. Risk of New-Onset Liver Injuries Due to COVID-19 in Preexisting Hepatic Conditions—Review of the Literature. Medicina 2023, 59, 62. https://doi.org/10.3390/medicina59010062
Bucurica S, Ionita Radu F, Bucurica A, Socol C, Prodan I, Tudor I, Sirbu CA, Plesa FC, Jinga M. Risk of New-Onset Liver Injuries Due to COVID-19 in Preexisting Hepatic Conditions—Review of the Literature. Medicina. 2023; 59(1):62. https://doi.org/10.3390/medicina59010062
Chicago/Turabian StyleBucurica, Sandica, Florentina Ionita Radu, Ana Bucurica, Calin Socol, Ioana Prodan, Ioana Tudor, Carmen Adella Sirbu, Florentina Cristina Plesa, and Mariana Jinga. 2023. "Risk of New-Onset Liver Injuries Due to COVID-19 in Preexisting Hepatic Conditions—Review of the Literature" Medicina 59, no. 1: 62. https://doi.org/10.3390/medicina59010062