key: cord-0945139-3xkjnmze
authors: Ekpanyapong, Sirina; Bunchorntavakul, Chalermrat; Reddy, K. Rajender
title: COVID‐19 and the Liver: Lessons Learnt from the EAST and the WEST, A Year Later
date: 2021-08-12
journal: J Viral Hepat
DOI: 10.1111/jvh.13590
sha: 874c3bd45fa345b576d3de0a1ccc8277e8e75075
doc_id: 945139
cord_uid: 3xkjnmze

Globally, the severe acute respiratory syndrome coronavirus 2 (SARS‐CoV‐2 virus) has been a major cause for significant morbidity and mortality. Since the start of the pandemic, several hepato‐biliary manifestations in coronavirus disease 2019 (COVID‐19) have been described and unique considerations raised. The review aims to summarize the pathogenesis and hepato‐biliary manifestations in COVID‐19 and discuss the similarities, contrasting features and disease‐specific management across a range of hepato‐biliary diseases from the EAST and the WEST. Published studies and regional society guidelines from the EAST and the WEST were comprehensively reviewed and summarized. A wide range of hepato‐biliary manifestations, including the infrequent and chronic manifestation of cholangiopathy, has been observed in COVID‐19. The pathogenesis of liver injury is multifactorial and with scant evidence for a direct SARS‐CoV‐2 infection of the liver. Patients with non‐alcoholic fatty liver disease, cirrhosis, and liver cancer are potentially at increased risk for severe COVID‐19, and there are unique considerations in chronic hepatitis B or C, hepatocellular carcinoma, and in those immunosuppressed such as autoimmune hepatitis or liver transplant recipients. With the surges in SARS‐CoV‐2 infection, liver transplant activity has variably been impacted. Preliminarily, SARS‐CoV‐2 vaccines appear to be safe in those with chronic liver disease and in transplant recipients, while emerging data suggest the need for a third dose in immunosuppressed patients. In conclusion, patients with chronic liver disease, particularly cirrhosis, and liver transplant recipients, are vulnerable to severe COVID‐19. Over the past year, several unique considerations have been highlighted across a spectrum of hepato‐biliary diseases. Vaccination is strongly recommended for those with chronic liver disease and liver transplant recipients.

The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2 virus) has affected people from different parts of the World and has been a major cause for significant morbidity and mortality to date. Coronavirus disease 2019 (COVID- 19) , the disease caused by SARS-CoV-2, can present with various clinical features and while pulmonary manifestation is the most common, hepatic abnormalities can be encountered in up to 50% of infected individuals. 1, 2 The spectrum is variable and can range from asymptomatic abnormalities in hepatic biochemical tests to severe liver injury with some reports of acute-on-chronic liver failure in patients with underlying cirrhosis. [3] [4] [5] Hepatic dysfunction has been associated with poor outcome and which has been noted to be more frequent in critically ill patients. 6 The cause for hepatic dysfunction is hypothesized to be based on one or more factors such as ischaemic liver injury, immunemediated liver injury, drug-induced liver injury, pre-existing liver diseases or a direct cytopathic effect of the virus. 1, 7 Further, it has been noted that up to 2%-11% of patients with COVID-19 had preexisting liver disease 2 and that patients with underlying cirrhosis had higher mortality. 1 This review highlights several observations, and the lessons learnt since the pandemic started, on liver manifestations in COVID-19, from the EAST and the WEST, including prevalence, severity and pathogenesis. Further, we also summarize on the similarities and contrasting features in outcomes and diseasespecific management in those on immunosuppressive therapy, posttransplantation state, hepatocellular carcinoma (HCC), patients with chronic liver disease, compensated/decompensated cirrhosis, viral hepatitis, non-alcoholic fatty liver disease (NAFLD) and autoimmune liver diseases and also provide emerging data on the safety and efficacy of vaccines in those with chronic liver disease, as well as the immunosuppressed. While COVID-19 patients are encountered by a wide range of providers, including primary care, emergency room, infectious disease, gastroenterology, hepatology, critical care and palliative care specialties, this review aims to provide information specifically for those who evaluate and provide care to those with a spectrum of liver-related clinical situations in the context of COVID-19.

Since the outbreak of the novel coronavirus (SARS-CoV-2) in Wuhan,

March 2020 and globally has led to disastrous public health consequences. Although most of the COVID-19 cases have been mild, fatality due to respiratory failure and severe pneumonia is not uncommon with an estimated 2.5% case fatality rate worldwide, 8 and with a WHO estimated 3.8 million deaths globally by June 2021. 9 Liver impairment has been described as an elevation of aspartate transaminase (AST) or alanine transaminase (ALT) in around 10%-58%, mild bilirubin elevation in 3%-23%, slight alkaline phosphatase (ALP) elevation in 1%-10% and gamma-glutamyl transferase (GGT) elevation in 13%-54% in patients with COVID-19. 2, [10] [11] [12] [13] [14] [15] [16] [17] [18] [19] [20] [21] [22] [23] [24] [25] [26] [27] [28] [29] Most of the hepatic biochemical test abnormalities have been noted to return to normal values within 2-3 weeks and without specific treatment. 23 The pattern of liver injury is mostly hepatocellular rather than cholestatic although one would have expected a predominance of a cholestatic injury due to an abundance in the biliary epithelium of ACE2 receptors, to which the SARS-CoV-2 has an affinity. 30, 31 Patients with severe COVID-19 seem to have higher rate of liver impairment as noted by ALT or AST being more than three-fold the upper limit of normal (ULN) or total bilirubin of more than two-fold of the ULN. 7 AST is usually higher than ALT and has been associated with severe COVID-19 and mortality, which could possibly be the result of immune-mediated inflammation or non-hepatic injury. 32, 33 Interestingly, a report from Cai Q et al. found that COVID-19 patients with abnormal hepatic biochemical tests had higher risk of progressing to severe disease during hospitalization (odds ratio (OR) = 2.73 with hepatocellular pattern, and OR = 4.44 with mixed cholestasishepatocellular injury pattern). 22 However, some studies found no correlation between hepatic biochemical test abnormalities and severe clinical consequences or survival. 23, 24 Low serum albumin at hospital admission has been a marker of COVID-19 severity. [34] [35] [36] Fan et al. reported that patients with abnormal hepatic biochemical tests were more likely to be male, associated with higher levels of procalcitonin and C-reactive protein, and longer mean hospital stay compared to patients with normal tests (15.09 ± 4.79 days vs. 12.76 ± 4.14 days) (p = 0.021). 18 Further, a multicentre cohort (COVID-LIVER-CHESS) from China (n = 70) found that a longer time from illness onset to admission resulted in greater risk of liver injury in patients with COVID-19, thus suggesting the need of early detection of SARS-CoV-2 infection. 37 In contrast, severe COVID-19 is uncommon in children, and usually not associated with abnormal liver biochemistries; thus, when evaluating COVID-19-infected children with AST or ALT elevation, it is suggested that there be a search for underlying liver diseases and other coexisting infections. 38, 39 Data on liver manifestations and prevalence of hepatic biochemical test abnormalities in reports on COVID-19 from the EAST and the WEST are summarized in Table 1 and Table 2 . Because of a high prevalence of LFT abnormalities, regular monitoring of liver biochemistries should be performed in all COVID-19 patients. 39 It is important to always consider other aetiologies unrelated to COVID-19 when assessing COVID-19 patients with elevated liver enzymes; other viral infections such as hepatitis A, B and C should also be evaluated. 40 Data on pre-existing liver diseases were reported in several studies and has been around 2%-11%. 2 Patients with cirrhosis are at increased risk of infections and associated complications due to cirrhosis-associated immune dysfunction. 41, 42 Mortality due to COVID-19 appears higher in patients with more advanced liver disease and the highest in cirrhosis. 32,42

SARS-CoV-2 is a single, positive-stranded RNA virus that replicates using a virally encoded RNA dependent RNA polymerase. 32 The underlying mechanisms of liver injury in those with COVID-19 are believed to be multifactorial, some of which are based on histopathology from core samples at autopsy. 7 (Figure 1 ). -ALD was an independent risk factor for death (OR 

There is no evidence that stable chronic liver disease due to autoimmune hepatitis, primary biliary cholangitis or primary sclerosing cholangitis has an increased susceptibility to SARS-CoV-2 infection. 2 alone. 67 Another multicentre retrospective study from Italy in patients with cirrhosis and COVID-19 infection (n = 50) noted an evolution to ACLF in around 28% and with a 30-day mortality rate of 34%. 5 The severity of lung and liver diseases (according to CLIF-C, CLIF-OF and MELD scores) independently predicted mortality, and in patients with cirrhosis, mortality was significantly higher in those with COVID-19 than those with cirrhosis-associated bacterial infections. 5 Concomitantly, a study from India in patients with CLD and cirrhosis infected with COVID-19 (n = 28) reported poor outcomes in patients with cirrhosis, with worst survival rates in those with ACLF, and requirement of mechanical ventilation independently predicted mortality (hazard ratio = 13.68). 66 (Figure 2 ). Global liver society recommendations 32, 42, 60 with some similarities and contrasting aspects in patients with chronic viral hepatitis, autoimmune liver diseases, NAFLD, cirrhosis,

LT recipients and HCC are summarized in Table 3 .

In -Recommendation include continuation of treatment for hepatitis B or C if already on treatment -There is no contraindication to initiating treatment of hepatitis B and C, as clinically warranted, in patients without COVID-19 -In patients with COVID-19, initiating hepatitis B treatment is usually not immediately warranted but not contraindicated, and should be considered when there is clinical suspicion of hepatitis B flare or when initiating immunosuppressive agents, corticosteroids, or IL-6 monoclonal antibody -Initiating treatment of hepatitis C in a patient with COVID-19 is not immediately warranted and can be delayed till after resolution of COVID-19

Unique aspects in the EAST and the WEST EAST -Multicentre study from China reported prevalence of HBV infection in COVID-19 patients ranging from 2.1-12.2% 11, 124, 125 WEST -In a large series (n = 5700) from the Northeastern United States, prevalence of HBV and HCV infections in COVID-19 infected patients were reported to be 0.1% and <0.1%, respectively 28

-In patients with AIH without COVID-19, continuing the same dosage of immunosuppressive agents is recommended, as reducing or stopping immunosuppressive agents may cause disease flare -If active AIH is diagnosed, initiating immunosuppressive therapy is recommended despite COVID-19 infection 40 -In AIH patients with active COVID-19 and elevated liver biochemistries, do not presume disease flare without biopsy confirmation 32 -In patients with AIH and active COVID-19, consider lowering the overall level of immunosuppression to decrease the risk of superinfection or medication-induced lymphopenia and which should be individualized adjustment based on severity of COVID-19 32 -Vaccination for Streptococcus pneumoniae and influenza should be emphasized 63 

EAST -A study from India in patients with cirrhosis infected with COVID-19 reported poor outcomes in patients with cirrhosis, with the worst survival rates in ACLF 66 WEST -A multicentre North American study found that patients with cirrhosis+ COVID-19 had similar mortality compared with patients with cirrhosis alone, but higher than patients with COVID-19 alone 67 -An international registry (SECURE-cirrhosis and COVID-Hep) demonstrated that patients with cirrhosis experienced high rates of hepatic decompensation and death following COVID-19 infection, and mortality increased with greater Child-Pugh class 57 -A multicentre retrospective study from Italy found that mortality in patients with cirrhosis and COVID-19 was significantly higher than those with cirrhosis and bacterial infections 5 

The authors declare no conflicts of interest.

Review of the literature. 

-Immunosuppression and immunodeficiency were associated with increased risk of severe COVID-19 disease 130 However, case reports have suggested that temporary reduction of immunosuppressive agents during COVID-19 infection is justified 131 -A multicentre study from India (LDLT = 31) reported on the perioperative safety and good outcomes in carefully timed LDLT (1 COVID-19 infected), even in COVID-19 hotspots 132 WEST -Some studies reported higher mortality rates in liver and other solid organ transplant recipients and at around 20-25% 35, [73] [74] [75] [76] [77] 133, 134 -Elderly, obesity, male sex, history of cancer and comorbidities were associated with severe COVID-19 in immunosuppressed patients and transplant recipients 70, 72, 74, 76, 77, 135 -Results from 2 International registries (COVID-Hep and SECURE-Cirrhosis) found that LT state, overall, was not associated with increased mortality, but increased age and presence of comorbidities were 74 -Gastrointestinal symptoms were common in solid organ transplant recipients being infected with COVID-19 35, 76 -Complete discontinuation of immunosuppression after COVID-19 diagnosis is not recommended; mycophenolate was associated with severe disease and should be temporary withdrawn or switched to other immunosuppressions 71,73 -Reports from Italy (especially in paediatric LT recipients) showed low mortality rates in transplant recipients <5% 70, 136 HCCandother cancers 

EAST -Risk factors for severe COVID-19 infection in patients with cancer include the last anticancer treatment within 14 days and advanced age (≥65 years) 81,82 -In contrast, some studies reported mortality from COVID-19 in patients with cancer found to be associated with age, sex, and comorbidities, 80, 137 but not to the use of cytotoxic chemotherapy or other anticancer treatment 80 WEST -Increased age, male sex, smoking status, number of comorbidities, ECOG performance status of ≥2, and active cancer were independent factors associated with increased 30-day mortality 138 -During COVID-19 era, fewer patients with HCC presented to the multidisciplinary tumour board, and patients with HCC experienced significant treatment delay longer than 1 month in 2020 compared with 2019 (21.5% vs. 9.5%, p < 0.001) 87

Abbreviations: ACEI, angiotensin-converting enzyme inhibitor; ACLF, acute-on-chronic liver failure; AFP, alpha-fetoprotein; AIH, autoimmune hepatitis; ALT, alanine transaminase; ARB, angiotensin II receptor blocker; AST, aspartate transaminase; ECOG, Eastern Cooperative Oncology Group; FIB-4, fibrosis-4; HBV, hepatitis B virus; HCC, hepatocellular carcinoma; HCV, hepatitis C virus; LDLT, living-donor liver transplant; LFT, liver function test; LSM, liver stiffness measurement; LT, liver transplant; N, number of patients; NAFLD, non-alcoholic fatty liver disease; NASH, non-alcoholic steatohepatitis; NSAIDS, non-steroidal anti-inflammatory drugs; TACE, trans-arterial chemoembolization.

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COVID-19 and the Liver: Lessons Learnt from the EAST and the WEST, A Year Later