Corona virus disease 2019-associated liver injury in cold regions

Abstract

The corona virus disease 2019 (COVID-19) pandemic has created a global health and economic crisis. Our studies uncovered that in addition to respiratory symptoms, liver damage is also common in COVID-19 patients; however, the cause of liver damage has not been fully elucidated. In this article, we summarize the clinical manifestations and pathological features of COVID-19 reported in published relevant studies and delineate the etiology and pathogenesis of COVID-19-related liver injury. We speculate that cold stimulation may be associated with COVID-19-related liver injury, which should be considered in clinical decision-making and treatment of COVID-19 in cold regions.

Keywords

corona virus disease 2019 / severe acute respiratory syndrome coronavirus 2 / liver injury / cold

References

[1] Huang C, Wang Y, Li X, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet, 2020; 395(10223): 497-506.

[2] Medicine JHU. COVID-19 Dashboard by the Center for Systems Science and Engineering (CSSE) at Johns Hopkins University (JHU). 2022. Accessed on May 20, 2022.

[3] Wu F, Zhao S, Yu B, et al. A new coronavirus associated with human respiratory disease in China. Nature, 2020; 579(7798): 265-269.

[4] Zhou P, Yang X L, Wang X G, et al. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature, 2020; 579(7798): 270-273.

[5] Zhu N, Zhang D, Wang W, et al. A Novel Coronavirus from Patients with Pneumonia in China, 2019. N Engl J Med, 2020; 382(8): 727-733.

[6] Wu J, Li W, Shi X, et al. Early antiviral treatment contributes to alleviate the severity and improve the prognosis of patients with novel coronavirus disease (COVID-19). J Intern Med, 2020; 288(1): 128-138.

[7] World meter. COVID-19 CORONAVIRUS PANDEMIC. Accessed on May 23, 2022.

[8] Icard P, Simula L, Rei J, et al. On the footsteps of Hippocrates, Sanctorius and Harvey to better understand the influence of cold on the occurrence of COVID-19 in European countries in 2020. Biochimie, 2021; 191: 164-171.

[9] Lu R, Zhao X, Li J, et al. Genomic characterisation and epidemiology of 2019 novel coronavirus: implications for virus origins and receptor binding. Lancet, 2020; 395(10224): 565-574.

[10] Lan J, Ge J, Yu J, et al. Structure of the SARS-CoV-2 spike receptor-binding domain bound to the ACE2 receptor. Nature, 2020; 581(7807): 215-220.

[11] Hoffmann M, Kleine-Weber H, Schroeder S, et al. SARS-CoV-2 Cell Entry Depends on ACE2 and TMPRSS2 and Is Blocked by a Clinically Proven Protease Inhibitor. Cell, 2020; 181(2): 271-280.e8.

[12] Walls A C, Park Y J, Tortorici M A, et al. Structure, Function, and Antigenicity of the SARS-CoV-2 Spike Glycoprotein. Cell, 2020; 181(2): 281-292.e6.

[13] Xie M, Chen Q. Insight into 2019 novel coronavirus - An updated interim review and lessons from SARS-CoV and MERS-CoV. Int J Infect Dis, 2020; 94: 119-124.

[14] Chen N, Zhou M, Dong X, et al. Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study. Lancet, 2020; 395(10223): 507-513.

[15] Guan W J, Ni Z Y, Hu Y, et al. Clinical Characteristics of Coronavirus Disease 2019 in China. N Engl J Med, 2020; 382(18): 1708-1720.

[16] Wu J, Liu J, Zhao X, et al. Clinical Characteristics of Imported Cases of Coronavirus Disease 2019 (COVID-19) in Jiangsu Province: A Multicenter Descriptive Study. Clin Infect Dis, 2020; 71(15): 706-712.

[17] Recalcati S. Cutaneous manifestations in COVID-19: a first perspective. Br J Dermatol, 2020; 182(6): 1477-1478.

[18] Wu Z Y, McGoogan J M. Characteristics ofand 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(13): 1239-1242.

[19] Marjot T, Webb G J, Barritt A St, et al. COVID-19 and liver disease: mechanistic and clinical perspectives. Nat Rev Gastroenterol Hepatol, 2021; 18(5): 348-364.

[20] Wu J, Song S, Cao H C, et al. Liver diseases in COVID-19: Etiology, treatment and prognosis. World J Gastroenterol, 2020; 26(19): 2286-2293.

[21] Kulkarni A V, Kumar P, Tevethia H V, et al. Systematic review with meta-analysis: liver manifestations and outcomes in COVID-19. Aliment Pharmacol Ther, 2020; 52(4): 584-599.

[22] Xu L, Liu J, Lu M, et al. Liver injury during highly pathogenic human coronavirus infections. Liver Int, 2020; 40(5): 998-1004.

[23] Jothimani D, Venugopal R, Abedin M F, et al. COVID-19 and the liver. J Hepatol, 2020; 73(5): 1231-1240.

[24] Cai Q, Huang D, Yu H, et al. COVID-19: Abnormal liver function tests. J Hepatol, 2020; 73(3): 566-574.

[25] Ding Z Y, Li G X, Chen L, et al. Association of liver abnormalities with in-hospital mortality in patients with COVID-19. J Hepatol, 2021; 74(6): 1295-1302.

[26] Weber S, Hellmuth J C, Scherer C, et al. Liver function test abnormalities at hospital admission are associated with severe course of SARS-CoV-2 infection: a prospective cohort study. Gut, 2021; 70(10): 1925-1932.

[27] Yip T C, Lui G C, Wong V W, et al. Liver injury is independently associated with adverse clinical outcomes in patients with COVID-19. Gut, 2021; 70(4): 733-742.

[28] Mao R, Qiu Y, He J S, et al. Manifestations and prognosis of gastrointestinal and liver involvement in patients with COVID-19: a systematic review and meta-analysis. Lancet Gastroenterol Hepatol, 2020; 5(7): 667-678.

[29] Chen T, Wu D, Chen H, et al. Clinical characteristics of 113 deceased patients with coronavirus disease 2019: retrospective study. BMJ, 2020; 368: m1091.

[30] Ponziani F R, Del Zompo F, Nesci A, et al. Liver involvement is not associated with mortality: results from a large cohort of SARS-CoV-2- positive patients. Aliment Pharmacol Ther, 2020; 52(6): 1060-1068.

[31] Zhang Y, Zheng L, Liu L, et al. Liver impairment in COVID-19 patients: A retrospective analysis of 115 cases from a single centre in Wuhan city, China. Liver Int, 2020; 40(9): 2095-2103.

[32] Yang X, Yu Y, Xu J, et al. Clinical course and outcomes of critically ill patients with SARS-CoV-2 pneumonia in Wuhan, China: a single-centered, retrospective, observational study. Lancet Respir Med, 2020; 8(5): 475-481.

[33] Xu X W, Wu X X, Jiang X G, et al. Clinical findings in a group of patients infected with the 2019 novel coronavirus (SARS-Cov-2) outside of Wuhan, China: retrospective case series. BMJ, 2020; 368: m606.

[34] Shi H, Han X, Jiang N, et al. Radiological findings from 81 patients with COVID-19 pneumonia in Wuhan, China: a descriptive study. Lancet Infect Dis, 2020; 20(4): 425-434.

[35] Wang D, Hu B, Hu C, et al. Clinical characteristics of 138 hospitalized patients with 2019 novel coronavirus-infected pneumonia in Wuhan, China. JAMA, 2020; 323(11): 1061-1069.

[36] Yang H Y, Jin B, Mao Y L. Liver injury in COVID-19: What do we know now? Hepatobiliary Pancreat Dis Int, 2020; 19(5): 407-408.

[37] Lei F, Liu Y M, Zhou F, et al. Longitudinal association between markers of liver injury and mortality in covid-19 in china. Hepatology, 2020; 72(2): 389-398.

[38] Richardson S, Hirsch J S, Narasimhan M, et al. Presenting characteristics, comorbidities, and outcomes among 5700 patients hospitalized with COVID-19 in the New York City Area. JAMA, 2020; 323(20): 2052-2059.

[39] Ding Y, He L, Zhang Q, et al. Organ distribution of severe acute respiratory syndrome (SARS) associated coronavirus (SARS-CoV) in SARS patients: implications for pathogenesis and virus transmission pathways. J Pathol, 2004; 203(2): 622-630.

[40] Sonzogni A, Previtali G, Seghezzi M, et al. Liver histopathology in severe COVID 19 respiratory failure is suggestive of vascular alterations. Liver Int, 2020; 40(9): 2110-2116.

[41] Wang Y, Liu S, Liu H, et al. SARS-CoV-2 infection of the liver directly contributes to hepatic impairment in patients with COVID-19. J Hepatol, 2020; 73(4): 807-816.

[42] Zhao Y, Zhao Z, Wang Y, et al. Single-cell RNA expression profiling of ACE2, the receptor of SARS-CoV-2. Am J Respir Crit Care Med, 2020; 202(5): 756-759.

[43] Hikmet F, Mear L, Edvinsson A, et al. The protein expression profile of ACE 2 in human tissues. Mol Syst Biol, 2020; 16(7): e9610.

[44] Hamming I, Timens W, Bulthuis ML, et al. Tissue distribution of ACE 2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis. J Pathol, 2004; 203(2): 631-637.

[45] Chai X, Hu L, Zhang Y, et al. Specific ACE 2 Expression in Cholangiocytes May Cause Liver Damage After 2019-nCoV Infection. bioRxiv, 2020. doi: 10.1101/2020.02.03.931766.

[46] Zhao B, Ni C, Gao R, et al. Recapitulation of SARS-CoV-2 infection and cholangiocyte damage with human liver ductal organoids. Protein Cell, 2020; 11(10): 771-775.

[47] Zhang J J, Dong X, Cao Y Y, et al. Clinical characteristics of 140 patients infected with SARS-CoV-2 in Wuhan, China. Allergy, 2020; 75(7): 1730-1741.

[48] Zhou MWY. A precision medicine approach to managing Wuhan Coronavirus. Precis Clin Med, 2020; 4(3): 14-21.

[49] Song Y, Liu P, Shi X L, et al. SARS-CoV-2 induced diarrhoea as onset symptom in patient with COVID-19. Gut, 2020; 69(6): 1143-1144.

[50] Ma C, Cong Y, Zhang H. COVID-19 and the digestive system. Am J Gastroenterol, 2020; 115(7): 1003-1006.

[51] Zhang H, Li H B, Lyu J R, et al. Specific ACE 2 expression in small intestinal enterocytes may cause gastrointestinal symptoms and injury after 2019-nCoV infection. Int J Infect Dis, 2020; 96: 19-24.

[52] Nardo A D, Schneeweiss-Gleixner M, Bakail M, et al. Pathophysiological mechanisms of liver injury in COVID-19. Liver Int, 2021; 41(1): 20-32.

[53] William M. Lee MD. Drug-Induced Hepatotoxicity. N Engl J Med, 1995; 333: 17.

[54] Qiu H, Tong Z, Ma P, et al. Intensive care during the coronavirus epidemic. Intensive Care Med, 2020; 46(4): 576-578.

[55] Fan Z, Chen L, Li J, et al. Clinical features of COVID-19-related liver functional abnormality. Clin Gastroenterol Hepatol, 2020; 18(7): 1561-1566.

[56] Lizardo-Thiebaud M J, Cervantes-Alvarez E, Limon-de la Rosa N, et al. Direct or collateral liver damage in SARS-CoV-2-infected patients. Semin Liver Dis, 2020; 40(3): 321-330.

[57] Varga Z, Flammer A J, Steiger P, et al. Endothelial cell infection and endotheliitis in COVID-19. Lancet, 2020; 395(10234): 1417-1418.

[58] Ackermann M, Verleden S E, Kuehnel M, et al. Pulmonary vascular endothelialitis, thrombosis, and angiogenesis in Covid-19. N Engl J Med, 2020; 383(2): 120-128.

[59] Gu S X, Tyagi T, Jain K, et al. Thrombocytopathy and endotheliopathy: crucial contributors to COVID-19 thromboinflammation. Nat Rev Cardiol, 2021; 18(3): 194-209.

[60] Sepanlou S G, Safiri S, Bisignano C, et al. The global, regional, and national burden of cirrhosis by cause in 195 countries and territories, 1990-2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet Gastroenterol Hepatol, 2020; 5(3): 245-266.

[61] Ji D, Qin E, Xu J, et al. Non-alcoholic fatty liver diseases in patients with COVID-19: A retrospective study. J Hepatol, 2020; 73(2): 451-453.

[62] Lipsitch M, Viboud C. Influenza seasonality: lifting the fog. Proc Natl Acad Sci U S A, 2009; 106(10): 3645-3646.

[63] Wolkoff P. Indoor air humidity, air quality, and health - An overview. Int J Hyg Environ Health, 2018; 221(3): 376-390.

[64] Tan J, Mu L, Huang J, et al. An initial investigation of the association between the SARS outbreak and weather: with the view of the environmental temperature and its variation. J Epidemiol Community Health, 2005; 59(3): 186-192.

[65] Araújo MB, Naimi B. Spread of SARS-CoV-2 Coronavirus likely constrained by climate. medRxiv, 2020. doi: 10.1101/2020.03.12.20034728.

[66] Wang M, Jiang A, Gong L, et al. Temperature Significantly Change COVID-19 Transmission in 429 cities. medRxiv, 2020. ChemRxiv. doi: 10.1101/2020.02.22.20025791

[67] Näyhä S, Hassi J. Cold and mortality from ischaemic heart disease in northern Finland. Arctic Med Res, 1995; 54 Suppl 2: 19-25.

[68] Näyhä S. Cold and the risk of cardiovascular diseases. A review. Int J Circumpolar Health, 2002; 61(4): 373-380.

[69] Sun Z. Cardiovascular responses to cold exposure. Front Biosci (Elite Ed), 2010; 2(2): 495-503.

[70] Waseem N, Chen PH. Hypoxic Hepatitis: A Review and Clinical Update. J Clin Transl Hepatol, 2016; 4(3): 263-268.

[71] Lightsey J M, Rockey D C. Current concepts in ischemic hepatitis. Curr Opin Gastroenterol, 2017; 33(3): 158-163.

[72] Dunn G D, Hayes P, Breen K J, et al. The liver in congestive heart failure a review. Am J Med Sci, 1973; 265(3): 174-189.