Liver injury associated with acute respiratory distress syndrome and the prospects of mesenchymal stem cells therapy for liver failure

Home/2021, Vol. 9, No. 2/Liver injury associated with acute respiratory distress syndrome and the prospects of mesenchymal stem cells therapy for liver failure

Cell and Organ Transplantology. 2021; 9(2):in press.
DOI: 10.22494/cot.v9i2.130

Liver injury associated with acute respiratory distress syndrome and the prospects of mesenchymal stromal cells therapy for liver failure

Redko O., Dovgalyuk A., Dovbush A., Nebesna Z., Yakubyshyna L., Krynytska I.

  • I. Horbachevsky Ternopil National Medical University

Abstract

The pathogenesis of acute respiratory distress syndrome (ARDS) includes neutrophilic alveolitis, alteration of alveolar epithelium and endothelium, formation of hyaline membranes and microvascular thrombosis, which results in an acute hypoxemic respiratory failure. ARDS results in major structural and cellular changes in organs and organ systems. It causes liver dysfunction in critical patients through paracrine action of cytokines and other pro-inflammatory mediators as well as hypoxemia, oxidative stress, toxins and hypoperfusion.
Coronavirus disease 2019 (COVID-19)-associated ARDS affects liver through the development of systemic inflammatory response syndrome and hypoxia as well as cytokine storm. Liver injury manifests itself as increased plasma levels of hepatic transaminases and cholestatic liver enzymes. Stem cell therapy is one of the promising modern methods for treating ARDS-induced liver failure.
Many studies showed the ability of multipotent mesenchymal stromal cells (MMSCs) to differentiate into functional hepatocyte-like cells, which were then successfully used for liver regeneration. MMSCs were proven to be able to prevent the apoptosis of hepatocytes, as well as have anti-fibrotic and anti-inflammatory activity which allows their successful use in the treatment of ARDS-induced liver injury.

Key words: acute respiratory distress syndrome; COVID-19; mesenchymal stromal cells; liver injury; liver failure

 

1. Ranieri VM, Rubenfeld GD, Thompson BT, Ferguson ND, Caldwell E, et al. Definition Task Force ARDS. Acute respiratory distress syndrome. Jama, 2012; 307(23): 2526-2533. DOI: 10.1001/jama.2012.5669
https://doi.org/10.1001/jama.2012.5669
2. Bourenne J, Carvelli J, Papazian L. Evolving definition of acute respiratory distress syndrome. J Thorac Dis. 2019; 11(3):S390. DOI: 10.21037/jtd.2018.12.24
https://doi.org/10.21037/jtd.2018.12.24
PMid:30997228 PMCid:PMC6424760
3. Thille AW, Esteban A, Fernandez-Segoviano P, et al. Comparison of the Berlin definition for acute respiratory distress syndrome with autopsy. Am J Respir Crit Care Med. 2013; 187:761-7 DOI: 10.1164/rccm.201211-1981OC
https://doi.org/10.1164/rccm.201211-1981OC
PMid:23370917
4. Kamyshnyi A, Krynytska I, Matskevych V, Marushchak M, Lushchak O. Arterial hypertension as a risk comorbidity associated with COVID-19 pathology. Int J Hypertens. 2020; 2020:8019360. DOI: 10.1155/2020/8019360.
https://doi.org/10.1155/2020/8019360
PMid:33489355 PMCid:PMC7803108
5. Herrero R, Sánchez G, Asensio I, López E, Ferruelo A, Vaquero J, et al. Liver-lung interactions in acute respiratory distress syndrome. Intensive Care Med Exp. 2020; 8(1):1-13. DOI: 10.1186/s40635-020-00337-9
https://doi.org/10.1186/s40635-020-00337-9
PMid:33336286 PMCid:PMC7746785
6. Cai Y, Zou Z, Liu L, Chen S, Chen Y, Lin Z, Chen Y. Bone marrow-derived mesenchymal stem cells inhibits hepatocyte apoptosis after acute liver injury. Int J Clin Exp. 2015; 8(1): 107.
PMID: 25755697
7. Zhang Y, Li Y, Li W, Cai J, Yue M, Jiang L, et al. Therapeutic effect of human umbilical cord mesenchymal stem cells at various passages on acute liver failure in rats. Stem Cells Int. 2018; 2018. DOI: 10.1155/2018/7159465
https://doi.org/10.1155/2018/7159465
PMid:30538751 PMCid:PMC6261392
8. Lopes-Pacheco M, Robba C, Rocco PRM, Pelosi P. Current understanding of the therapeutic benefits of mesenchymal stem cells in acute respiratory distress syndrome. Cell Biol Toxicol. 2020; 36(1):83-102. DOI: 10.1007/s10565-019-09493-5
https://doi.org/10.1007/s10565-019-09493-5
PMid:31485828 PMCid:PMC7222160
9. Tsuchiya A, Kojima Y, Ikarashi S, Seino S, Watanabe Y, Kawata Y, et al. Clinical trials using mesenchymal stem cells in liver diseases and inflammatory bowel diseases. Inflamm Regen. 2017; 37(1): 1-15. DOI: 10.1186/s41232-017-0045-6
https://doi.org/10.1186/s41232-017-0045-6
PMid:29259715 PMCid:PMC5725741
10. Xiao K, Hou F, Huang X, Li B, Qian ZR, Xie L. Mesenchymal stem cells: current clinical progress in ARDS and COVID-19. Stem Cell Res Therapy. 2020; 11(1):1-7. DOI: 10.1186/s13287-020-01804-6
https://doi.org/10.1186/s13287-020-01804-6
PMid:32698898 PMCid:PMC7373844
11. Wang YH, Wu DB, Chen B, Chen EQ, Tang H. Progress in mesenchymal stem cell-based therapy for acute liver failure. Stem Cell Res Therapy. 2018; 9(1):1-9. DOI: 10.1186/s13287-018-0972-4
https://doi.org/10.1186/s13287-018-0972-4
PMid:30143052 PMCid:PMC6109312
12. Hu C, Wu Z, Li L. Pre-treatments enhance the therapeutic effects of mesenchymal stem cells in liver diseases. JCMM. 2020; 24(1):40-49. DOI: 10.1111/jcmm.14788
https://doi.org/10.1111/jcmm.14788
PMid:31691463 PMCid:PMC6933358
13. Dominici MLBK, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini FC, Krause, DS, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006; 8(4):315-317. DOI: 10.1080/14653240600855905.
https://doi.org/10.1080/14653240600855905
PMid:16923606
14. Amin MA, Sabry D, Rashed LA, et al. Short-term evaluation of autologous transplantation of bone marrow-derived mesenchymal stem cells in patients with cirrhosis: Egyptian study. Clin Trans. 2013; 27(4):607-612. DOI: 10.1111/ctr.12179
https://doi.org/10.1111/ctr.12179
PMid:23923970
15. Wang L, Li J, Liu H, et al. Pilot study of umbilical cord-derived mesenchymal stem cell transfusion in patients with primary biliary cirrhosis. J Gastroenterol Hepatol. 2013; 28(1):85-92. DOI: 10.1111/jgh.12029
https://doi.org/10.1111/jgh.12029
PMid:23855301
16. Jang YO, Kim YJ, Baik SK, et al. Histological improvement following administration of autologous bone marrow-derived mesenchymal stem cells for alcoholic cirrhosis: a pilot study. Liver Int. 2014; 34:33-41. DOI: 10.1111/liv.12218
https://doi.org/10.1111/liv.12218
PMid:23782511
17. Salama H, Zekri AR, Medhat E, et al. Peripheral vein infusion of autologous mesenchymal stem cells in Egyptian HCV-positive patients with end-stage liver disease. Stem Cell Res Ther. 2014; 5:70. DOI: 10.1186/scrt459
https://doi.org/10.1186/scrt459
PMid:24886681 PMCid:PMC4097846
18. Wang L, Han Q, Chen H, et al. Allogeneic bone marrow mesenchymal stem cell transplantation in patients with UDCA-resistant primary biliary cirrhosis. Stem Cells Dev. 2014; 23:2482-2489. DOI: 10.1089/scd.2013.0500
https://doi.org/10.1089/scd.2013.0500
PMid:24835895
19. Xu L, Gong Y, Wang B, et al. Randomized trial of autologous bone marrow mesenchymal stem cells transplantation for hepatitis B virus cirrhosis: regulation of Treg/Th17 cells. J Gastroenterol Hepatol. 2014; 29:1620-1628. DOI: 10.1111/jgh.12653
https://doi.org/10.1111/jgh.12653
PMid:24942592
20. Suk KT, Yoon JH, Kim MY, et al. Transplantation with autologous bone marrow-derived mesenchymal stem cells for alcoholic cirrhosis: Phase 2 trial. Hepatology. 2016; 64:2185-2197. DOI: 10.1002/hep.28693
https://doi.org/10.1002/hep.28693
PMid:27339398
21. Lin BL, Chen JF, Qiu WH, et al. Allogeneic bone marrow-derived mesenchymal stromal cells for hepatitis B virus-related acute-onchronic liver failure: a randomized controlled trial. Hepatology. 2017; 66:209-219. DOI: 10.1002/hep.29189
https://doi.org/10.1002/hep.29189
PMid:28370357
22. Matthay MA, Ware LB, Zimmerman GA. The acute respiratory distress syndrome. J Clin Investig. 2012; 122(8): 2731-2740. DOI: 10.1172/JCI60331
https://doi.org/10.1172/JCI60331
PMid:22850883 PMCid:PMC3408735
23. Bellani G, Laffey JG, Pham T, Fan E, Brochard L, Esteban A, et al. Epidemiology, patterns of care, and mortality for patients with acute respiratory distress syndrome in intensive care units in 50 countries. Jama. 2016; 315(8): 788-800. DOI: 10.1001/jama.2016.0291
https://doi.org/10.1001/jama.2016.0291
PMid:26903337
24. Kallet RH, Lipnick MS, Zhuo H, Pangilinan LP, Gomez A. Characteristics of nonpulmonary organ dysfunction at onset of ARDS based on the Berlin definition. 2019. https://researcherprofiles.org/profile/5784350630992403
https://doi.org/10.4187/respcare.06165
PMid:30992403
25. Michael AM, Zemans RL, Zimmerman GA, et al. Acute respiratory distress syndrome. Nat Rev Dis Primers. 2019; 5:18. DOI: 10.1038/s41572-019-0069-0
https://doi.org/10.1038/s41572-019-0069-0
PMid:30872586 PMCid:PMC6709677
26. Thompson BT, Chambers RC, Liu KD. Acute respiratory distress syndrome. N Engl J Med. 2017; 377:562-72. DOI: 10.1056/NEJMra1608077
https://doi.org/10.1056/NEJMra1608077
PMid:28792873
27. Papazian L, Aubron C, Brochard L, Chiche J-D, Combes A, Dreyfuss D, et al. Formal guidelines: management of acute respiratory distress syndrome. Ann Intensive Care. 2019; 9(1):1-18. DOI: 10.1186/s13613-019-0540-9
https://doi.org/10.1186/s13613-019-0540-9
PMid:31197492 PMCid:PMC6565761
28. Raghavendran K, Napolitano LM. Severe Acute Respiratory Distress Syndrome, An Issue of Critical Care Clinics-E-Book. 2011; 27(3):429-437. DOI: 10.1016/j.ccc.2011.05.006
https://doi.org/10.1016/j.ccc.2011.05.006
PMid:21742209 PMCid:PMC3173767
29. Raghavendran K, Napolitano LM. ALI and ARDS: challenges and advances. Crit Care Clin. 2011, 27(3):429. DOI: 10.1016/j.ccc.2011.05.012
https://doi.org/10.1016/j.ccc.2011.05.012
PMid:21742208
30. Amato MB, Meade MO, Slutsky AS, et al. Driving pressure and survival in the acute respiratory distress syndrome. N Engl J Med. 2015; 372:747-55. DOI: 10.1056/NEJMsa1410639
https://doi.org/10.1056/NEJMsa1410639
PMid:25693014
31. Rui L. Energy metabolism in the liver. Compr Physiol. 2014; 4:177-197. DOI: 10.1002/cphy.c130024
https://doi.org/10.1002/cphy.c130024
PMid:24692138 PMCid:PMC4050641
32. Guillot A, Tacke F. Liver macrophages: old dogmas and new insights. Hepatology communications. 2019; 3(6):730-743. DOI: 10.1002/hep4.1356
https://doi.org/10.1002/hep4.1356
PMid:31168508 PMCid:PMC6545867
33. Kolaczkowska E, Jenne CN, Surewaard BGJ, Thanabalasuriar A, Lee W-Y, Sanz M-J, et al. Molecular mechanisms of NET formation and degradation revealed by intravital imaging in the liver vasculature. Nat Commun. 2015; 6(1):1-13. DOI: 10.1038/ncomms7673
https://doi.org/10.1038/ncomms7673
PMid:25809117 PMCid:PMC4389265
34. Wang Y, Liu W, Liu X, Sheng M, Pei Y, Lei R, et al. Role of liver in modulating the release of inflammatory cytokines involved in lung and multiple organ dysfunction in severe acute pancreatitis. Cell Biochem Biophys. 2015; 71(2):765-776. DOI: 10.1007/s12013-014-0261-5
https://doi.org/10.1007/s12013-014-0261-5
PMid:25260395
35. Yang P, Formanek P, Scaglione S, Afshar M. Risk factors and outcomes of acute respiratory distress syndrome in critically ill patients with cirrhosis. Hepatol Res. 2019; 49(3):335-343. DOI:10.1111/hepr.1324
https://doi.org/10.1111/hepr.13240
PMid:30084205 PMCid:PMC6560637
36. Patterson EK, Yao LJ, Ramic N, Lewis JF, Cepinskas G, McCaig L, et al. Lung-derived mediators induce cytokine production in downstream organs via an NF-κB-dependent mechanism. Mediators of inflammation. 2013. DOI: 10.1155/2013/586895
https://doi.org/10.1155/2013/586895
PMid:23606793 PMCid:PMC3625542
37. Karcz M, Bankey B, Schwaiberger D, Lachmann B, Papadakos PJ. Acute respiratory failure complicating advanced liver disease. In: Seminars in respiratory and critical care medicine. Thieme Medical Publishers. 2012: 96-110. DOI: 10.1055/s-0032-1301738
https://doi.org/10.1055/s-0032-1301738
PMid:22447264
38. Weber M, Lambeck S, Ding N, Henken S, Kohl M, Deigner HP, et al. Hepatic induction of cholesterol biosynthesis reflects a remote adaptive response to pneumococcal pneumonia. The FASEB Journal. 2012; 26(6):2424-2436. DOI: 10.1096/fj.11-191957
https://doi.org/10.1096/fj.11-191957
PMid:22415311
39. Quinton LJ, Blahna MT, Jones MR, Allen E, Ferrari JD, Hilliard KL, et al. Hepatocyte-specific mutation of both NF-κB RelA and STAT3 abrogates the acute phase response in mice. J Clin Investig. 2012; 122(5):1758-1763. DOI: 10.1172/JCI59408
https://doi.org/10.1172/JCI59408
PMid:22466650 PMCid:PMC3336975
40. Enaud R, Prevel R, Ciarlo E, Beaufils F, Wieërs G, Guery B, et al. The gut-lung axis in health and respiratory diseases: a place for inter-organ and inter-kingdom crosstalks. Front Cell Infect Microbiol. 2020; 10:9. DOI: 10.3389/fcimb.2020.00009
https://doi.org/10.3389/fcimb.2020.00009
PMid:32140452 PMCid:PMC7042389
41. Albillos A, Gottardi A, de Rescigno M. The gut-liver axis in liver disease: pathophysiological basis for therapy. J Hepatol. 2020; 72(3):558-577. DOI: 10.1016/j.jhep.2019.10.003
https://doi.org/10.1016/j.jhep.2019.10.003
PMid:31622696
42. Young RP, Hopkins RJ, Marsland B. The gut-liver-lung axis. Modulation of the innate immune response and its possible role in chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol. 2016; 54(2):161-169. DOI: 10.1165/rcmb.2015-0250PS
https://doi.org/10.1165/rcmb.2015-0250PS
PMid:26473323
43. Horvatits T, Drolz A, Trauner M, Fuhrmann V. Liver injury and failure in critical illness. Hepatology. 2019; 70(6):2204-2215. DOI: 10.1002/hep.30824
https://doi.org/10.1002/hep.30824
PMid:31215660
44. Lescot T, Karvellas C, Beaussier M, Magder S. Acquired liver injury in the intensive care unit. Anesthesiology. 2012; 117(4):898-904. DOI: 10.1097/ALN.0b013e318266c6df
https://doi.org/10.1097/ALN.0b013e318266c6df
PMid:22854981
45. Dickson RP. The lung microbiome and ARDS. It is time to broaden the model. 2018. DOI: 10.1164/rccm.201710-2096ED
https://doi.org/10.1164/rccm.201710-2096ED
PMid:29091746 PMCid:PMC6005245
46. Mukherjee S, Hanidziar D. More of the gut in the lung: how two microbiomes meet in ARDS. Yale J Biol Med. 2018; 91(2):143-149.
47. Dickson RP, Singer BH, Newstead MW, Falkowski NR, Erb-Downward JR, Standiford TJ, et al. Enrichment of the lung microbiome with gut bacteria in sepsis and the acute respiratory distress syndrome. Nat Microbiol. 2016; 1(10):1-9. DOI: 10.1038/nmicrobiol.2016.113
https://doi.org/10.1038/nmicrobiol.2016.113
PMid:27670109 PMCid:PMC5076472
48. de Jong PR, González-Navajas JM, Jansen NJG. The digestive tract as the origin of systemic inflammation. Crit Care. 2016; 20(1):1-12. DOI: 10.1186/s13054-016-1458-3
https://doi.org/10.1186/s13054-016-1458-3
PMid:27751165 PMCid:PMC5067918
49. Massey VL, Poole LG, Siow DL, Torres E, Warner NL, Schmidt RH, et al. Chronic Alcohol Exposure Enhances Lipopolysaccharide‐Induced Lung Injury in Mice: Potential Role of Systemic Tumor Necrosis Factor-Alpha. Alcohol Clin Exp Res. 2015; 39(10):1978-1988. DOI: 10.1111/acer.12855
https://doi.org/10.1111/acer.12855
PMid:26380957 PMCid:PMC4804458
50. Massey VL. Potential role of the gut/liver/lung axis in alcohol-induced tissue pathology. Biomolecule. 2015; 5(4):2477-2503. DOI: 10.3390/biom5042477
https://doi.org/10.3390/biom5042477
PMid:26437442 PMCid:PMC4693244
51. Dizier S, Forel J-M, Ayzac L, Richard J-C, Hraiech S, Lehingue S, et al. Early hepatic dysfunction is associated with a worse outcome in patients presenting with acute respiratory distress syndrome: a post-hoc analysis of the ACURASYS and PROSEVA studies. PLoS One. 2015; 10(12):e0144278. DOI: 10.1371/journal.pone.0144278
https://doi.org/10.1371/journal.pone.0144278
PMid:26636318 PMCid:PMC4670098
52. Wang Z, Li W, Guo Q, Wang Y, Ma L, Zhang X. Insulin-like growth factor-1 signaling in lung development and inflammatory lung diseases. Biomed Res Int. 2018; 2018. DOI: 10.1155/2018/6057589
https://doi.org/10.1155/2018/6057589
PMid:30018981 PMCid:PMC6029485
53. Kobayashi K, Horikami D, Omori K, Nakamura T, Yamazaki A, Maeda S, et al. Thromboxane A 2 exacerbates acute lung injury via promoting edema formation. Scientific reports. 2016; 6(1):1-12. DOI: 10.1038/srep32109
https://doi.org/10.1038/srep32109
PMid:27562142 PMCid:PMC4999811
54. Cuccurullo A, Greco E, Lupia E, De Giuli P, Bosco O, Martin-Conte E, et al. Blockade of thrombopoietin reduces organ damage in experimental endotoxemia and polymicrobial sepsis. PLoS One. 2016; 11(3):e0151088. DOI: 10.1371/journal.pone.0151088
https://doi.org/10.1371/journal.pone.0151088
PMid:26963510 PMCid:PMC4786277
55. Hilliard KL, Allen E, Traber KE, Yamamoto K, Stauffer NM, Wasserman GA, et al. The lung-liver axis: a requirement for maximal innate immunity and hepatoprotection during pneumonia. Am J Respir Cell Mol Biol. 2015; 53(3):378-390. DOI: 10.1165/rcmb.2014-0195OC
https://doi.org/10.1165/rcmb.2014-0195OC
PMid:25607543 PMCid:PMC4566062
56. Nardo AD, Schneeweiss-Gleixner M, Bakail M, Dixon ED, Lax SF, Trauner M. Pathophysiological mechanisms of liver injury in COVID-19. Liver Int. 2021; 41(1):20-32. DOI: 10.1111/liv.14730
https://doi.org/10.1111/liv.14730
PMid:33190346 PMCid:PMC7753756
57. Huang C, Wang Y, Li X, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet. 2020; 395:497-506. DOI: 10.1016/S0140-6736(20)30183-5
https://doi.org/10.1016/S0140-6736(20)30183-5
58. Liu Y, Sun W, Li J, et al. Clinical features and progression of acute respiratory distress syndrome in coronavirus disease. medRxiv. 2020. DOI: 10.1101/2020.02.17.20024166
https://doi.org/10.1101/2020.02.17.20024166
59. Hu LL, Wang WJ, Zhu QJ, Yang L. Novel coronavirus pneumonia related liver injury: etiological analysis and treatment strategy. Chin J Hepatol. 2020; 28:E001-E001. DOI:10.3760/cma.j.issn.1007-3418.2020.02.001.
60. Zu ZY, Jiang MD, Xu PP, Chen W, Ni QQ, Lu GM, et al. Coronavirus disease 2019 (COVID-19): A perspective from China. Radiology. 2020. DOI: 10.1148/radiol.2020200490
https://doi.org/10.1148/radiol.2020200490
PMid:32083985 PMCid:PMC7233368
61. Ren M Jie L, Jun S, Subrata G, Liang-Ru Z, Hong Y, et al. Implications of COVID-19 for patients with pre-existing digestive diseases. Lancet Gastroenterol Hepatol. 2020. DOI:10.1016/S2468-1253(20)30076-5.
https://doi.org/10.1016/S2468-1253(20)30076-5
62. Li J, Fan JG. Characteristics and mechanism of liver injury in 2019 coronavirus disease. Journal of clinical and translational hepatology. 2020; 8(1):13. DOI: 10.14218/JCTH.2020.00019
https://doi.org/10.14218/JCTH.2020.00019
PMid:32274341 PMCid:PMC7132021
63. 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. DOI: 10.1016/j.jhep.2020.05.002
https://doi.org/10.1016/j.jhep.2020.05.002
PMid:32437830 PMCid:PMC7211738
64. Wang Y, Lu F, Zhao J. Reply to: Correspondence relating to “SARSCoV- 2 infection of the liver directly contributes to hepatic impairment in patients with COVID-19”. J Hepatol. 2020. DOI: 10.1016/j.jhep.2020.06.028
https://doi.org/10.1016/j.jhep.2020.06.028
PMid:32589896 PMCid:PMC7309894
65. Zhang C, Shi L, Wang FS. Liver injury in COVID-19: management and chal-lenges. Lancet Gastroenterol Hepatol. 2020; 5:428-30. DOI: 10.1016/S2468-1253(20)7-13005
https://doi.org/10.1016/S2468-1253(20)30057-1
66. Liu J, Li S, Liu J, et al. Longitudinal characteristics of lymphocyte responses and cytokine profiles in the peripheral blood of SARS-CoV-2 infected patients. EBioMedicine. 2020; 55:102763. DOI: 10.1016/j.ebiom.2020.102763
https://doi.org/10.1016/j.ebiom.2020.102763
PMid:32361250 PMCid:PMC7165294
67. Kucharski AJ, Russell TW, Diamond C, et al. Early dynamics of transmission and control of COVID-19: a mathematical modelling study. Lancet Infect Dis. 2020; 20:553-558. DOI: 10.1016/S1473-3099(20)30144-4
https://doi.org/10.1016/S1473-3099(20)30144-4
68. Ridruejo E, Soza A. The liver in times of COVID-19: What hepatologists should know. Annals of hepatology. 2020; 19(4):353-358. DOI: 10.1016/j.aohep.2020.05.001
https://doi.org/10.1016/j.aohep.2020.05.001
PMid:32425991 PMCid:PMC7233236
69. Cai Q, Huang D, Yu H, et al. COVID-19: Abnormal liver function tests. J Hepatol. 2020. DOI: 10.1016/j.jhep.2020.04.006
https://doi.org/10.1016/j.jhep.2020.04.006
PMid:32298767 PMCid:PMC7194951
70. Lax SF, Skok K, Zechner P, et al. Pulmonary arterial thrombosis in covid-19 with fatal outcome: results from a prospective, single-center, clinicopathologic case series. Ann Intern Med. 2020. DOI: 10.7326/M20-2566
https://doi.org/10.7326/M20-2566
PMid:32422076 PMCid:PMC7249507
71. Ji D, Qin E, Xu J, et al. Non-alcoholic fatty liver diseases in patients with COVID-19: A retrospective study. J Hepatol. 2020. DOI: 10.1016/j.jhep.2020.03.044
https://doi.org/10.1016/j.jhep.2020.03.044
PMid:32278005 PMCid:PMC7141624
72. Sonzogni A, Previtali G, Seghezzi M, et al. Liver histopathology in severe COVID 19 respiratory failure is suggestive of vascular alterations. Liver Int. 2020; 40:2110-2116. DOI: 10.1111/liv.14601
https://doi.org/10.1111/liv.14601
PMid:32654359 PMCid:PMC7404964
73. Bernal-Monterde V, Casas-Deza D, Letona-Giménez L, et al. SARSCoV- 2 Infection Induces a Dual Response in Liver Function Tests: Association with Mortality during Hospitalization. Biomedicines. 2020; 8:328. DOI: 10.3390/biomedicines8090328
https://doi.org/10.3390/biomedicines8090328
PMid:32899640 PMCid:PMC7555293
74. 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; 395:507-513. DOI: 10.1016/S0140-6736(20)30211-7
https://doi.org/10.1016/S0140-6736(20)30211-7
75. Guan W, Ni Z, Hu Y, et al. Clinical characteristics of coronavirus disease 2019 in China. N. N Engl J Med. 2020; 382:1708-1720. DOI: 10.1016/j.jemermed.2020.04.004
https://doi.org/10.1016/j.jemermed.2020.04.004
PMCid:PMC7266766
76. 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; 323:1061-1069. DOI: 10.1001/jama.2020.1585
https://doi.org/10.1001/jama.2020.1585
PMid:32031570 PMCid:PMC7042881
77. Xie H, Zhao J, Lian N, Lin S, Xie Q, Zhuo H. Clinical characteristics of non ICU hospitalized patients with coronavirus disease 2019 and liver injury: a retrospective study. Liver Int. 2020; 40:1321-1326. DOI: 10.1111/liv.14449
https://doi.org/10.1111/liv.14449
PMid:32239591 PMCid:PMC7228333
78. Richardson S, Hirsch JS, Narasimhan M, Crawford JM, McGinn T, DavidsonKW, et al. Presenting characteristics comorbidities, and outcomes among 5700 patients hospitalized with COVID-19 in the New York City Area. JAMA. 2020. DOI: 10.1001/jama.2020.6775
https://doi.org/10.1001/jama.2020.6775
PMid:32320003 PMCid:PMC7177629
79. Wang J, Zhu L, Xue L, Liu L, Yan X, Yan X, et al. Risk factors of liver injury in patients with coronavirus disease 2019 in Jiangsu, China: A retrospective, multi center study. Journal of Medical Virology. 2021; 93(6):3305-3311. DOI: 10.1002/jmv.26663
https://doi.org/10.1002/jmv.26663
PMid:33174624
80. Kulkarni AV, Kumar P, Tevethia HV, et al. Systematic review with meta-analysis: liver manifestations and outcomes in COVID-19. Aliment Pharmacol Ther. 2020; 52. DOI: 10.1111/apt.15916
https://doi.org/10.1111/apt.15916
PMid:32638436 PMCid:PMC7361465
81. Yadav DK, Singh A, Zhang Q, et al. Involvement of liver in COVID- 19: systematic review and meta-analysis. Gut. 2020. DOI: 10.1136/gutjn l-2020-322072
https://doi.org/10.1136/gutjnl-2020-322072
PMid:32669289 PMCid:PMC7948176
82. Kumar-M P, Mishra S, Jha DK, et al. Coronavirus disease (COVID- 19) and the liver: a comprehensive systematic review and meta- analysis. Hepatol Int. 2020. DOI: 10.1007/s12072-020-10071-9
https://doi.org/10.1007/s12072-020-10071-9
PMid:32623633 PMCid:PMC7335221
83. Paliogiannis P, Zinellu A. Bilirubin levels in patients with mild and severe Covid-19: A pooled analysis. Liver International. 2020; 40:1787-1788. DOI: 10.1111/liv.14477
https://doi.org/10.1111/liv.14477
PMid:32304343 PMCid:PMC7264680
84. Parasa S, Desai M, Chandrasekar VT, et al. Prevalence of Gastrointestinal Symptoms and Fecal Viral Shedding in Patients With Coronavirus Disease 2019. JAMA Netw Open. 2020; 3:e2011335. DOI: 10.1001/jamanetworkopen.2020.11335
https://doi.org/10.1001/jamanetworkopen.2020.11335
PMid:32525549 PMCid:PMC7290409
85. Waseem N, Chen P-H. Hypoxic Hepatitis: A Review and Clinical Update. J Clin Transl Hepatol. 2016; 4:263-268. DOI: 10.14218/JCTH.2016.00022
https://doi.org/10.14218/JCTH.2016.00022
86. Horvatits T, Trauner M, Fuhrmann V. Hypoxic liver injury and cholestasis in critically ill patients. Curr Opin Crit Care. 2013; 19:128-132. DOI: 10.1097/MCC.0b013e32835ec9e6
https://doi.org/10.1097/MCC.0b013e32835ec9e6
PMid:23403733
87. Henrion J. Hypoxic hepatitis. Liver Int. 2012; 32:1039-1052. DOI: 10.1111/j.1478-3231.2011.02655.x
https://doi.org/10.1111/j.1478-3231.2011.02655.x
PMid:22098491
88. Li J, Li RJ, Lv GY, Liu HQ. The mechanisms and strategies to protect from hepatic ischemia-reperfusion injury. Eur Rev Med Pharmacol Sci. 2015; 19:2036-2047.
89. Fayssoil A, Mustafic H, Mansencal N. The Right Ventricle in COVID-19 Patients. J Clean Prod. 2020; 130. DOI: 10.1016/j.amjcard.2020.06.007
https://doi.org/10.1016/j.amjcard.2020.06.007
PMid:32624188 PMCid:PMC7280141
90. Horvatits T, Drolz A, Trauner M, Fuhrmann V. Liver Injury and Failure in Critical Illness. Hepatology. 2019; 70:2204-2215. DOI: 10.1002/hep.30824
https://doi.org/10.1002/hep.30824
PMid:31215660
91. Vieillard-Baron A, Naeije R, Haddad F, Bogaard HJ, Bull TM, Fletcher N, et al. Diagnostic workup, etiologies and management of acute right ventricle failure. Intensive care medicine. 2018, 44(6):774-790. DOI: 10.1007/s00134-018-5172-2
https://doi.org/10.1007/s00134-018-5172-2
PMid:29744563
92. Kang H, Kim MY, Eom YW, Baik SK. Mesenchymal stem cells for the treatment of liver disease: present and perspectives. Gut and liver. 2020; 14(3):306. DOI: 10.5009/gnl18412
https://doi.org/10.5009/gnl18412
PMid:31581387 PMCid:PMC7234888
93. Eom YW, Shim KY, Baik SK. Mesenchymal stem cell therapy for liver fibrosis. Korean J Intern Med. 2015; 30:580-589. DOI: 10.3904/kjim.2015.30.5.580
https://doi.org/10.3904/kjim.2015.30.5.580
PMid:26354051 PMCid:PMC4578027
94. Yin L, Zhu Y, Yang J, Ni Y, Zhou Z, Chen Y, et al. Adipose tissue-derived mesenchymal stem cells differentiated into hepatocyte-like cells in vivo and in vitro. Mol Rep Med. 2015, 11(3):1722-1732. DOI: 10.3892/mmr.2014.2935
https://doi.org/10.3892/mmr.2014.2935
PMid:25395242 PMCid:PMC4270341
95. Kadota Y, Yagi H, Inomata K, Matsubara K, Hibi T, Abe Y, et al. Mesenchymal stem cells support hepatocyte function in engineered liver grafts. Organogenesis. 2014; 10(2):268-277. DOI: 10.4161/org.27879
https://doi.org/10.4161/org.27879
PMid:24488046 PMCid:PMC4154962
96. Mou XZ, Lin J, Chen JY, Li YF, Wu XX, Xiang BY, et al. Menstrual blood-derived mesenchymal stem cells differentiate into functional hepatocyte-like cells. Journal of Zhejiang University SCIENCE B. 2013; 14(11):961-972. DOI: 10.1631/jzus.B1300081
https://doi.org/10.1631/jzus.B1300081
PMid:24190442 PMCid:PMC3829645
97. Wu XB, Tao R. Hepatocyte differentiation of mesenchymal stem cells. HBPD INT. 2012; 11(4):360-371. DOI: 10.1016/s1499-3872(12)60193-3
https://doi.org/10.1016/S1499-3872(12)60193-3
98. Han YJ, Kang YH, Shivakumar SB, Bharti D, Son YB, Choi YH, et al. Stem cells from cryopreserved human dental pulp tissues sequentially differentiate into definitive endoderm and hepatocyte-like cells in vitro. Int J Med Sci. 2017; 14(13):1418. DOI:10.7150/ijms.22152#
https://doi.org/10.7150/ijms.22152
PMid:29200956 PMCid:PMC5707759
99. Kidd S, Spaeth E, Dembinski JL, Dietrich M, Watson K, Klopp A, et al. Direct evidence of mesenchymal stem cell tropism for tumor and wounding microenvironments using in vivo bioluminescent imaging. Stem cells. 2009; 27(10):2614-2623. DOI: 10.1002/stem.187
https://doi.org/10.1002/stem.187
PMid:19650040 PMCid:PMC4160730
100. Wang J, Cen P, Chen J, Fan L, Li J, Cao H, et al. Role of mesenchymal stem cells, their derived factors, and extracellular vesicles in liver failure. Stem Cell Res Ther. 2017; 8:137. DOI: doi.org/10.1186/s13287-017-0576-4
https://doi.org/10.1186/s13287-017-0576-4
PMid:28583199 PMCid:PMC5460333
101. Prakash MD, Miller S, Randall-Demllo S, Nurgali K. Mesenchymal stem cell treatment of inflammation-induced cancer. Inflamm Bowel Dis. 2016; 22(11):2694-2703. DOI: 10.1097/MIB.0000000000000900
https://doi.org/10.1097/MIB.0000000000000900
PMid:27753693
102. Kumar P, Kandoi S, Misra R, Vijayalakshmi S, Rajagopal K, Verma RS. The mesenchymal stem cell secretome: a new paradigm towards cell-free therapeutic mode in regenerative medicine. Cytokine Growth Factor Rev. 2019; 46:1-9. DOI: 10.1016/j.cytogfr.2019.04.002
https://doi.org/10.1016/j.cytogfr.2019.04.002
PMid:30954374
103. Zarrabi M, Mousavi SH, Abroun S, Sadeghi B. Potential uses for cord blood mesenchymal stem cells. Cell Journal (Yakhteh). 2014; 15(4):274.
104. Ribeiro A, Laranjeira P, Mendes S, Velada I, Leite C, Andrade P, et al. Mesenchymal stem cells from umbilical cord matrix, adipose tissue and bone marrow exhibit different capability to suppress peripheral blood B, natural killer and T cells. Stem Cell Res Ther. 2013; 4(5):1-16. DOI: 10.1186/scrt336
https://doi.org/10.1186/scrt336
PMid:24406104 PMCid:PMC3854702
105. Kim G, Eom YW, Baik SK, Shin Y, Lim YL, Kim MY, et al. Therapeutic effects of mesenchymal stem cells for patients with chronic liver diseases: systematic review and meta-analysis. Journal of Korean Medical Science. 2015; 30(10):1405-1415. DOI: 10.3346/jkms.2015.30.10.1405
https://doi.org/10.3346/jkms.2015.30.10.1405
PMid:26425036 PMCid:PMC4575928
106. Secunda R, Vennila R, Mohanashankar AM, Rajasundari M, Jeswanth S, Surendran R. Isolation, expansion and characterisation of mesenchymal stem cells from human bone marrow, adipose tissue, umbilical cord blood and matrix: a comparative study. Cytotechnology. 2015; 67(5):793-807. DOI: 10.1007/s10616-014-9718-z
https://doi.org/10.1007/s10616-014-9718-z
PMid:24798808 PMCid:PMC4545441
107. Huang B, Cheng X, Wang H, et al. Mesenchymal stem cells and their secreted molecules predominantly ameliorate fulminant hepatic failure and chronic liver fibrosis in mice respectively. J Transl Med. 2016; 14:45. DOI: 10.1186/s12967-016-0792-1
https://doi.org/10.1186/s12967-016-0792-1
PMid:26861623 PMCid:PMC4746907
108. Liu YC, Zou XB, Chai YF, et al. Macrophage polarization in inflammatory diseases. Int J Biol Sci. 2014; 10:520-529. DOI: 10.7150/ijbs.8879
https://doi.org/10.7150/ijbs.8879
PMid:24910531 PMCid:PMC4046879
109. Ali G, Mohsin S, Khan M, et al. Nitric oxide augments mesenchymal stem cell ability to repair liver fibrosis. J Transl Med. 2012; 10:75. DOI: 10.1186/1479-5876-10-75
https://doi.org/10.1186/1479-5876-10-75
PMid:22533821 PMCid:PMC3419634
110. Gazdic M, Arsenijevic A, Markovic BS, Volarevic A, Dimova I, Djonov V, et al. Mesenchymal stem cell-dependent modulation of liver diseases. Int J Biol Sci. 2017; 13(9):1109. DOI: 10.7150/ijbs.20240
https://doi.org/10.7150/ijbs.20240
PMid:29104502 PMCid:PMC5666326
111. Heymann F, Hamesch K, Weiskirchen R, et al. The concanavalin A model of acute hepatitis in mice. Lab Anim. 2015; 49 (1):12-20. DOI: 10.1177/0023677215572841
https://doi.org/10.1177/0023677215572841
PMid:25835734
112. Ryu KH, Kim SY, Kim YR, et al. Tonsil-derived mesenchymal stem cells alleviate concanavalin A-induced acute liver injury. Exp Cell Res. 2014; 326:143-154. DOI: 10.1016/j.yexcr.2014.06.007
https://doi.org/10.1016/j.yexcr.2014.06.007
PMid:24954408
113. Zhu X, He B, Zhou X, et al. Effects of transplanted bone-marrow-derived mesenchymal stem cells in animal models of acute hepatitis. Cell Tissue Res. 2013; 351:477-486. DOI: 10.1007/s00441-012-1524-3
https://doi.org/10.1007/s00441-012-1524-3
PMid:23143676
114. El-Ansary M, Abdel-Aziz I, Mogawer S, et al. Phase II trial: undifferentiated versus differentiated autologous mesenchymal stem cells transplantation in Egyptian patients with HCV induced liver cirrhosis. Stem Cell Rev. 2012; 8:972-981. DOI: 10.1007/s12015-011-9322-y
https://doi.org/10.1007/s12015-011-9322-y
PMid:21989829
115. Shi M, Zhang Z, Xu R, et al. Human mesenchymal stem cell transfusion is safe and improves liver function in acute-on-chronic liver failure patients. Stem Cells Transl Med 2012; 1:725-731. DOI: 10.5966/sctm.2012-0034
https://doi.org/10.5966/sctm.2012-0034
PMid:23197664 PMCid:PMC3659658
116. Li YH, Xu Y, Wu HM, Yang J, Yang LH, Yue-Meng W. Umbilical cord-derived mesenchymal stem cell transplantation in hepatitis B virus related acute-onchronic liver failure treated with plasma exchange and Entecavir: a 24-month prospective study. Stem Cell Rev. 2016; 12:645-53. DOI: 10.1007/s12015-016-9683-3
https://doi.org/10.1007/s12015-016-9683-3
PMid:27687792
117. Zhang Z, Lin H, Shi M, et al. Human umbilical cord mesenchymal stromal cells improve liver function and ascites in decompensated liver cirrhosis patients. J Gastroenterol Hepatol. 2012; 27(2):112-120. DOI: 10.1111/j.1440-1746.2011.07024.x
https://doi.org/10.1111/j.1440-1746.2011.07024.x
PMid:22320928

Redko O, Dovgalyuk A, Dovbush A, Nebesna Z, Yakubyshyna L, Krynytska I. Liver injury associated with acute respiratory distress syndrome and the prospects of mesenchymal stem cells therapy for liver failure. Cell Organ Transpl. 2021; 9(2):in press. doi:10.22494/cot.v9i2.130

Creative Commons License
Is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.