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
