Chinese expert consensus on the evaluation and postoperative management of lung transplant recipient in COVID-19 patients_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

 Chinese Medical Doctor Association Thoracic Surgeons Branch , Shanghai Medical Association Thoracic Surgery Specialist Branch , Shanghai Medical Doctor Association Thoracic Surgeons Branch , Specialist Alliance for the Promotion and Enhancement of Clinical Competence in General Thoracic Surgery

Department of Thoracic Surgery, Shanghai Pulmonary Hospital, Shanghai, 200433, P. R. China;

Corresponding author：

Chinese Medical Doctor Association Thoracic Surgeons Branch, Email: chenthoracic@163.com

Keywords：

Coronavirus disease 2019 (COVID-19); COVID-related acute respiratory distress syndrome; post COVID-19 pulmonary fibrosis; lung transplantation evaluation; antiviral

DOI：

10.7507/1007-4848.202411028

Video：

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Since the beginning of the coronavirus disease 2019 (COVID-19) pandemic at the end of December 2019, more than 85% of the population in China has been infected. Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) mainly affects the respiratory system, especially the lungs. The mortality rate of patients with severe infection is high. A percentage of 6% to 10% of patients will eventually develop into COVID-related acute respiratory distress syndrome (CARDS), which requires mechanical ventilation and extracorporeal membrane oxygenation (ECMO) support. Some patients who survive acute lung injury will subsequently develop post COVID-19 pulmonary fibrosis (PCPF). Both fully treated CARDS and severe PCPF are suitable candidates for lung transplantation. Due to the special course, evaluation strategies are different from those used in patients with common end-stage lung disease. After lung transplantation in COVID-19 patients, special treatment is required, including standardized nucleic acid testing for the novel coronavirus, adjustment strategy of immunosuppressive drugs, and rational use of antiviral drugs, which is a big challenge for the postoperative management of lung transplantation. This consensus was evidence-based written and was reached by experts after multiple rounds of discussions, providing reference for assessment and postoperative management of patients with interstitial pneumonia after COVID-19 infection.

Citation： Chinese Medical Doctor Association Thoracic Surgeons Branch, Shanghai Medical Association Thoracic Surgery Specialist Branch, Shanghai Medical Doctor Association Thoracic Surgeons Branch, Specialist Alliance for the Promotion and Enhancement of Clinical Competence in General Thoracic Surgery. Chinese expert consensus on the evaluation and postoperative management of lung transplant recipient in COVID-19 patients. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2025, 32(1): 1-7. doi: 10.7507/1007-4848.202411028 Copy

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2.	Mokhtari T, Hassani F, Ghaffari N, et al. COVID-19 and multiorgan failure: A narrative review on potential mechanisms. J Mol Histol, 2020, 51(6): 613-628.
3.	Guan WJ, Ni ZY, Hu Y, et al. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med, 2020, 382(18): 1708-1720.
4.	King CS, Mannem H, Kukreja J, et al. Lung transplantation for patients with COVID-19. Chest, 2022, 161(1): 169-178.
5.	Wu C, Chen X, Cai Y, et al. Risk factors associated with acute respiratory distress syndrome and death in patients with coronavirus disease 2019 pneumonia in Wuhan, China. JAMA Intern Med, 2020, 180(7): 934-943.
6.	Horby P, Lim WS, Emberson JR, et al. Dexamethasone in hospitalized patients with COVID-19. N Engl J Med, 2021, 384(8): 693-704.
7.	Group RC. Dexamethasone in hospitalized patients with COVID-19. N Engl J Med, 2021, 384(8): 693-704.
8.	Beigel JH, Tomashek KM, Dodd LE, et al. Remdesivir for the treatment of COVID-19—Final report. N Engl J Med, 2020, 383(19): 1813-1826.
9.	McDonald LT. Healing after COVID-19: Are survivors at risk for pulmonary fibrosis? Am J Physiol Lung Cell Mol Physiol, 2021, 320(2): L257-L265.
10.	Schaheen L, Bremner RM, Walia R, et al. Lung transplantation for coronavirus disease 2019 (COVID-19): The who, what, where, when, and why. J Thorac Cardiovasc Surg, 2022, 163(3): 865-868.
11.	Van Der Mark SC, Hoek RAS, Hellemons ME. Developments in lung transplantation over the past decade. Eur Respir Rev, 2020, 29(157): 190132.
12.	Valapour M, Lehr CJ, Skeans MA, et al. OPTN/SRTR 2016 annual data report: Lung. Am J Transplant, 2018, 18(Suppl 1): 363-433.
13.	Chambers DC, Cherikh WS, Harhay MO, et al. The International Thoracic Organ Transplant Registry of the International Society for Heart and Lung Transplantation: Thirty-sixth adult lung and heart-lung transplantation Report-2019; Focus theme: Donor and recipient size match. J Heart Lung Transplant, 2019, 38(10): 1042-1055.
14.	Erasmus ME, van der Bij W. Death after lung transplantation: Improving long term survival despite perilous early postoperative years. Transpl Int, 2020, 33(2): 128-129.
15.	Bharat A, Querrey M, Markov NS, et al. Lung transplantation for patients with severe COVID-19. Sci Transl Med, 2020, 12(574): eabe4282.
16.	Sahin MF, Beyoglu MA, Turkkan S, et al. Donor lung evaluation and lung transplantation in the COVID-19 era. Exp Clin Transplant, 2022, 20(9): 842-848.
17.	Cerier E, Lung K, Kurihara C, et al. Lung transplantation in coronavirus-19 patients: What we have learned so far. Clin Chest Med, 2023, 44(2): 347-357.
18.	Fernandes LM, Pêgo-Fernandes PM. New challenges for lung transplantation in the era of COVID-19. Sao Paulo Med J, 2022, 140(1): 1-4.
19.	中华医学会器官移植学分会. 中国肺移植受者选择与术前评估技术规范 (2019 版). 中华移植杂志: 电子版, 2019, 13(2) : 81-86.Chinese Society of Organ Transplantation, Chinese Medical Association. Technical specifications for recipient selection and preoperative evaluation of lung transplantation in China (2019 Edition). Chin J Transplant (Electronic Edition), 2019, 13(2): 81-86.
20.	Bharat A, Machuca TN, Querrey M, et al. Early outcomes after lung transplantation for severe COVID-19: A series of the first consecutive cases from four countries. Lancet Respir Med, 2021, 9(5): 487-497.
21.	Han X, Fan Y, Alwalid O, et al. Six-month follow-up chest CT findings after severe COVID-19 pneumonia. Radiology, 2021, 299(1): E177-E186.
22.	Tabatabaei SMH, Rajebi H, Moghaddas F, et al. Chest CT in COVID-19 pneumonia: What are the findings in mid-term follow-up? Emerg Radiol, 2020, 27(6): 711-719.
23.	Huang Y, Tan C, Wu J, et al. Impact of coronavirus disease 2019 on pulmonary function in early convalescence phase. Respir Res, 2020, 21(1): 163.
24.	Guler SA, Ebner L, Aubry-Beigelman C, et al. Pulmonary function and radiological features 4 months after COVID-19: First results from the national prospective observational Swiss COVID-19 lung study. Eur Respir J, 2021, 57(4): 2003690.
25.	Ojo AS, Balogun SA, Williams OT, et al. Pulmonary fibrosis in COVID‐19 survivors: Predictive factors and risk reduction strategies. Pulmonary medicine, 2020, 2020(1): 6175964.
26.	Evans RA, McAuley H, Harrison EM, et al. Physical, cognitive, and mental health impacts of COVID-19 after hospitalisation (PHOSP-COVID): A UK multicentre, prospective cohort study. Lancet Respir Med, 2021, 9(11): 1275-1287.
27.	Hui DS, Joynt GM, Wong KT, et al. Impact of severe acute respiratory syndrome (SARS) on pulmonary function, functional capacity and quality of life in a cohort of survivors. Thorax, 2005, 60(5): 401-409.
28.	Wong KT, Antonio GE, Hui DS, et al. Severe acute respiratory syndrome: Thin-section computed tomography features, temporal changes, and clinicoradiologic correlation during the convalescent period. J Comput Assist Tomogr, 2004, 28(6): 790-795.
29.	Bazdyrev E, Rusina P, Panova M, et al. Lung fibrosis after COVID-19: Treatment prospects. Pharmaceuticals (Basel), 2021, 14(8): 807.
30.	Kurihara C, Manerikar A, Querrey M, et al. Clinical characteristics and outcomes of patients with COVID-19-associated acute respiratory distress syndrome who underwent lung transplant. JAMA, 2022, 327(7): 652-661.
31.	《新型冠状病毒感染防控方案(试行第十版)》. URL: http://www.nhc.gov.cn/xcs/zhengcwj/202301/bdc1ff75feb94934ae1dade176d30936.shtml. Accessed on 2024-10-02.Prevention and Control Plan for Novel Coronavirus Infection (Tenth Trial Edition)". URL: http://www.nhc.gov.cn/xcs/zhengcwj/202301/bdc1ff75feb94934ae1dade176d30936.shtml. Accessed on 2024-10-02.
32.	Yin S, Wang X, Song T. Tacrolimus use and COVID-19 infection in patients after solid organ transplantation. Gastroenterology, 2021, 161(2): 728-730.
33.	Belli LS, Fondevila C, Cortesi PA, et al. Protective role of tacrolimus, deleterious role of age and comorbidities in liver transplant recipients with COVID-19: Results from the ELITA/ELTR multi-center European study. Gastroenterology, 2021, 160(4): 1151-1163.
34.	Karruli A, Spiezia S, Boccia F, et al. Effect of immunosuppression maintenance in solid organ transplant recipients with COVID-19: Systematic review and meta-analysis. Transpl Infect Dis, 2021, 23(4): e13595.
35.	Helleberg M, Niemann CU, Moestrup KS, et al. Persistent COVID-19 in an immunocompromised patient temporarily responsive to two courses of remdesivir therapy. J Infect Dis, 2020, 222(7): 1103-1107.
36.	Trottier CA, Wong B, Kohli R, et al. Dual antiviral therapy for persistent coronavirus disease 2019 and associated organizing pneumonia in an immunocompromised host. Clin Infect Dis, 2023, 76(5): 923-925.
37.	Martinez MA, Chen TY, Choi H, et al. Extended remdesivir infusion for persistent coronavirus disease 2019 infection. Proceedings of the Open Forum Infectious Diseases, F. 2022. Oxford University Press.
38.	Marjot T, Webb GJ, Barritt AS, et al. COVID-19 and liver disease: Mechanistic and clinical perspectives. Nat Rev Gastroenterol Hepatol, 2021, 18(5): 348-364.
39.	Chen Z, Xu W, Ma W, et al. Clinical laboratory evaluation of COVID-19. Clin Chim Acta, 2021, 519: 172-182.519-172.
40.	Karakoyun I, Colak A, Turken M, et al. Diagnostic utility of C-reactive protein to albumin ratio as an early warning sign in hospitalized severe COVID-19 patients. Int Immunopharmacol, 2021, 91: 107285.
41.	Liu X, Yue X, Liu F, et al. Analysis of clinical features and early warning signs in patients with severe COVID-19: A retrospective cohort study. PLoS One, 2020, 15(6): e0235459.
42.	Wang X, Che Q, Ji X, et al. Correlation between lung infection severity and clinical laboratory indicators in patients with COVID-19: A cross-sectional study based on machine learning. BMC Infect Dis, 2021, 21(1): 192.
43.	Guo J, Wang S, Xia H, et al. Cytokine signature associated with disease severity in COVID-19. Front Immunol, 2021, 20: 12: 681516.
44.	Mitchell O, Cosar AM, Malik MU, et al. Late liver function test abnormalities post-adult liver transplantation: A review of the etiology, investigation, and management. Hepatol Int, 2016, 10(1): 106-114.
45.	Wadei HM, Lee DD, Croome KP, et al. Early allograft dysfunction after liver transplantation is associated with short- and long-term kidney function impairment. Am J Transplant, 2016, 16(3): 850-859.
46.	Buchan TA, Moayedi Y, Truby LK, et al. Incidence and impact of primary graft dysfunction in adult heart transplant recipients: A systematic review and meta-analysis. J Heart Lung Transplant, 2021, 40(7): 642-651.
47.	Shah RJ, Diamond JM. Primary graft dysfunction (PGD) following lung transplantation. Proceedings of the seminars in respiratory and critical care medicine, F, 2018. Thieme Medical Publishers.
48.	Roach A, Chikwe J, Catarino P, et al. Lung transplantation for COVID19 related respiratory failure in the United States. N Engl J Med, 2022, 386(12): 1187-1188.

1. Wu Z, McGoogan JM. Characteristics of and important lessons from the coronavirus disease 2019 (COVID-19) outbreak in China: Summary of a report of 72 314 cases from the Chinese Center for Disease Control and Prevention. JAMA, 2020, 323(13): 1239-1242.
2. Mokhtari T, Hassani F, Ghaffari N, et al. COVID-19 and multiorgan failure: A narrative review on potential mechanisms. J Mol Histol, 2020, 51(6): 613-628.
3. Guan WJ, Ni ZY, Hu Y, et al. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med, 2020, 382(18): 1708-1720.
4. King CS, Mannem H, Kukreja J, et al. Lung transplantation for patients with COVID-19. Chest, 2022, 161(1): 169-178.
5. Wu C, Chen X, Cai Y, et al. Risk factors associated with acute respiratory distress syndrome and death in patients with coronavirus disease 2019 pneumonia in Wuhan, China. JAMA Intern Med, 2020, 180(7): 934-943.
6. Horby P, Lim WS, Emberson JR, et al. Dexamethasone in hospitalized patients with COVID-19. N Engl J Med, 2021, 384(8): 693-704.
7. Group RC. Dexamethasone in hospitalized patients with COVID-19. N Engl J Med, 2021, 384(8): 693-704.
8. Beigel JH, Tomashek KM, Dodd LE, et al. Remdesivir for the treatment of COVID-19—Final report. N Engl J Med, 2020, 383(19): 1813-1826.
9. McDonald LT. Healing after COVID-19: Are survivors at risk for pulmonary fibrosis? Am J Physiol Lung Cell Mol Physiol, 2021, 320(2): L257-L265.
10. Schaheen L, Bremner RM, Walia R, et al. Lung transplantation for coronavirus disease 2019 (COVID-19): The who, what, where, when, and why. J Thorac Cardiovasc Surg, 2022, 163(3): 865-868.
11. Van Der Mark SC, Hoek RAS, Hellemons ME. Developments in lung transplantation over the past decade. Eur Respir Rev, 2020, 29(157): 190132.
12. Valapour M, Lehr CJ, Skeans MA, et al. OPTN/SRTR 2016 annual data report: Lung. Am J Transplant, 2018, 18(Suppl 1): 363-433.
13. Chambers DC, Cherikh WS, Harhay MO, et al. The International Thoracic Organ Transplant Registry of the International Society for Heart and Lung Transplantation: Thirty-sixth adult lung and heart-lung transplantation Report-2019; Focus theme: Donor and recipient size match. J Heart Lung Transplant, 2019, 38(10): 1042-1055.
14. Erasmus ME, van der Bij W. Death after lung transplantation: Improving long term survival despite perilous early postoperative years. Transpl Int, 2020, 33(2): 128-129.
15. Bharat A, Querrey M, Markov NS, et al. Lung transplantation for patients with severe COVID-19. Sci Transl Med, 2020, 12(574): eabe4282.
16. Sahin MF, Beyoglu MA, Turkkan S, et al. Donor lung evaluation and lung transplantation in the COVID-19 era. Exp Clin Transplant, 2022, 20(9): 842-848.
17. Cerier E, Lung K, Kurihara C, et al. Lung transplantation in coronavirus-19 patients: What we have learned so far. Clin Chest Med, 2023, 44(2): 347-357.
18. Fernandes LM, Pêgo-Fernandes PM. New challenges for lung transplantation in the era of COVID-19. Sao Paulo Med J, 2022, 140(1): 1-4.
19. 中华医学会器官移植学分会. 中国肺移植受者选择与术前评估技术规范 (2019 版). 中华移植杂志: 电子版, 2019, 13(2) : 81-86.Chinese Society of Organ Transplantation, Chinese Medical Association. Technical specifications for recipient selection and preoperative evaluation of lung transplantation in China (2019 Edition). Chin J Transplant (Electronic Edition), 2019, 13(2): 81-86.
20. Bharat A, Machuca TN, Querrey M, et al. Early outcomes after lung transplantation for severe COVID-19: A series of the first consecutive cases from four countries. Lancet Respir Med, 2021, 9(5): 487-497.
21. Han X, Fan Y, Alwalid O, et al. Six-month follow-up chest CT findings after severe COVID-19 pneumonia. Radiology, 2021, 299(1): E177-E186.
22. Tabatabaei SMH, Rajebi H, Moghaddas F, et al. Chest CT in COVID-19 pneumonia: What are the findings in mid-term follow-up? Emerg Radiol, 2020, 27(6): 711-719.
23. Huang Y, Tan C, Wu J, et al. Impact of coronavirus disease 2019 on pulmonary function in early convalescence phase. Respir Res, 2020, 21(1): 163.
24. Guler SA, Ebner L, Aubry-Beigelman C, et al. Pulmonary function and radiological features 4 months after COVID-19: First results from the national prospective observational Swiss COVID-19 lung study. Eur Respir J, 2021, 57(4): 2003690.
25. Ojo AS, Balogun SA, Williams OT, et al. Pulmonary fibrosis in COVID‐19 survivors: Predictive factors and risk reduction strategies. Pulmonary medicine, 2020, 2020(1): 6175964.
26. Evans RA, McAuley H, Harrison EM, et al. Physical, cognitive, and mental health impacts of COVID-19 after hospitalisation (PHOSP-COVID): A UK multicentre, prospective cohort study. Lancet Respir Med, 2021, 9(11): 1275-1287.
27. Hui DS, Joynt GM, Wong KT, et al. Impact of severe acute respiratory syndrome (SARS) on pulmonary function, functional capacity and quality of life in a cohort of survivors. Thorax, 2005, 60(5): 401-409.
28. Wong KT, Antonio GE, Hui DS, et al. Severe acute respiratory syndrome: Thin-section computed tomography features, temporal changes, and clinicoradiologic correlation during the convalescent period. J Comput Assist Tomogr, 2004, 28(6): 790-795.
29. Bazdyrev E, Rusina P, Panova M, et al. Lung fibrosis after COVID-19: Treatment prospects. Pharmaceuticals (Basel), 2021, 14(8): 807.
30. Kurihara C, Manerikar A, Querrey M, et al. Clinical characteristics and outcomes of patients with COVID-19-associated acute respiratory distress syndrome who underwent lung transplant. JAMA, 2022, 327(7): 652-661.
31. 《新型冠状病毒感染防控方案(试行第十版)》. URL: http://www.nhc.gov.cn/xcs/zhengcwj/202301/bdc1ff75feb94934ae1dade176d30936.shtml. Accessed on 2024-10-02.Prevention and Control Plan for Novel Coronavirus Infection (Tenth Trial Edition)". URL: http://www.nhc.gov.cn/xcs/zhengcwj/202301/bdc1ff75feb94934ae1dade176d30936.shtml. Accessed on 2024-10-02.
32. Yin S, Wang X, Song T. Tacrolimus use and COVID-19 infection in patients after solid organ transplantation. Gastroenterology, 2021, 161(2): 728-730.
33. Belli LS, Fondevila C, Cortesi PA, et al. Protective role of tacrolimus, deleterious role of age and comorbidities in liver transplant recipients with COVID-19: Results from the ELITA/ELTR multi-center European study. Gastroenterology, 2021, 160(4): 1151-1163.
34. Karruli A, Spiezia S, Boccia F, et al. Effect of immunosuppression maintenance in solid organ transplant recipients with COVID-19: Systematic review and meta-analysis. Transpl Infect Dis, 2021, 23(4): e13595.
35. Helleberg M, Niemann CU, Moestrup KS, et al. Persistent COVID-19 in an immunocompromised patient temporarily responsive to two courses of remdesivir therapy. J Infect Dis, 2020, 222(7): 1103-1107.
36. Trottier CA, Wong B, Kohli R, et al. Dual antiviral therapy for persistent coronavirus disease 2019 and associated organizing pneumonia in an immunocompromised host. Clin Infect Dis, 2023, 76(5): 923-925.
37. Martinez MA, Chen TY, Choi H, et al. Extended remdesivir infusion for persistent coronavirus disease 2019 infection. Proceedings of the Open Forum Infectious Diseases, F. 2022. Oxford University Press.
38. Marjot T, Webb GJ, Barritt AS, et al. COVID-19 and liver disease: Mechanistic and clinical perspectives. Nat Rev Gastroenterol Hepatol, 2021, 18(5): 348-364.
39. Chen Z, Xu W, Ma W, et al. Clinical laboratory evaluation of COVID-19. Clin Chim Acta, 2021, 519: 172-182.519-172.
40. Karakoyun I, Colak A, Turken M, et al. Diagnostic utility of C-reactive protein to albumin ratio as an early warning sign in hospitalized severe COVID-19 patients. Int Immunopharmacol, 2021, 91: 107285.
41. Liu X, Yue X, Liu F, et al. Analysis of clinical features and early warning signs in patients with severe COVID-19: A retrospective cohort study. PLoS One, 2020, 15(6): e0235459.
42. Wang X, Che Q, Ji X, et al. Correlation between lung infection severity and clinical laboratory indicators in patients with COVID-19: A cross-sectional study based on machine learning. BMC Infect Dis, 2021, 21(1): 192.
43. Guo J, Wang S, Xia H, et al. Cytokine signature associated with disease severity in COVID-19. Front Immunol, 2021, 20: 12: 681516.
44. Mitchell O, Cosar AM, Malik MU, et al. Late liver function test abnormalities post-adult liver transplantation: A review of the etiology, investigation, and management. Hepatol Int, 2016, 10(1): 106-114.
45. Wadei HM, Lee DD, Croome KP, et al. Early allograft dysfunction after liver transplantation is associated with short- and long-term kidney function impairment. Am J Transplant, 2016, 16(3): 850-859.
46. Buchan TA, Moayedi Y, Truby LK, et al. Incidence and impact of primary graft dysfunction in adult heart transplant recipients: A systematic review and meta-analysis. J Heart Lung Transplant, 2021, 40(7): 642-651.
47. Shah RJ, Diamond JM. Primary graft dysfunction (PGD) following lung transplantation. Proceedings of the seminars in respiratory and critical care medicine, F, 2018. Thieme Medical Publishers.
48. Roach A, Chikwe J, Catarino P, et al. Lung transplantation for COVID19 related respiratory failure in the United States. N Engl J Med, 2022, 386(12): 1187-1188.

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