COVID-19 Infection in Heart Transplant Recipients: Results of a Six-Month Prospective Survey-Based Study
-
Vahideh Lalehfar
,
Farnoosh Larti
,
Ali Mehrakizadeh
,
Alireza Bakhshandeh
,
Roya Sattarzadeh Badkoubeh
,
Shabnam Mohammadzadeh
,
Akram Sardari
Abstract
Solid-organ transplantation recipients were assumed highly vulnerable to coronavirus disease 2019 (COVID-19). However, the results of previous studies in patients with orthotopic heart transplantation (OHT) under immunosuppressive therapy are contradictory. Therefore, we aimed to assess the prevalence of COVID-19 infection and associated risk factors, along with the six-month outcomes in COVID-19 positive OHT patients. This single-center telephone-based survey was conducted on OHT patients. Using a detailed questionnaire, exposure to COVID-19, related symptoms, and preventive self-care measures were collected. Outcomes of COVID-19-positive patients were reassessed using another survey six months later. 118 OHT patients (male: n=87, 73.7%) were included with a mean age of 45.3±13.1 years. Sixteen patients (13.5%) reported one or more symptoms compatible with COVID-19, of whom 12 (10.2%) tested positive. Our results indicated no statistically significant association between COVID-19 and comorbidities. Poor adherence to self-care measures and contact with positive index cases were both significantly associated with COVID-19 infection (P<0.001). A later six months follow-up showed that two out of 12 (16.6%) COVID-19 positive OHT patients died. There was no statistically significant difference between the prevalence of COVID-19 in our patients compared to Iran’s general population (P=0.152). Non-compliance with personal protective protocols and a history of contact with COVID-19 cases were the most risk factors for COVID-19 infection in OHT patients.
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3. Decerf B, Ferreira FHG, Mahler DG, Sterck O. Lives and livelihoods: Estimates of the global mortality and poverty effects of the Covid-19 pandemic. World Dev 2021;146:105561.
4. Meshram HS, Kute VB, Patel H, Banerjee S, Navadiya V, Desai S, et al. Feasibility and safety of remdesivir in SARS‐CoV2 infected renal transplant recipients: A retrospective cohort from a developing nation. Transpl Infect Dis 2021;23:e13629.
5. Guan W, Ni Z, Hu Y, Liang W, Ou C, He J, et al. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med 2020;382:1708-20.
6. Zhou F, Yu T, Du R, Fan G, Liu Y, Liu Z, et al. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet 2020;395:1054-62.
7. Rivinius R, Kaya Z, Schramm R, Boeken U, Provaznik Z, Heim C, et al. COVID-19 among heart transplant recipients in Germany: a multicenter survey. Clin Res Cardiol 2020;109:1531-9.
8. Coll E, Fernández-Ruiz M, Sánchez-Álvarez JE, Martínez-Fernández JR, Crespo M, Gayoso J, et al. COVID-19 in transplant recipients: The Spanish experience. Am J Transplant 2021;21:1825-37.
9. Akalin E, Azzi Y, Bartash R, Seethamraju H, Parides M, Hemmige V, et al. Covid-19 and kidney transplantation. N Engl J Med 2020;382:2475-7.
10. Pereira MR, Mohan S, Cohen DJ, Husain SA, Dube GK, Ratner LE, et al. COVID‐19 in solid organ transplant recipients: initial report from the US epicenter. Am J Transplant 2020;20:1800-8.
11. Crespo‐Leiro MG, Metra M, Lund LH, Milicic D, Costanzo MR, Filippatos G, et al. Advanced heart failure: a position statement of the Heart Failure Association of the European Society of Cardiology. Eur J Heart Fail 2018;20:1505-35.
12. Li F, Cai J, Dong N. First cases of COVID-19 in heart transplantation from China. J Hear Lung Transplant 2020;39:496-7.
13. Schoot TS, Kerckhoffs APM, Hilbrands LB, van Marum RJ. Immunosuppressive Drugs and COVID-19: A Review Front Pharmacol 2020;11:1333.
14. Abdelrahman Z, Liu Q, Jiang S, Li M, Sun Q, Zhang Y, et al. Evaluation of the Current Therapeutic Approaches for COVID-19: A Systematic Review and a Meta-analysis. Front Pharmacol 2021;12:607408.
15. Kates OS, Fisher CE, Stankiewicz‐Karita HC, Shepherd AK, Church EC, Kapnadak SG, et al. Earliest cases of coronavirus disease 2019 (COVID‐19) identified in solid organ transplant recipients in the United States. Am J Transplant 2020;20:1885-90.
16. Mohammadzadeh S, Mehrakizadeh A, Safari S, Mirzaaghayan M, Badkoubeh RS, Tavoosi A, et al. Lessons learnt from COVID-19 in adult congenital heart patient in Tehran: a survey-based study of prevention, exposure, susceptibility, and outcomes. Cardiol Young 2021;31:617-26.
17. Zhang SY, Lian JS, Hu JH, Zhang XL, Lu YF, Cai H, et al. Clinical characteristics of different subtypes and risk factors for the severity of illness in patients with COVID-19 in Zhejiang, China. Infect Dis Poverty 2020;9:85.
18. Khalagi K, Gharibzadeh S, Khalili D, Mansournia MA, Mirab Samiee S, Aghamohamadi S, et al. Prevalence of COVID-19 in Iran: results of the first survey of the Iranian COVID-19 Serological Surveillance programme. Clin Microbiol Infect 2021;27:1666-71.
19. Marinelli T, Wee LYA, Rowe E, Chhetri R, Friel O, Higgins G, et al. Respiratory viruses cause late morbidity in recipients of hematopoietic stem cell transplantation. Biol Blood Marrow Transplant 2020;26:782-8.
20. Abbas S, Raybould JE, Sastry S, de la Cruz O. Respiratory viruses in transplant recipients: more than just a cold. Clinical syndromes and infection prevention principles. Int J Infect Dis 2017;62:86-93.
21. Lee C, Choi WJ. Overview of COVID-19 inflammatory pathogenesis from the therapeutic perspective. Arch Pharm Res 2021;44:99-116.
22. Chen G, Wu DI, Guo W, Cao Y, Huang D, Wang H, et al. Clinical and immunological features of severe and moderate coronavirus disease 2019. J Clin Invest 2020;130:2620-9.
23. Tomaso B, Lorenzo B, Alessandro F, Matteo N, Raphael C, Olimpia B, et al. COVID-19 in Heart Transplant Recipients. JACC Hear Fail 2021;9:52-61.
24. Al‐Darzi W, Aurora L, Michaels A, Cowger J, Grafton G, Selektor Y, et al. Heart transplant recipients with confirmed 2019 novel coronavirus infection: The Detroit experience. Clin Transplant 2020;34:e14091.
25. Latif F, Farr MA, Clerkin KJ, Habal MV, Takeda K, Naka Y, et al. Characteristics and outcomes of recipients of heart transplant with coronavirus disease 2019. JAMA Cardiol 2020;5:1165-9.
26. Raja MA, Mendoza MA, Villavicencio A, Anjan S, Reynolds JM, Kittipibul V, et al. COVID-19 in solid organ transplant recipients: A systematic review and meta-analysis of current literature. Transplant Rev (Orlando) 2021;35:100588.
27. Buitrago-Garcia D, Egli-Gany D, Counotte MJ, Hossmann S, Imeri H, Ipekci AM, et al. Occurrence and transmission potential of asymptomatic and presymptomatic SARS-CoV-2 infections: A living systematic review and meta-analysis. PLoS Med 2020;17:e1003346.
28. Pizzo PA. Fever in Immunocompromised Patients. N Engl J Med 1999;341:893-900.
29. Verma A, Khorsandi SE, Dolcet A, Prachalias A, Suddle A, Heaton N, et al. Low prevalence and disease severity of COVID-19 in post-liver transplant recipients—A single centre experience. Liver Int 2020;40:1972-6.
30. Singhvi A, Barghash M, Lala A, Mitter SS, Parikh A, Oliveros E, et al. Challenges in heart transplantation during COVID-19: a single-center experience. J Hear Lung Transplant 2020;39:894-903.
31. Azzi Y, Bartash R, Scalea J, Loarte-Campos P, Akalin E. COVID-19 and Solid Organ Transplantation: A Review Article. Transplantation 2021;105, 37-55.
32. Mehta P, McAuley DF, Brown M, Sanchez E, Tattersall RS, Manson JJ. COVID-19: consider cytokine storm syndromes and immunosuppression. Lancet 2020;395:1033-4.
33. Zhao M. Cytokine storm and immunomodulatory therapy in COVID-19: role of chloroquine and anti-IL-6 monoclonal antibodies. Int J Antimicrob Agents 2020;55:105982.
34. Willicombe M, Thomas D, McAdoo S. COVID-19 and calcineurin inhibitors: should they get left out in the storm? J Am Soc Nephrol 2020;31:1145-6.
35. Letizia C, d’Ambrosio C, De Ciocchis A, Scavo D, Pozzilli P. Serum angiotensin-converting enzyme levels in patients with recent-onset insulin-dependent diabetes after one year of low-dose cyclosporin therapy. IMDIAB Study Group. Int J Clin Pharmacol Res 1995;15:209-13.
36. Hošková L, Málek I, Kautzner J, Honsová E, van Dokkum RPE, Husková Z, et al. Tacrolimus-induced hypertension and nephrotoxicity in Fawn-Hooded rats are attenuated by dual inhibition of renin–angiotensin system. Hypertens Res 2014;37:724-32.
37. Kupferman JC, Beaudoin R, Carr R, Hay D, Casellas D, Kaskel FJ, et al. Activation of the renal renin-angiotensin system by cyclosporine A and FK 506 in the rat. Transplant Proc 1994;5:2891-3.
38. Julien J, Farge D, Kreft-Jais C, Guyene TT, Plouin PF, Houssin D, et al. Cyclosporine-induced stimulation of the renin-angiotensin system after liver and heart transplantation. Transplantation 1993;56:885-91.
39. Schreiber SL, Crabtree GR. The mechanism of action of cyclosporin A and FK506. Immunol Today 1992;13:136-42.
2. Jee Y. WHO international health regulations emergency committee for the COVID-19 outbreak. Epidemiol Health 2020;42:e2020013.
3. Decerf B, Ferreira FHG, Mahler DG, Sterck O. Lives and livelihoods: Estimates of the global mortality and poverty effects of the Covid-19 pandemic. World Dev 2021;146:105561.
4. Meshram HS, Kute VB, Patel H, Banerjee S, Navadiya V, Desai S, et al. Feasibility and safety of remdesivir in SARS‐CoV2 infected renal transplant recipients: A retrospective cohort from a developing nation. Transpl Infect Dis 2021;23:e13629.
5. Guan W, Ni Z, Hu Y, Liang W, Ou C, He J, et al. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med 2020;382:1708-20.
6. Zhou F, Yu T, Du R, Fan G, Liu Y, Liu Z, et al. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet 2020;395:1054-62.
7. Rivinius R, Kaya Z, Schramm R, Boeken U, Provaznik Z, Heim C, et al. COVID-19 among heart transplant recipients in Germany: a multicenter survey. Clin Res Cardiol 2020;109:1531-9.
8. Coll E, Fernández-Ruiz M, Sánchez-Álvarez JE, Martínez-Fernández JR, Crespo M, Gayoso J, et al. COVID-19 in transplant recipients: The Spanish experience. Am J Transplant 2021;21:1825-37.
9. Akalin E, Azzi Y, Bartash R, Seethamraju H, Parides M, Hemmige V, et al. Covid-19 and kidney transplantation. N Engl J Med 2020;382:2475-7.
10. Pereira MR, Mohan S, Cohen DJ, Husain SA, Dube GK, Ratner LE, et al. COVID‐19 in solid organ transplant recipients: initial report from the US epicenter. Am J Transplant 2020;20:1800-8.
11. Crespo‐Leiro MG, Metra M, Lund LH, Milicic D, Costanzo MR, Filippatos G, et al. Advanced heart failure: a position statement of the Heart Failure Association of the European Society of Cardiology. Eur J Heart Fail 2018;20:1505-35.
12. Li F, Cai J, Dong N. First cases of COVID-19 in heart transplantation from China. J Hear Lung Transplant 2020;39:496-7.
13. Schoot TS, Kerckhoffs APM, Hilbrands LB, van Marum RJ. Immunosuppressive Drugs and COVID-19: A Review Front Pharmacol 2020;11:1333.
14. Abdelrahman Z, Liu Q, Jiang S, Li M, Sun Q, Zhang Y, et al. Evaluation of the Current Therapeutic Approaches for COVID-19: A Systematic Review and a Meta-analysis. Front Pharmacol 2021;12:607408.
15. Kates OS, Fisher CE, Stankiewicz‐Karita HC, Shepherd AK, Church EC, Kapnadak SG, et al. Earliest cases of coronavirus disease 2019 (COVID‐19) identified in solid organ transplant recipients in the United States. Am J Transplant 2020;20:1885-90.
16. Mohammadzadeh S, Mehrakizadeh A, Safari S, Mirzaaghayan M, Badkoubeh RS, Tavoosi A, et al. Lessons learnt from COVID-19 in adult congenital heart patient in Tehran: a survey-based study of prevention, exposure, susceptibility, and outcomes. Cardiol Young 2021;31:617-26.
17. Zhang SY, Lian JS, Hu JH, Zhang XL, Lu YF, Cai H, et al. Clinical characteristics of different subtypes and risk factors for the severity of illness in patients with COVID-19 in Zhejiang, China. Infect Dis Poverty 2020;9:85.
18. Khalagi K, Gharibzadeh S, Khalili D, Mansournia MA, Mirab Samiee S, Aghamohamadi S, et al. Prevalence of COVID-19 in Iran: results of the first survey of the Iranian COVID-19 Serological Surveillance programme. Clin Microbiol Infect 2021;27:1666-71.
19. Marinelli T, Wee LYA, Rowe E, Chhetri R, Friel O, Higgins G, et al. Respiratory viruses cause late morbidity in recipients of hematopoietic stem cell transplantation. Biol Blood Marrow Transplant 2020;26:782-8.
20. Abbas S, Raybould JE, Sastry S, de la Cruz O. Respiratory viruses in transplant recipients: more than just a cold. Clinical syndromes and infection prevention principles. Int J Infect Dis 2017;62:86-93.
21. Lee C, Choi WJ. Overview of COVID-19 inflammatory pathogenesis from the therapeutic perspective. Arch Pharm Res 2021;44:99-116.
22. Chen G, Wu DI, Guo W, Cao Y, Huang D, Wang H, et al. Clinical and immunological features of severe and moderate coronavirus disease 2019. J Clin Invest 2020;130:2620-9.
23. Tomaso B, Lorenzo B, Alessandro F, Matteo N, Raphael C, Olimpia B, et al. COVID-19 in Heart Transplant Recipients. JACC Hear Fail 2021;9:52-61.
24. Al‐Darzi W, Aurora L, Michaels A, Cowger J, Grafton G, Selektor Y, et al. Heart transplant recipients with confirmed 2019 novel coronavirus infection: The Detroit experience. Clin Transplant 2020;34:e14091.
25. Latif F, Farr MA, Clerkin KJ, Habal MV, Takeda K, Naka Y, et al. Characteristics and outcomes of recipients of heart transplant with coronavirus disease 2019. JAMA Cardiol 2020;5:1165-9.
26. Raja MA, Mendoza MA, Villavicencio A, Anjan S, Reynolds JM, Kittipibul V, et al. COVID-19 in solid organ transplant recipients: A systematic review and meta-analysis of current literature. Transplant Rev (Orlando) 2021;35:100588.
27. Buitrago-Garcia D, Egli-Gany D, Counotte MJ, Hossmann S, Imeri H, Ipekci AM, et al. Occurrence and transmission potential of asymptomatic and presymptomatic SARS-CoV-2 infections: A living systematic review and meta-analysis. PLoS Med 2020;17:e1003346.
28. Pizzo PA. Fever in Immunocompromised Patients. N Engl J Med 1999;341:893-900.
29. Verma A, Khorsandi SE, Dolcet A, Prachalias A, Suddle A, Heaton N, et al. Low prevalence and disease severity of COVID-19 in post-liver transplant recipients—A single centre experience. Liver Int 2020;40:1972-6.
30. Singhvi A, Barghash M, Lala A, Mitter SS, Parikh A, Oliveros E, et al. Challenges in heart transplantation during COVID-19: a single-center experience. J Hear Lung Transplant 2020;39:894-903.
31. Azzi Y, Bartash R, Scalea J, Loarte-Campos P, Akalin E. COVID-19 and Solid Organ Transplantation: A Review Article. Transplantation 2021;105, 37-55.
32. Mehta P, McAuley DF, Brown M, Sanchez E, Tattersall RS, Manson JJ. COVID-19: consider cytokine storm syndromes and immunosuppression. Lancet 2020;395:1033-4.
33. Zhao M. Cytokine storm and immunomodulatory therapy in COVID-19: role of chloroquine and anti-IL-6 monoclonal antibodies. Int J Antimicrob Agents 2020;55:105982.
34. Willicombe M, Thomas D, McAdoo S. COVID-19 and calcineurin inhibitors: should they get left out in the storm? J Am Soc Nephrol 2020;31:1145-6.
35. Letizia C, d’Ambrosio C, De Ciocchis A, Scavo D, Pozzilli P. Serum angiotensin-converting enzyme levels in patients with recent-onset insulin-dependent diabetes after one year of low-dose cyclosporin therapy. IMDIAB Study Group. Int J Clin Pharmacol Res 1995;15:209-13.
36. Hošková L, Málek I, Kautzner J, Honsová E, van Dokkum RPE, Husková Z, et al. Tacrolimus-induced hypertension and nephrotoxicity in Fawn-Hooded rats are attenuated by dual inhibition of renin–angiotensin system. Hypertens Res 2014;37:724-32.
37. Kupferman JC, Beaudoin R, Carr R, Hay D, Casellas D, Kaskel FJ, et al. Activation of the renal renin-angiotensin system by cyclosporine A and FK 506 in the rat. Transplant Proc 1994;5:2891-3.
38. Julien J, Farge D, Kreft-Jais C, Guyene TT, Plouin PF, Houssin D, et al. Cyclosporine-induced stimulation of the renin-angiotensin system after liver and heart transplantation. Transplantation 1993;56:885-91.
39. Schreiber SL, Crabtree GR. The mechanism of action of cyclosporin A and FK506. Immunol Today 1992;13:136-42.
| Files | ||
| Issue | Vol 60, No 6 (2022) | |
| Section | Articles | |
| DOI | https://doi.org/10.18502/acta.v60i6.10037 | |
| Keywords | ||
| Coronavirus disease 2019 (COVID-19) Heart transplantation Immunosuppression Preventive self-care measures Telephone-based survey | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Lalehfar V, Larti F, Mehrakizadeh A, Bakhshandeh A, Sattarzadeh Badkoubeh R, Mohammadzadeh S, Sardari A. COVID-19 Infection in Heart Transplant Recipients: Results of a Six-Month Prospective Survey-Based Study. Acta Med Iran. 2022;60(6):329-337.
