COVID-19 in Immunocompromised Patients: A Systematic Review

Anna Stainer; Francesco Amati; Giulia Suigo; Edoardo Simonetta; Andrea Gramegna; Antonio Voza; Stefano Aliberti

doi:10.1055/s-0041-1740110

Seminars in Respiratory and Critical Care Medicine, Table of Contents

Semin Respir Crit Care Med 2021; 42(06): 839-858
DOI: 10.1055/s-0041-1740110

Review Article

COVID-19 in Immunocompromised Patients: A Systematic Review

Anna Stainer

¹Department of Biomedical Sciences, Humanitas University, Pieve Emanuele, Milan, Italy

²Respiratory Unit, IRCCS Humanitas Research Hospital, Rozzano, Milan, Italy

,

Francesco Amati

¹Department of Biomedical Sciences, Humanitas University, Pieve Emanuele, Milan, Italy

²Respiratory Unit, IRCCS Humanitas Research Hospital, Rozzano, Milan, Italy

,

Giulia Suigo

²Respiratory Unit, IRCCS Humanitas Research Hospital, Rozzano, Milan, Italy

,

Edoardo Simonetta

³Department of Pathophysiology and Transplantation, University of Milan, Milan, Italy

⁴Fondazione IRCCS Ca' Granda, Ospedale Maggiore Policlinico, Respiratory Department, Milan, Italy

,

Andrea Gramegna

³Department of Pathophysiology and Transplantation, University of Milan, Milan, Italy

⁴Fondazione IRCCS Ca' Granda, Ospedale Maggiore Policlinico, Respiratory Department, Milan, Italy

,

Antonio Voza

¹Department of Biomedical Sciences, Humanitas University, Pieve Emanuele, Milan, Italy

⁵Emergency Medicine Unit, IRCCS Humanitas Research Hospital, Rozzano, Milan, Italy

,

Stefano Aliberti

¹Department of Biomedical Sciences, Humanitas University, Pieve Emanuele, Milan, Italy

²Respiratory Unit, IRCCS Humanitas Research Hospital, Rozzano, Milan, Italy

› Author Affiliations

Abstract

Severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) was first identified as a novel coronavirus in Wuhan, Hubei province, central China, in December 2019, and is responsible for the 2019-to-present pandemic. According to the most recent data released by the World Health Organization, more than 200 million people have been infected by SARS-CoV-2 so far, and more than 4 million people died worldwide. Although our knowledge on SARS-CoV-2 and COVID-19 is constantly growing, data on COVID-19 in immunocompromised patients are still limited. The aim of the present systematic review is to describe clinical picture, disease severity, proposed treatment regimen, and response to vaccination in patients with different types and severity of immunosuppression.

Keywords

COVID-19 - immunosuppression - SARS-CoV-2

Full Text

References

References
1 Huang C, Wang Y, Li X. et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 2020; 395 (10223): 497-506
2 Weekly epidemiological update on COVID-19—28 September 2021. CE [cited October 11, 2021]. Available at: https://www.who.int/publications/m/item/weekly-epidemiological-update-on-covid-19—28-september-2021
3 Lotfi M, Hamblin MR, Rezaei N. COVID-19: Transmission, prevention, and potential therapeutic opportunities. Clin Chim Acta 2020; 508: 254-266
4 Guan W-J, Ni Z-Y, Hu Y. et al; China Medical Treatment Expert Group for COVID-19. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med 2020; 382 (18) 1708-1720
5 Colavita F, Lapa D, Carletti F. et al. SARS-CoV-2 isolation from ocular secretions of a patient with COVID-19 in Italy with prolonged viral RNA detection. Ann Intern Med 2020; 173 (03) 242-243
6 Recalcati S. Cutaneous manifestations in COVID-19: a first perspective. J Eur Acad Dermatol Venereol 2020; 34 (05) e212-e213
7 Annweiler C, Sacco G, Salles N. et al. National French Survey of coronavirus disease (COVID-19) symptoms in people aged 70 and over. Clin Infect Dis 2021; 72 (03) 490-494
8 Escher F, Pietsch H, Aleshcheva G. et al. Detection of viral SARS-CoV-2 genomes and histopathological changes in endomyocardial biopsies. ESC Heart Fail 2020; 7 (05) 2440-2447
9 Pun BT, Badenes R, Heras La Calle G. et al; COVID-19 Intensive Care International Study Group. Prevalence and risk factors for delirium in critically ill patients with COVID-19 (COVID-D): a multicentre cohort study. Lancet Respir Med 2021; 9 (03) 239-250
10 Mundula V, Stainer A, Motta F, Ciccarelli M. Two-month acute microangiopathic brain injury follow-up in severe COVID-19: a case report. Neuroimmunol Neuroinflammation [Internet]. . October 16, 2020 [cited January 5, 2021];7. Accessed October 30, 2021 at: https://nnjournal.net/article/view/3714
11 Aliberti S, Amati F, Pappalettera M. et al. COVID-19 multidisciplinary high dependency unit: the Milan model. Respir Res 2020; 21 (01) 260
12 Chalmers JD, Crichton ML, Goeminne PC. et al. Management of hospitalised adults with coronavirus disease 2019 (COVID-19): a European Respiratory Society living guideline. Eur Respir J 2021; 57 (04) 2100048
13 Mehta P, Fajgenbaum DC. Is severe COVID-19 a cytokine storm syndrome: a hyperinflammatory debate. Curr Opin Rheumatol 2021; 33 (05) 419-430
14 Moher D, Liberati A, Tetzlaff J, Altman DG. PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 2009; 6 (07) e1000097
15 Arya A, Li M, Aburjania N. et al. COVID-19 in solid organ transplantation: disease severity and clinical update. Transplant Proc 2021; 53 (04) 1227-1236
16 Tschopp J, L'Huillier AG, Mombelli M. et al; Swiss Transplant Cohort Study (STCS). First experience of SARS-CoV-2 infections in solid organ transplant recipients in the Swiss Transplant Cohort Study. Am J Transplant 2020; 20 (10) 2876-2882
17 de Melo AC, Thuler LCS, da Silva JL. et al; Brazilian National Cancer Institute COVID-19 Task Force. Cancer in patients with COVID-19: a report from the Brazilian National Cancer Institute. PLoS One 2020; 15 (10) e0241261
18 Brar G, Pinheiro LC, Shusterman M. et al. COVID-19 severity and outcomes in patients with cancer: a matched cohort study. J Clin Oncol 2020; 38 (33) 3914-3924
19 Broseta JJ, Rodríguez-Espinosa D, Cuadrado E. et al. SARS-CoV-2 infection in a Spanish cohort of CKD-5D patients: prevalence, clinical presentation, outcomes, and de-isolation results. Blood Purif 2021; 50 (4-5): 531-538
20 Lum E, Bunnapradist S, Multani A. et al. Spectrum of coronavirus disease 2019 outcomes in kidney transplant recipients: a single-center experience. Transplant Proc 2020; 52 (09) 2654-2658
21 Wang B, Van Oekelen O, Mouhieddine TH. et al. A tertiary center experience of multiple myeloma patients with COVID-19: lessons learned and the path forward. J Hematol Oncol 2020; 13 (01) 94
22 Messika J, Eloy P, Roux A. et al; French Group of Lung Transplantation. COVID-19 in lung transplant recipients. Transplantation 2021; 105 (01) 177-186
23 Dheir H, Sipahi S, Yaylacı S. et al. Clinical course of COVID-19 disease in immunosuppressed renal transplant patients. Turk J Med Sci 2021; 51 (02) 428-434
24 Thompson MA, Henderson JP, Shah PK. et al; COVID-19 and Cancer Consortium. Association of convalescent plasma therapy with survival in patients with hematologic cancers and COVID-19. JAMA Oncol 2021; 7 (08) 1167-1175
25 Reuken PA, Andreas N, Grunert PC, Glöckner S, Kamradt T, Stallmach A. T cell response after SARS-CoV-2 vaccination in immunocompromised patients with inflammatory bowel disease. J Crohn's Colitis 2021; jjab147
26 Medeiros-Ribeiro AC, Aikawa NE, Saad CGS. et al. Immunogenicity and safety of the CoronaVac inactivated vaccine in patients with autoimmune rheumatic diseases: a phase 4 trial. Nat Med 2021; 27 (10) 1744-1751
27 Braun-Moscovici Y, Kaplan M, Braun M. et al. Disease activity and humoral response in patients with inflammatory rheumatic diseases after two doses of the Pfizer mRNA vaccine against SARS-CoV-2. Ann Rheum Dis 2021; 80 (10) 1317-1321
28 Kappelman MD, Weaver KN, Boccieri M, Firestine A, Zhang X, Long MD. PREVENT-COVID Study Group. Humoral immune response to messenger RNA COVID-19 vaccines among patients with inflammatory bowel disease. Gastroenterology 2021; 161 (04) 1340-1343.e2
29 Furer V, Eviatar T, Zisman D. et al. Immunogenicity and safety of the BNT162b2 mRNA COVID-19 vaccine in adult patients with autoimmune inflammatory rheumatic diseases and in the general population: a multicentre study. Ann Rheum Dis 2021; 80 (10) 1330-1338
30 Geisen UM, Berner DK, Tran F. et al. Immunogenicity and safety of anti-SARS-CoV-2 mRNA vaccines in patients with chronic inflammatory conditions and immunosuppressive therapy in a monocentric cohort. Ann Rheum Dis 2021; 80 (10) 1306-1311
31 Mrak D, Tobudic S, Koblischke M. et al. SARS-CoV-2 vaccination in rituximab-treated patients: B cells promote humoral immune responses in the presence of T-cell-mediated immunity. Ann Rheum Dis 2021; 80 (10) 1345-1350
32 Peled Y, Ram E, Lavee J. et al. BNT162b2 vaccination in heart transplant recipients: clinical experience and antibody response. J Heart Lung Transplant 2021; 40 (08) 759-762
33 Rosenthal N, Cao Z, Gundrum J, Sianis J, Safo S. Risk factors associated with in-hospital mortality in a US national sample of patients with COVID-19. JAMA Netw Open 2020; 3 (12) e2029058
34 Williamson EJ, Walker AJ, Bhaskaran K. et al. Factors associated with COVID-19-related death using OpenSAFELY. Nature 2020; 584 (7821): 430-436
35 Saini KS, Tagliamento M, Lambertini M. et al. Mortality in patients with cancer and coronavirus disease 2019: a systematic review and pooled analysis of 52 studies. Eur J Cancer 2020; 139: 43-50
36 Western Cape Department of Health in collaboration with the National Institute for Communicable Diseases, South Africa. Risk factors for coronavirus disease 2019 (COVID-19) death in a population cohort study from the Western Cape Province, South Africa. Clin Infect Dis 2021; 73 (07) e2005-e2015
37 Aziz F, Mandelbrot D, Singh T. et al. Early report on published outcomes in kidney transplant recipients compared to nontransplant patients infected with coronavirus disease 2019. Transplant Proc 2020; 52 (09) 2659-2662
38 Morlacchi LC, Rossetti V, Gigli L. et al. COVID-19 in lung transplant recipients: a case series from Milan, Italy. Transpl Infect Dis 2020; 22 (06) e13356
39 Gao Y, Chen Y, Liu M, Shi S, Tian J. Impacts of immunosuppression and immunodeficiency on COVID-19: a systematic review and meta-analysis. J Infect 2020; 81 (02) e93-e95
40 Vespro V, Andrisani MC, Fusco S. et al. Chest X-ray findings in a large cohort of 1117 patients with SARS-CoV-2 infection: a multicenter study during COVID-19 outbreak in Italy. Intern Emerg Med 2021; 16 (05) 1173-1181
41 Altmayer S, Zanon M, Pacini GS. et al. Comparison of the computed tomography findings in COVID-19 and other viral pneumonia in immunocompetent adults: a systematic review and meta-analysis. Eur Radiol 2020; 30 (12) 6485-6496
42 Kunihiro Y, Tanaka N, Kawano R. et al. Differentiation of pulmonary complications with extensive ground-glass attenuation on high-resolution CT in immunocompromised patients. Jpn J Radiol 2021; 39 (09) 868-876
43 Szydłowicz M, Matos O. Pneumocystis pneumonia in the COVID-19 pandemic era: similarities and challenges. Trends Parasitol 2021; 37 (10) 859-862
44 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
45 Focosi D, Anderson AO, Tang JW, Tuccori M. Convalescent plasma therapy for COVID-19: state of the art. Clin Microbiol Rev 2020; 33 (04) e00072-e20
46 Blasi F, Gramegna A, Sotgiu G. et al. SARS-CoV-2 vaccines: a critical perspective through efficacy data and barriers to herd immunity. Respir Med 2021; 180: 106355
47 Huang C, Huang L, Wang Y. et al. 6-month consequences of COVID-19 in patients discharged from hospital: a cohort study. Lancet 2021; 397 (10270): 220-232
48 Huang L, Yao Q, Gu X. et al. 1-year outcomes in hospital survivors with COVID-19: a longitudinal cohort study. Lancet 2021; 398 (10302): 747-758
49 Wu X, Liu X, Zhou Y. et al. 3-month, 6-month, 9-month, and 12-month respiratory outcomes in patients following COVID-19-related hospitalisation: a prospective study. Lancet Respir Med 2021; 9 (07) 747-754
50 Faverio P, Luppi F, Rebora P. et al. Six-month pulmonary impairment after severe COVID-19: a prospective, multicentre follow-up study. Respir Int Rev Thorac Dis 2021; 100 (11) 1078-1087
51 Guchelaar NAD, van Laar JAM, Hermans MAW. et al. Characteristics of COVID-19 infection and antibody formation in patients known at a tertiary immunology department. J Transl Autoimmun 2021; 4: 100084
52 Scharrer S, Kutschera M, Weseslindtner L, Primas C, Vogelsang H. Humoral response to COVID-19 infection in immunosuppressed patients with inflammatory bowel disease. Eur J Gastroenterol Hepatol 2021; 33 (03) 443-447
53 Bakasis A-D, Mavragani CP, Boki KA. et al. COVID-19 infection among autoimmune rheumatic disease patients: data from an observational study and literature review. J Autoimmun 2021; 123: 102687
54 Loinaz C, Marcacuzco A, Fernández-Ruiz M. et al. Varied clinical presentation and outcome of SARS-CoV-2 infection in liver transplant recipients: Initial experience at a single center in Madrid, Spain. Transpl Infect Dis 2020; 22 (05) e13372
55 Krasnow MR, Litt HK, Lehmann CJ, Lio J, Zhu M, Sherer R. Cancer, transplant, and immunocompromising conditions were not significantly associated with severe illness or death in hospitalized COVID-19 patients. J Clin Virol 2021; 140: 104850
56 El Fakih R, Haroon A, Alfraih F. et al. Clinical course and outcomes of COVID-19 in hematopoietic cell transplant patients, a regional report from the Middle East. Bone Marrow Transplant 2021; 56 (09) 2144-2151
57 Sran K, Olsburgh J, Kasimatis T. et al. COVID-19 in kidney transplant patients from a large UK transplant center: exploring risk factors for disease severity. Transplant Proc 2021; 53 (04) 1160-1168
58 Colmenero J, Rodríguez-Perálvarez M, Salcedo M. et al. Epidemiological pattern, incidence, and outcomes of COVID-19 in liver transplant patients. J Hepatol 2021; 74 (01) 148-155
59 Roberts MB, Izzy S, Tahir Z, Al Jarrah A, Fishman JA, El Khoury J. COVID-19 in solid organ transplant recipients: dynamics of disease progression and inflammatory markers in ICU and non-ICU admitted patients. Transpl Infect Dis 2020; 22 (05) e13407
60 Yi SG, Rogers AW, Saharia A. et al. Early experience with COVID-19 and solid organ transplantation at a US high-volume transplant center. Transplantation 2020; 104 (11) 2208-2214
61 Kenig A, Ishay Y, Kharouf F, Rubin L. Treatment of B-cell depleted COVID-19 patients with convalescent plasma and plasma-based products. Clin Immunol 2021; 227: 108723
62 Gupta A, Kute VB, Patel HV. et al. Feasibility of convalescent plasma therapy in kidney transplant recipients with severe COVID-19: a single-center prospective cohort study. Exp Clin Transplant 2021; 19 (04) 304-309
63 Harrington P, Doores KJ, Radia D. et al. Single dose of BNT162b2 mRNA vaccine against severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) induces neutralising antibody and polyfunctional T-cell responses in patients with chronic myeloid leukaemia. Br J Haematol 2021; 194 (06) 999-1006
64 Ali NM, Alnazari N, Mehta SA. et al. Development of COVID-19 infection in transplant recipients after SARS-CoV-2 vaccination. Transplantation 2021; 105 (09) e104-e106
65 Shroff RT, Chalasani P, Wei R, Pennington D, Quirk G, Schoenle MV. et al. Immune responses to two and three doses of the BNT162b2 mRNA vaccine in adults with solid tumors. Nat Med 2021; Nov; 27 (11) 2002-2011
66 Boyarsky BJ, Werbel WA, Avery RK. et al. Immunogenicity of a single dose of SARS-CoV-2 messenger RNA vaccine in solid organ transplant recipients. JAMA 2021; 325 (17) 1784-1786
67 Gavriatopoulou M, Terpos E, Ntanasis-Stathopoulos I. et al. Poor neutralizing antibody responses in 106 patients with WM after vaccination against SARS-CoV-2; a prospective study. Blood Adv 2021:bloodadvances.2021005444
68 Thuluvath PJ, Robarts P, Chauhan M. Analysis of antibody responses after COVID-19 vaccination in liver transplant recipients and those with chronic liver diseases. J Hepatol 2021; S0168-8278 (21)02002-X
69 Strengert M, Becker M, Ramos GM. et al. Cellular and humoral immunogenicity of a SARS-CoV-2 mRNA vaccine in patients on haemodialysis. EBioMedicine 2021; 70: 103524
70 Easdale S, Shea R, Ellis L. et al. Serologic responses following a single dose of SARS-CoV-2 vaccination in allogeneic stem cell transplantation recipients. Transplant Cell Ther 2021; 27 (10) 880.e1-880.e4
71 Schramm R, Costard-Jäckle A, Rivinius R. et al. Poor humoral and T-cell response to two-dose SARS-CoV-2 messenger RNA vaccine BNT162b2 in cardiothoracic transplant recipients. Clin Res Cardiol 2021; 110 (08) 1142-1149
72 Narasimhan M, Mahimainathan L, Clark AE. et al. Serological response in lung transplant recipients after two doses of SARS-CoV-2 mRNA vaccines. Vaccines (Basel) 2021; 9 (07) 708
73 Danthu C, Hantz S, Dahlem A. et al. Humoral response after SARS-CoV-2 mRNA vaccination in a cohort of hemodialysis patients and kidney transplant recipients. J Am Soc Nephrol 2021; 32 (09) 2153-2158
74 Rincon-Arevalo H, Choi M, Stefanski A-L. et al. Impaired humoral immunity to SARS-CoV-2 BNT162b2 vaccine in kidney transplant recipients and dialysis patients. Sci Immunol 2021; 6 (60) eabj1031
75 Havlin J, Svorcova M, Dvorackova E. et al. Immunogenicity of BNT162b2 mRNA COVID-19 vaccine and SARS-CoV-2 infection in lung transplant recipients. J Heart Lung Transplant 2021; 40 (08) 754-758
76 Bertrand D, Hamzaoui M, Lemée V. et al. Antibody and T cell response to SARS-CoV-2 messenger RNA BNT162b2 vaccine in kidney transplant recipients and HEMODIALYSIS PATIENTS. J Am Soc Nephrol 2021; 32 (09) 2147-2152