Clin Microbiol Infect. 2021 Oct 28; doi: 10.1016/j.cmi.2021.09.036. Epub 2021 Oct 28.
Immunological and clinical efficacy of COVID-19 vaccines in immunocompromised populations: a systematic review.
Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases
Simon Galmiche, Liem Binh Luong Nguyen, Eric Tartour, Xavier de Lamballerie, Linda Wittkop, Paul Loubet, Odile Launay
Affiliations
Affiliations
- Assistance Publique - Hôpitaux de Paris (AP-HP), CIC Cochin Pasteur, Hôpital Cochin, Paris, France.
- AP-HP, Immunologie Biologique, Hôpital Européen Georges Pompidou, Paris, France.
- Aix Marseille Université, IRD 190, INSERM 1207, Unité des Virus Emergents, UVE, IHU Méditerranée Infection, Marseille, France.
- Institut de Santé Publique d'Epidémiologie et de Développement, INSERM, Bordeaux Population Health Research Center, UMR 1219, Centre d'Investigation Clinique-Epidémiologie Clinique 1401, University of Bordeaux, Service d'Information Médicale, CHU de Bordeaux, Pôle de Santé Publique, Bordeaux, France.
- INSERM U1047, Department of Infectious and Tropical Diseases, CHU Nîmes, Université Montpellier, Nîmes, France.
- Université de Paris, Faculté de Médecine Paris Descartes, AP-PH, Inserm, CIC Cochin Pasteur, Paris, France. Electronic address: [email protected].
PMID: 35020589
PMCID: PMC8595936 DOI: 10.1016/j.cmi.2021.09.036
Abstract
BACKGROUND: Available data show that COVID-19 vaccines may be less effective in immunocompromised populations, who are at increased risk of severe COVID-19.
OBJECTIVES: We conducted a systematic review of literature to assess immunogenicity, efficacy and effectiveness of COVID-19 vaccines in immunocompromised populations.
DATA SOURCES: We searched Medline and Embase databases.
STUDY ELIGIBILITY CRITERIA, PATIENTS, INTERVENTIONS: We included studies of COVID-19 vaccines after complete vaccination in immunocompromised patients until 31 August 2021. Studies with <10 patients, safety data only and case series of breakthrough infections were excluded.
METHODS: Risk of bias was assessed via the tool developed by the National Institutes of Health on interventional and observational studies. Immunogenicity was assessed through non-response rate defined as no anti-SARS-CoV-2 spike protein antibodies, efficacy and effectiveness by the relative reduction in risk of SARS-CoV-2 infection or COVID-19. We collected factors associated with the risk of non-response. We presented collected data by immunosuppression type.
RESULTS: We screened 5917 results, included 162 studies. There were 157 on immunogenicity in 25 209 participants, including 7835 cancer or haematological malignancy patients (31.1%), 6302 patients on dialysis (25.0%), 5974 solid organ transplant recipients (23.7%) and 4680 immune-mediated disease patients (18.6%). Proportion of non-responders seemed higher among solid organ transplant recipients (range 18-100%) and patients with haematological malignancy (range 14-61%), and lower in patients with cancer (range 2-36%) and patients on dialysis (range 2-30%). Risk factors for non-response included older age, use of corticosteroids, immunosuppressive or anti-CD20 agent. Ten studies evaluated immunogenicity of an additional dose. Five studies evaluated vaccine efficacy or effectiveness: three on SARS-CoV-2 infection (range 71-81%), one on COVID-19-related hospitalization (62.9%), one had a too small sample size.
CONCLUSIONS: This systematic review highlights the risk of low immunogenicity of COVID-19 vaccines in immunocompromised populations, especially solid organ transplant recipients and patients with haematological malignancy. Despite lack of vaccine effectiveness data, enhanced vaccine regimens may be necessary.
Copyright © 2021 European Society of Clinical Microbiology and Infectious Diseases. Published by Elsevier Ltd. All rights reserved.
Keywords: COVID-19; Cancer; Dialysis; Effectiveness; Efficacy; Immunogenicity; SARS-CoV-2 immunocompromised; Solid organ transplant; Vaccine
References
- Kidney Int. 2021 Aug;100(2):476-477 - PubMed
- Ther Adv Neurol Disord. 2021 Aug 13;14:17562864211038111 - PubMed
- Med Clin (Barc). 2021 May 27;: - PubMed
- Blood Adv. 2021 Aug 24;5(16):3053-3061 - PubMed
- J Clin Invest. 2021 Jul 15;131(14): - PubMed
- Kidney Int Rep. 2021 Sep;6(9):2521-2522 - PubMed
- Am J Transplant. 2021 Mar;21(3):1295-1303 - PubMed
- Antivir Ther. 2012;17(5):893-903 - PubMed
- Am J Kidney Dis. 2021 Oct;78(4):571-581 - PubMed
- Ann Rheum Dis. 2020 Dec 2;: - PubMed
- Blood Cancer J. 2021 Aug 10;11(8):142 - PubMed
- Leukemia. 2020 Nov;34(11):3047-3049 - PubMed
- Ann Rheum Dis. 2021 Oct;80(10):1357-1359 - PubMed
- Vaccines (Basel). 2021 Jul 04;9(7): - PubMed
- J Heart Lung Transplant. 2021 Aug;40(8):759-762 - PubMed
- Pol Arch Intern Med. 2021 Sep 30;131(9):797-801 - PubMed
- Immunol Res. 2021 Aug;69(4):309-311 - PubMed
- Blood Cancer J. 2021 Jul 30;11(7):136 - PubMed
- Ann Rheum Dis. 2021 Oct;80(10):1312-1316 - PubMed
- Cancer Cell. 2021 Aug 9;39(8):1091-1098.e2 - PubMed
- Lancet. 2021 Jan 9;397(10269):99-111 - PubMed
- Eur J Cancer. 2021 Sep;154:4-6 - PubMed
- Transplantation. 2021 Nov 1;105(11):e226-e233 - PubMed
- N Engl J Med. 2021 Jun 10;384(23):2187-2201 - PubMed
- Future Oncol. 2021 Nov;17(33):4447-4456 - PubMed
- Sci Immunol. 2021 Jun 15;6(60): - PubMed
- Transplantation. 2021 Dec 1;105(12):e283-e284 - PubMed
- Transplantation. 2021 Aug 1;105(8):e80-e81 - PubMed
- Clin Infect Dis. 2021 Jul 22;: - PubMed
- Inflamm Bowel Dis. 2021 Sep 16;: - PubMed
- Vaccine. 2006 Feb 20;24(8):1159-69 - PubMed
- Leukemia. 2021 Dec;35(12):3534-3541 - PubMed
- Arthritis Care Res (Hoboken). 2014 Jul;66(7):1016-26 - PubMed
- Lancet. 2020 Aug 15;396(10249):467-478 - PubMed
- J Am Soc Nephrol. 2021 Oct;32(10):2435-2438 - PubMed
- Br J Haematol. 2021 Oct;195(2):186-193 - PubMed
- J Clin Immunol. 2013 Feb;33(2):388-96 - PubMed
- Transplantation. 2021 Nov 1;105(11):e259-e260 - PubMed
- Ther Adv Neurol Disord. 2021 Apr 22;14:17562864211012835 - PubMed
- Lancet Rheumatol. 2021 Nov;3(11):e778-e788 - PubMed
- Kidney Int. 2021 Sep;100(3):700-702 - PubMed
- Lancet Reg Health Eur. 2021 Oct;9:100178 - PubMed
- Kidney Int. 2021 Sep;100(3):698-700 - PubMed
- Clin J Am Soc Nephrol. 2011 Sep;6(9):2208-14 - PubMed
- Blood. 2021 Oct 7;138(14):1278-1281 - PubMed
- Am J Hematol. 2021 Nov 1;96(11):E410-E413 - PubMed
- Transplantation. 2021 Aug 1;105(8):e82-e83 - PubMed
- Lancet Respir Med. 2021 Jun;9(6):e52-e53 - PubMed
- Front Immunol. 2021 Jun 16;12:704773 - PubMed
- Ann Allergy Asthma Immunol. 2021 Oct;127(4):501-503 - PubMed
- Am J Kidney Dis. 2009 Jul;54(1):77-85 - PubMed
- Transplant Cell Ther. 2021 Sep;27(9):788-794 - PubMed
- Gastroenterology. 2021 Aug;161(2):715-718.e4 - PubMed
- N Engl J Med. 2021 Apr 15;384(15):1412-1423 - PubMed
- N Engl J Med. 2021 Aug 12;385(7):661-662 - PubMed
- Clin J Am Soc Nephrol. 2011 Nov;6(11):2573-8 - PubMed
- Ann Rheum Dis. 2021 Oct;80(10):1351-1352 - PubMed
- J Rheumatol. 2018 Jun;45(6):733-744 - PubMed
- Mult Scler Relat Disord. 2021 Sep;54:103150 - PubMed
- Ann Rheum Dis. 2021 Oct;80(10):1317-1321 - PubMed
- Am J Transplant. 2021 Dec;21(12):3990-4002 - PubMed
- Cancers (Basel). 2021 Aug 20;13(16): - PubMed
- N Engl J Med. 2021 Sep 23;385(13):1244-1246 - PubMed
- Transplantation. 2021 Nov 1;105(11):e267-e269 - PubMed
- JAMA. 2021 Jul 23;: - PubMed
- Inflamm Bowel Dis. 2021 Oct 20;27(11):1862-1864 - PubMed
- Leuk Lymphoma. 2021 Dec;62(13):3308-3310 - PubMed
- J Crohns Colitis. 2021 Aug 11;: - PubMed
- JAMA Oncol. 2021 Aug 1;7(8):1133-1140 - PubMed
- Nephrol Dial Transplant. 2021 Aug 27;36(9):1756-1757 - PubMed
- Kidney Int. 2021 Jun;99(6):1496-1498 - PubMed
- Am J Transplant. 2022 Jan;22(1):322-323 - PubMed
- Am J Transplant. 2021 Dec;21(12):3980-3989 - PubMed
- Influenza Other Respir Viruses. 2013 Sep;7(5):809-14 - PubMed
- Blood. 2021 Sep 2;138(9):811-814 - PubMed
- Gastroenterology. 2021 Sep;161(3):827-836 - PubMed
- Ann Rheum Dis. 2021 Oct;80(10):1322-1329 - PubMed
- Kidney Int. 2021 Oct;100(4):928-936 - PubMed
- Ann Rheum Dis. 2021 Oct;80(10):1365-1366 - PubMed
- Clin Infect Dis. 2021 Jun 24;: - PubMed
- Nephrol Dial Transplant. 2021 Apr 11;: - PubMed
- Clin Infect Dis. 2021 Aug 2;73(3):e661-e671 - PubMed
- Ann Oncol. 2021 Aug;32(8):1053-1055 - PubMed
- J Am Soc Nephrol. 2022 Jan;33(1):33-37 - PubMed
- Haematologica. 2021 Jul 29;: - PubMed
- J Hematol Oncol. 2021 May 17;14(1):81 - PubMed
- Transplant Rev (Orlando). 2021 Jan;35(1):100588 - PubMed
- JAMA. 2020 Jul 14;324(2):131-132 - PubMed
- Ann Rheum Dis. 2021 Oct;80(10):e164 - PubMed
- J Hepatol. 2022 Jan;76(1):237-239 - PubMed
- Nephrol Dial Transplant. 2021 Aug 27;36(9):1704-1709 - PubMed
- Clin Microbiol Infect. 2021 Dec;27(12):1851-1855 - PubMed
- EBioMedicine. 2021 Nov;73:103679 - PubMed
- Nat Med. 2021 Aug;27(8):1319-1321 - PubMed
- Kidney Int. 2020 Dec;98(6):1519-1529 - PubMed
- J Allergy Clin Immunol. 2021 Sep;148(3):739-749 - PubMed
- Vaccine. 2011 Nov 21;29(50):9316-20 - PubMed
- J Am Soc Nephrol. 2021 Sep;32(9):2147-2152 - PubMed
- J Intern Med. 2021 Dec;290(6):1264-1267 - PubMed
- Kidney Int Rep. 2021 Jun;6(6):1699-1700 - PubMed
- Ann Rheum Dis. 2021 Oct;80(10):1330-1338 - PubMed
- Nat Med. 2021 Sep;27(9):1530-1535 - PubMed
- Eur J Cancer. 2021 Sep;154:30-34 - PubMed
- Ann Rheum Dis. 2021 Oct;80(10):1339-1344 - PubMed
- Kidney Int. 2021 Sep;100(3):697-698 - PubMed
- Transplantation. 2021 Oct 1;105(10):e137-e138 - PubMed
- Ann Rheum Dis. 2021 Oct;80(10):1345-1350 - PubMed
- Kidney Int. 2021 Jun;99(6):1490-1492 - PubMed
- Am J Kidney Dis. 2021 Nov;78(5):766-768 - PubMed
- Am J Transplant. 2021 Aug;21(8):2727-2739 - PubMed
- Transplantation. 2021 Sep 1;105(9):e94-e95 - PubMed
- Nephrol Dial Transplant. 2021 Aug 27;36(9):1709-1716 - PubMed
- Vaccine. 2012 Nov 6;30(48):6864-70 - PubMed
- N Engl J Med. 2021 Feb 4;384(5):403-416 - PubMed
- Nephrol Dial Transplant. 2020 Nov 1;35(11):1973-1983 - PubMed
- Rheumatol Int. 2021 Aug;41(8):1429-1440 - PubMed
- Arthritis Rheumatol. 2021 Aug 4;: - PubMed
- Hum Vaccin Immunother. 2017 Mar 4;13(3):543-550 - PubMed
- Clin J Am Soc Nephrol. 2021 Jul;16(7):1037-1042 - PubMed
- Nat Med. 2021 Oct;27(10):1744-1751 - PubMed
- J Natl Cancer Inst. 2021 Aug 28;: - PubMed
- Eur J Heart Fail. 2021 Sep;23(9):1555-1559 - PubMed
- J Clin Oncol. 2019 Oct 20;37(30):2795-2804 - PubMed
- J Heart Lung Transplant. 2021 Dec;40(12):1579-1588 - PubMed
- Am J Transplant. 2021 Aug;21(8):2913-2915 - PubMed
- J Neurol. 2022 Jan;269(1):39-43 - PubMed
- Br J Haematol. 2021 Nov;195(4):523-531 - PubMed
- Am J Kidney Dis. 2021 Aug;78(2):314-317 - PubMed
- AIDS. 2021 Nov 15;35(14):2399-2401 - PubMed
- Hum Vaccin Immunother. 2019;15(12):2910-2913 - PubMed
- Lancet Oncol. 2021 Jun;22(6):765-778 - PubMed
- EBioMedicine. 2021 Aug;70:103524 - PubMed
- Clin Microbiol Infect. 2021 Dec;27(12):1861.e1-1861.e5 - PubMed
- Leukemia. 2021 Sep;35(9):2727-2730 - PubMed
- Ann Intern Med. 2021 Sep;174(9):1336-1338 - PubMed
- Liver Transpl. 2021 Dec;27(12):1852-1856 - PubMed
- Am J Transplant. 2021 Aug;21(8):2919-2921 - PubMed
- Cancer Cell. 2021 Aug 9;39(8):1034-1036 - PubMed
- Ann Oncol. 2021 Nov;32(11):1443-1444 - PubMed
- Clin J Am Soc Nephrol. 2021 Jul;16(7):1073-1082 - PubMed
- Clin J Am Soc Nephrol. 2021 Aug;16(8):1258-1260 - PubMed
- Lancet Rheumatol. 2021 Jul;3(7):e470-e472 - PubMed
- Transplantation. 2021 Nov 1;105(11):e234-e243 - PubMed
- Blood Adv. 2021 Aug 24;5(16):3062-3065 - PubMed
- J Hepatol. 2021 Dec;75(6):1434-1439 - PubMed
- Am J Hematol. 2021 Oct 1;96(10):1195-1203 - PubMed
- J Hematol Oncol. 2021 Jul 29;14(1):119 - PubMed
- Lancet Haematol. 2021 Aug;8(8):e542-e544 - PubMed
- Indian J Gastroenterol. 2015 Sep;34(5):372-9 - PubMed
- Am J Transplant. 2021 Dec;21(12):3971-3979 - PubMed
- Vaccines (Basel). 2021 Jun 30;9(7): - PubMed
- J Geriatr Oncol. 2021 Nov;12(8):1253-1255 - PubMed
- Clin Kidney J. 2021 Jul 06;14(10):2266-2267 - PubMed
- RMD Open. 2019 Sep 9;5(2):e001035 - PubMed
- MMWR Morb Mortal Wkly Rep. 2021 Sep 17;70(37):1284-1290 - PubMed
- Nephrol Dial Transplant. 2021 Aug 27;36(9):1754-1755 - PubMed
- Hemodial Int. 2021 Oct;25(4):565-566 - PubMed
- N Engl J Med. 2021 May 20;384(20):1899-1909 - PubMed
- N Engl J Med. 2021 Aug 12;385(7):585-594 - PubMed
- Lancet HIV. 2021 Aug;8(8):e474-e485 - PubMed
- Vaccine. 2020 May 19;38(24):3995-4000 - PubMed
- Gastroenterology. 2021 Nov;161(5):1715-1717.e1 - PubMed
- Lancet. 2021 Jul 24;398(10297):298-299 - PubMed
- Transplantation. 2021 Sep 1;105(9):2119-2123 - PubMed
- Cancer Cell. 2021 Aug 9;39(8):1031-1033 - PubMed
- ACR Open Rheumatol. 2021 Sep;3(9):622-628 - PubMed
- Clin Infect Dis. 2021 May 17;: - PubMed
- Blood. 2011 Dec 22;118(26):6769-71 - PubMed
- Vaccines (Basel). 2021 Apr 08;9(4): - PubMed
- Lancet Haematol. 2021 Aug;8(8):e583-e592 - PubMed
- Viruses. 2021 Apr 25;13(5): - PubMed
- Am J Transplant. 2021 Aug;21(8):2719-2726 - PubMed
- Lancet. 2021 Mar 6;397(10277):881-891 - PubMed
- Clin Res Cardiol. 2021 Aug;110(8):1142-1149 - PubMed
- Gastroenterology. 2021 Oct;161(4):1340-1343.e2 - PubMed
- Ann Rheum Dis. 2021 Oct;80(10):1306-1311 - PubMed
- Transplantation. 2021 Dec 1;105(12):e280-e281 - PubMed
- Hum Vaccin Immunother. 2014;10(1):104-13 - PubMed
- Hum Vaccin Immunother. 2014;10(8):2387-94 - PubMed
- Int J Cancer. 2021 Jan 15;148(2):363-374 - PubMed
- Neurology. 2020 Oct 6;95(14):e1999-e2008 - PubMed
- Blood. 2021 Jun 10;137(23):3165-3173 - PubMed
- Ann Intern Med. 2021 Sep;174(9):1330-1332 - PubMed
- Transpl Infect Dis. 2021 Oct;23(5):e13705 - PubMed
- Am J Transplant. 2021 Nov;21(11):3806-3807 - PubMed
- Clin Chem. 2021 Dec 30;68(1):251-253 - PubMed
- J Am Soc Nephrol. 2021 Sep;32(9):2153-2158 - PubMed
- Am J Transplant. 2021 Aug;21(8):2916-2918 - PubMed
- Kidney Int. 2021 Sep;100(3):702-704 - PubMed
- J Heart Lung Transplant. 2021 Aug;40(8):754-758 - PubMed
- Kidney Int. 2021 Jun;99(6):1498-1500 - PubMed
- Haematologica. 2021 Jul 29;: - PubMed
- Rev Neurol (Paris). 2021 Dec;177(10):1237-1240 - PubMed
- Gut. 2021 Oct;70(10):1884-1893 - PubMed
- Ann Rheum Dis. 2021 Oct;80(10):e161 - PubMed
- Lancet. 2021 May 15;397(10287):1819-1829 - PubMed
- J Hepatol. 2021 Aug;75(2):435-438 - PubMed
- Cancer Cell. 2021 Aug 9;39(8):1028-1030 - PubMed
- N Engl J Med. 2020 Dec 31;383(27):2603-2615 - PubMed
- Lancet Respir Med. 2021 Sep;9(9):999-1009 - PubMed
- Lancet HIV. 2021 Sep;8(9):e568-e580 - PubMed
- Front Immunol. 2021 Jun 30;12:690698 - PubMed
- Eur J Nucl Med Mol Imaging. 2021 Oct;48(11):3540-3549 - PubMed
- N Engl J Med. 2021 May 13;384(19):1824-1835 - PubMed
- Nat Med. 2021 Sep;27(9):1525-1529 - PubMed
- N Engl J Med. 2020 Dec 17;383(25):2439-2450 - PubMed
- Vaccine. 2020 May 13;38(23):3934-3941 - PubMed
- Hum Vaccin Immunother. 2021 Feb 1;17(2):475-484 - PubMed
- JAMA. 2021 Jun 1;325(21):2204-2206 - PubMed
- Cancer Cell. 2021 Aug 9;39(8):1081-1090.e2 - PubMed
- Blood Cancer J. 2021 Aug 2;11(8):138 - PubMed
- Vaccine. 2013 Aug 2;31(35):3577-84 - PubMed
Publication Types