Trajectory analyses to identify persistently low responders to COVID-19 vaccination in patients with inflammatory bowel disease: a prospective multicentre controlled study, J-COMBAT.
COVID-19
Inflammatory bowel disease
Responder
Trajectory analyses
Vaccine
Journal
Journal of gastroenterology
ISSN: 1435-5922
Titre abrégé: J Gastroenterol
Pays: Japan
ID NLM: 9430794
Informations de publication
Date de publication:
10 2023
10 2023
Historique:
received:
18
05
2023
accepted:
18
07
2023
medline:
27
9
2023
pubmed:
10
8
2023
entrez:
10
8
2023
Statut:
ppublish
Résumé
The degree of immune response to COVID-19 vaccination in inflammatory bowel disease (IBD) patients based on actual changes in anti-SARS-CoV-2 antibody titres over time is unknown. Data were prospectively acquired at four predetermined time points before and after two vaccine doses in a multicentre observational controlled study. The primary outcome was humoral immune response and vaccination safety in IBD patients. We performed trajectory analysis to identify the degree of immune response and associated factors in IBD patients compared with controls. Overall, 645 IBD patients and 199 control participants were analysed. At 3 months after the second vaccination, the seronegative proportions were 20.3% (combination of anti-tumour necrosis factor [TNF]α and thiopurine) and 70.0% (triple combination including steroids), despite that 80.0% receiving the triple combination therapy were seropositive at 4 weeks after the second vaccination. Trajectory analyses indicated three degrees of change in immune response over time in IBD patients: high (57.7%), medium (35.6%), and persistently low (6.7%). In the control group, there was only one degree, which corresponded with IBD high responders. Older age, combined anti-TNFα and thiopurine (odds ratio [OR], 37.68; 95% confidence interval [CI], 5.64-251.54), steroids (OR, 21.47; 95%CI, 5.47-84.26), and tofacitinib (OR, 10.66; 95%CI, 1.49-76.31) were factors associated with persistently low response. Allergy history (OR, 0.17; 95%CI, 0.04-0.68) was a negatively associated factor. Adverse reactions after the second vaccination were significantly fewer in IBD than controls (31.0% vs 59.8%; p < 0.001). Most IBD patients showed a sufficient immune response to COVID-19 vaccination regardless of clinical factors. Assessment of changes over time is essential to optimize COVID-19 vaccination, especially in persistently low responders.
Sections du résumé
BACKGROUND
The degree of immune response to COVID-19 vaccination in inflammatory bowel disease (IBD) patients based on actual changes in anti-SARS-CoV-2 antibody titres over time is unknown.
METHODS
Data were prospectively acquired at four predetermined time points before and after two vaccine doses in a multicentre observational controlled study. The primary outcome was humoral immune response and vaccination safety in IBD patients. We performed trajectory analysis to identify the degree of immune response and associated factors in IBD patients compared with controls.
RESULTS
Overall, 645 IBD patients and 199 control participants were analysed. At 3 months after the second vaccination, the seronegative proportions were 20.3% (combination of anti-tumour necrosis factor [TNF]α and thiopurine) and 70.0% (triple combination including steroids), despite that 80.0% receiving the triple combination therapy were seropositive at 4 weeks after the second vaccination. Trajectory analyses indicated three degrees of change in immune response over time in IBD patients: high (57.7%), medium (35.6%), and persistently low (6.7%). In the control group, there was only one degree, which corresponded with IBD high responders. Older age, combined anti-TNFα and thiopurine (odds ratio [OR], 37.68; 95% confidence interval [CI], 5.64-251.54), steroids (OR, 21.47; 95%CI, 5.47-84.26), and tofacitinib (OR, 10.66; 95%CI, 1.49-76.31) were factors associated with persistently low response. Allergy history (OR, 0.17; 95%CI, 0.04-0.68) was a negatively associated factor. Adverse reactions after the second vaccination were significantly fewer in IBD than controls (31.0% vs 59.8%; p < 0.001).
CONCLUSIONS
Most IBD patients showed a sufficient immune response to COVID-19 vaccination regardless of clinical factors. Assessment of changes over time is essential to optimize COVID-19 vaccination, especially in persistently low responders.
Identifiants
pubmed: 37561155
doi: 10.1007/s00535-023-02029-z
pii: 10.1007/s00535-023-02029-z
doi:
Substances chimiques
COVID-19 Vaccines
0
Types de publication
Journal Article
Multicenter Study
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1015-1029Subventions
Organisme : NCEZID CDC HHS
ID : 20HA2001
Pays : United States
Organisme : NCEZID CDC HHS
ID : 20HA2001
Pays : United States
Informations de copyright
© 2023. Japanese Society of Gastroenterology.
Références
Danese S, Cecconi M, Spinelli A. Management of IBD during the COVID-19 outbreak: resetting clinical priorities. Nat Rev Gastroenterol Hepatol. 2020;17:253–5.
doi: 10.1038/s41575-020-0294-8
pubmed: 32214232
pmcid: 7095422
Ng SC, Shi HY, Hamidi N, et al. Worldwide incidence and prevalence of inflammatory bowel disease in the 21st century: a systematic review of population-based studies. Lancet. 2017;390:2769–78.
doi: 10.1016/S0140-6736(17)32448-0
pubmed: 29050646
Murakami Y, Nishiwaki Y, Oba MS, et al. Estimated prevalence of ulcerative colitis and Crohn’s disease in Japan in 2014: an analysis of a nationwide survey. J Gastroenterol. 2019;54:1070–7.
doi: 10.1007/s00535-019-01603-8
pubmed: 31309327
Ungaro RC, Brenner EJ, Agrawal M, et al. Impact of medications on COVID-19 outcomes in inflammatory bowel disease: analysis of more than 6000 patients from an international registry. Gastroenterology. 2022;162:316–9.
doi: 10.1053/j.gastro.2021.09.011
pubmed: 34529987
Nakase H, Matsumoto T, Matsuura M, et al. Expert opinions on the current therapeutic management of inflammatory bowel disease during the COVID-19 pandemic: Japan IBD COVID-19 taskforce, intractable diseases, the health and labor sciences research. Digestion. 2021;102:814–22.
doi: 10.1159/000510502
pubmed: 32892197
Hayashi Y, Nakase H, Hisamatsu T, et al. Should we continue or discontinue inflammatory bowel disease medication in patients with coronavirus disease 2019? Gastroenterology. 2022;163:338–9.
doi: 10.1053/j.gastro.2022.03.008
pubmed: 35288110
Nakase H, Hayashi Y, Hirayama D, et al. Interim analysis of a multicenter registry study of COVID-19 patients with inflammatory bowel disease in Japan (J-COSMOS). J Gastroenterol. 2022;57:174–84.
doi: 10.1007/s00535-022-01851-1
pubmed: 35089397
pmcid: 8795939
Lin S, Kennedy NA, Saifuddin A, et al. Antibody decay, T cell immunity and breakthrough infections following two SARS-CoV-2 vaccine doses in inflammatory bowel disease patients treated with infliximab and vedolizumab. Nat Commun. 2022;13:1379. https://doi.org/10.1038/s41467-022-28517-z .
doi: 10.1038/s41467-022-28517-z
pubmed: 35296643
pmcid: 8927425
Kennedy NA, Lin S, Goodhand JR, et al. Infliximab is associated with attenuated immunogenicity to BNT162b2 and ChAdOx1 nCoV-19 SARS-CoV-2 vaccines in patients with IBD. Gut. 2021;70:1884–93.
doi: 10.1136/gutjnl-2021-324789
pubmed: 33903149
Alexander JL, Kennedy NA, Ibraheim H, et al. COVID-19 vaccine-induced antibody responses in immunosuppressed patients with inflammatory bowel disease (VIP): a multicentre, prospective, case-control study. Lancet Gastroenterol Hepatol. 2022;7:342–52.
doi: 10.1016/S2468-1253(22)00005-X
pubmed: 35123676
pmcid: 8813209
Food and Drug Administration. Guidance for Industry. Toxicity grading scale for healthy adult and adolescent volunteers enrolled in preventive vaccine clinical trials. URL: https://www.fda.gov/media/73679/download . Accessed: 3rd Dec 2022
Irsara C, Egger AE, Prokop W, et al. Clinical validation of the Siemens quantitative SARS-CoV-2 spike IgG assay (sCOVG) reveals improved sensitivity and a good correlation with virus neutralization titers. Clin Chem Lab Med. 2021;59:1453–62.
doi: 10.1515/cclm-2021-0214
pubmed: 33837679
Public Health England. Evaluation of sensitivity and specificity of four commercially available SARS-CoV-2 antibody immunoassays. URL: https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/898437/Evaluation__of_sensitivity_and_specificity_of_4_commercially_available_SARS-CoV-2_antibody_immunoassays.pdf Accessed: 3rd Dec 2022
Walsh EE, Frenck RW Jr, Falsey AR, et al. Safety and immunogenicity of two RNA-Based Covid-19 vaccine candidates. N Engl J Med. 2020;383:2439–50.
doi: 10.1056/NEJMoa2027906
pubmed: 33053279
Sakuraba A, Luna A, Micic D. Serologic response to coronavirus disease 2019 (COVID-19) vaccination in patients with immune-mediated inflammatory diseases: a systematic review and meta-analysis. Gastroenterology. 2022;162:88–108.
doi: 10.1053/j.gastro.2021.09.055
pubmed: 34599933
Wellens J, Colombel JF, Satsangi JJ, Wong SY. SARS-CoV-2 vaccination in IBD: past lessons, current evidence, and future challenges. J Crohns Colitis. 2021;15:1376–86.
doi: 10.1093/ecco-jcc/jjab046
pubmed: 33721882
Wong SY, Dixon R, Martinez Pazos V, et al. Serologic response to messenger RNA Coronavirus disease 2019 vaccines in inflammatory bowel disease patients receiving biologic therapies. Gastroenterology. 2021;161:715–8.
doi: 10.1053/j.gastro.2021.04.025
pubmed: 33887219
Lev-Tzion R, Focht G, Lujan R, et al. COVID-19 vaccine is effective in inflammatory bowel disease patients and is not associated with disease exacerbation. Clin Gastroenterol Hepatol. 2022;20:e1263–82.
doi: 10.1016/j.cgh.2021.12.026
pubmed: 34954338
Chiba S, Shinohara K. A predictive model to estimate fever after receipt of the second dose of Pfizer-BioNTech coronavirus disease 2019 vaccine: an observational cohort study. Health Sci Rep. 2022;5:e742. https://doi.org/10.1002/hsr2.742 .
doi: 10.1002/hsr2.742
pubmed: 35873402
pmcid: 9297380
Uwamino Y, Kurafuji T, Sato Y, et al. Young age, female sex, and presence of systemic adverse reactions are associated with high post-vaccination antibody titer after two doses of BNT162b2 mRNA SARS-CoV-2 vaccination: an observational study of 646 Japanese healthcare workers and university staff. Vaccine. 2022;40:1019–25.
doi: 10.1016/j.vaccine.2022.01.002
pubmed: 35033389
pmcid: 8739021
Liu JZ, van Sommeren S, Huang H, et al. Association analyses identify 38 susceptibility loci for inflammatory bowel disease and highlight shared genetic risk across populations. Nat Genet. 2015;47:979–86.
doi: 10.1038/ng.3359
pubmed: 26192919
pmcid: 4881818
Weaver KN, Zhang X, Dai X, et al. Impact of SARS-CoV-2 vaccination on inflammatory bowel disease activity and development of vaccine-related adverse events: results from PREVENT-COVID. Inflamm Bowel Dis. 2022;28:1497–505.
doi: 10.1093/ibd/izab302
pubmed: 34871388
Stankiewicz Karita HC, Dong TQ, Johnston C, et al. Trajectory of viral RNA load among persons with incident SARS-CoV-2 G614 infection (Wuhan strain) in association with COVID-19 symptom onset and severity. JAMA Netw Open. 2022;5:e2142796. https://doi.org/10.1001/jamanetworkopen.2021.42796 .
doi: 10.1001/jamanetworkopen.2021.42796
pubmed: 35006245
pmcid: 8749477
Sonabend R, Whittles LK, Imai N, et al. Non-pharmaceutical interventions, vaccination, and the SARS-CoV-2 delta variant in England: a mathematical modelling study. Lancet. 2021;398:1825–35.
doi: 10.1016/S0140-6736(21)02276-5
pubmed: 34717829
pmcid: 8550916