Vaccine Acceptance in Patients with Inflammatory Bowel Disease: Lessons Learned from the COVID-19 Pandemic
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Design and Patients
2.2. Exclusion Criteria
2.3. Questionnaire Items
2.4. Statistical Analysis
3. Results
3.1. Patients’ Sociodemographic and Clinical Characteristics
3.2. Assessment of COVID-19 Vaccine Uptake
3.3. Attitudes and Beliefs towards Vaccinations in General
3.4. COVID-19 Vaccine Acceptance: Propensity and Barriers
3.5. Sources for Information and Clinicians’ Advice
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Torres, J.; Bonovas, S.; Doherty, G.; Kucharzik, T.; Gisbert, J.P.; Raine, T.; Adamina, M.; Armuzzi, A.; Bachmann, O.; Bager, P.; et al. ECCO Guidelines on Therapeutics in Crohn’s Disease: Medical Treatment. J. Crohn’s Colitis 2020, 14, 4–22. [Google Scholar] [CrossRef] [PubMed]
- Harbord, M.; Eliakim, R.; Bettenworth, D.; Karmiris, K.; Katsanos, K.; Kopylov, U.; Kucharzik, T.; Molnár, T.; Raine, T.; Sebastian, S.; et al. Third European Evidence-based Consensus on Diagnosis and Management of Ulcerative Colitis. Part 2: Current Management. J. Crohn’s Colitis 2017, 11, 769–784. [Google Scholar] [CrossRef] [PubMed]
- Toruner, M.; Loftus, E.V.; Harmsen, W.S.; Zinsmeister, A.R.; Orenstein, R.; Sandborn, W.J.; Colombel, J.F.; Egan, L.J. Risk Factors for Opportunistic Infections in Patients With Inflammatory Bowel Disease. Gastroenterology 2008, 134, 929–936. [Google Scholar] [CrossRef] [PubMed]
- Ananthakrishnan, A.N.; McGinley, E.L. Infection-related hospitalizations are associated with increased mortality in patients with inflammatory bowel diseases. J. Crohn’s Colitis 2013, 7, 107–112. [Google Scholar] [CrossRef] [PubMed]
- Tinsley, A.; Navabi, S.; Williams, E.D.; Liu, G.; Kong, L.; Coates, M.D.; Clarke, K. Increased Risk of Influenza and Influenza-Related Complications Among 140,480 Patients With Inflammatory Bowel Disease. Inflamm. Bowel Dis. 2019, 25, 369–376. [Google Scholar] [CrossRef] [PubMed]
- Kucharzik, T.; Ellul, P.; Greuter, T.; Rahier, J.F.; Verstockt, B.; Abreu, C.; Albuquerque, A.; Allocca, M.; Esteve, M.; Farraye, F.A.; et al. ECCO Guidelines on the Prevention, Diagnosis, and Management of Infections in Inflammatory Bowel Disease. J. Crohn’s Colitis 2021, 15, 879–913. [Google Scholar] [CrossRef] [PubMed]
- Farraye, F.A.; Melmed, G.Y.; Lichtenstein, G.R.; Kane, S.V. ACG Clinical Guideline: Preventive Care in Inflammatory Bowel Disease. Am. J. Gastroenterol. 2017, 112, 241–258. [Google Scholar] [CrossRef]
- Lamb, C.A.; Kennedy, N.A.; Raine, T.; Hendy, P.A.; Smith, P.J.; Limdi, J.K.; Hayee, B.H.; Lomer, M.C.E.; Parkes, G.C.; Selinger, C.; et al. British Society of Gastroenterology consensus guidelines on the management of inflammatory bowel disease in adults. Gut 2019, 68 (Suppl. 3), s1–s106. [Google Scholar] [CrossRef]
- Al-Omar, H.A.; Sherif, H.M.; Mayet, A.Y. Vaccination status of patients using anti-TNF therapy and the physicians’ behavior shaping the phenomenon: Mixed-methods approach. PLoS ONE 2019, 14, e0223594. [Google Scholar] [CrossRef]
- Chan, W.; Salazar, E.; Lim, T.G.; Ong, W.C.; Shim, H.H. Vaccinations and inflammatory bowel disease—A systematic review. Dig. Liver Dis. 2021, 53, 1079–1088. [Google Scholar] [CrossRef]
- Hadi, Y.; Dulai, P.S.; Kupec, J.; Mohy-Ud-Din, N.; Jairath, V.; Farraye, F.A.; Kochhar, G.S. Incidence, outcomes, and impact of COVID-19 on inflammatory bowel disease: Propensity matched research network analysis. Aliment. Pharmacol. Ther. 2022, 55, 191–200. [Google Scholar] [CrossRef]
- Vernia, F.; Ashktorab, H.; Cesaro, N.; Monaco, S.; Faenza, S.; Sgamma, E.; Viscido, A.; Latella, G. COVID-19 and Gastrointestinal Tract: From Pathophysiology to Clinical Manifestations. Medicina 2023, 59, 1709. [Google Scholar] [CrossRef]
- Ungaro, R.C.; Brenner, E.J.; Agrawal, M.; Zhang, X.; Kappelman, M.D.; Colombel, J.F. Impact of Medications on COVID-19 Outcomes in Inflammatory Bowel Disease: Analysis of More Than 6000 Patients From an International Registry. Gastroenterology 2022, 162, 316–319. [Google Scholar] [CrossRef]
- Tse, F.; Moayyedi, P.; Waschke, K.A.; MacMillan, M.; Forbes, N.; Carroll, M.W.; Carman, N.; Leontiadis, G.I. COVID-19 Vaccination in Patients With Inflammatory Bowel Disease: Communiqué From the Canadian Association of Gastroenterology. J. Can. Assoc. Gastroenterol. 2021, 4, 49. [Google Scholar] [CrossRef] [PubMed]
- Alexander, J.L.; Moran, G.W.; Gaya, D.R.; Raine, T.; Hart, A.; Kennedy, N.A.; Lindsay, J.O.; MacDonald, J.; Segal, J.P.; Sebastian, S.; et al. SARS-CoV-2 vaccination for patients with inflammatory bowel disease: A British Society of Gastroenterology Inflammatory Bowel Disease section and IBD Clinical Research Group position statement. Lancet Gastroenterol. Hepatol. 2021, 6, 218–224. [Google Scholar] [CrossRef]
- Hadi, Y.B.; Thakkar, S.; Shah-Khan, S.M.; Hutson, W.; Sarwari, A.; Singh, S. COVID-19 Vaccination Is Safe and Effective in Patients With Inflammatory Bowel Disease: Analysis of a Large Multi-institutional Research Network in the United States. Gastroenterology 2021, 161, 1336–1339. [Google Scholar] [CrossRef]
- Dalal, R.S.; McClure, E.; Marcus, J.; Winter, R.W.; Hamilton, M.J.; Allegretti, J.R. COVID-19 Vaccination Intent and Perceptions Among Patients With Inflammatory Bowel Diseases. Clin. Gastroenterol. Hepatol. 2021, 19, 1730–1732. [Google Scholar] [CrossRef] [PubMed]
- Larson, H.J.; Jarrett, C.; Schulz, W.S.; Chaudhuri, M.; Zhou, Y.; Dube, E.; Schuster, M.; MacDonald, N.E.; Wilson, R. Measuring vaccine hesitancy: The development of a survey tool. Vaccine 2015, 33, 4165–4175. [Google Scholar] [CrossRef] [PubMed]
- World Health Organization Regional Office for Europe. COVID-19 Snapshot MOnitoring (COSMO) [Internet]. 2020. Available online: https://www.psycharchives.org/handle/20.500.12034/2397 (accessed on 24 August 2023).
- Szilagyi, P.G.; Thomas, K.; Shah, M.D.; Vizueta, N.; Cui, Y.; Vangala, S.; Kapteyn, A. National Trends in the US Public’s Likelihood of Getting a COVID-19 Vaccine—1 April to 8 December 2020. JAMA 2020, 325, 396–398. [Google Scholar] [CrossRef]
- Kennedy, N.A.; Jones, G.R.; Lamb, C.A.; Appleby, R.; Arnott, I.; Beattie, R.M.; Bloom, S.; Brooks, A.J.; Cooney, R.; Dart, R.J.; et al. British Society of Gastroenterology guidance for management of inflammatory bowel disease during the COVID-19 pandemic. Gut 2020, 69, 984–990. [Google Scholar] [CrossRef]
- Dudley, M.Z.; Privor-Dumm, L.; Dubé, È.; MacDonald, N.E. Words matter: Vaccine hesitancy, vaccine demand, vaccine confidence, herd immunity and mandatory vaccination. Vaccine 2020, 38, 709–711. [Google Scholar] [CrossRef] [PubMed]
- Melmed, G.Y.; Ippoliti, A.F.; Papadakis, K.A.; Tran, T.T.; Birt, J.L.; Lee, S.K.; Frenck, R.W.; Targan, S.R.; Vasiliauskas, E.A. Patients with Inflammatory Bowel Disease Are at Risk for Vaccine-Preventable Illnesses. Am. J. Gastroenterol. 2006, 101, 1834–1840. [Google Scholar] [CrossRef] [PubMed]
- Sallam, M. COVID-19 Vaccine Hesitancy Worldwide: A Concise Systematic Review of Vaccine Acceptance Rates. Vaccines 2021, 9, 160. [Google Scholar] [CrossRef] [PubMed]
- EpiCentro. (n.d.) Coronavirus. Sorveglianza Integrata COVID-19: I Principali Dati Nazionali. [Internet]. Available online: https://www.epicentro.iss.it/coronavirus/sars-cov-2-sorveglianza-dati (accessed on 8 January 2024).
- Bianchi, F.P.; Donghia, R.; Tatoli, R.; Bonfiglio, C. COVID-19 Immunization Rates in Patients with Inflammatory Bowel Disease Worldwide: A Systematic Review and Meta-Analysis. Vaccines 2023, 11, 1523. [Google Scholar] [CrossRef] [PubMed]
- Hu, S.; Liu, J.; Li, S.; Wu, Q.; Wang, X.; Xu, D.; Chen, Y. Patients with IBD have a more cautious attitude towards COVID-19 vaccination. Front. Immunol. 2023, 13, 1077308. [Google Scholar] [CrossRef] [PubMed]
- Costantino, A.; Noviello, D.; Conforti, F.S.; Aloi, M.; Armuzzi, A.; Bossa, F.; Ficari, F.; Leone, S.; Manguso, F.; Mocci, G.; et al. COVID-19 Vaccination Willingness and Hesitancy in Patients With Inflammatory Bowel Diseases: Analysis of Determinants in a National Survey of the Italian IBD Patients’ Association. Inflamm. Bowel Dis. 2022, 28, 474–478. [Google Scholar] [CrossRef] [PubMed]
- Reiter, P.L.; Pennell, M.L.; Katz, M.L. Acceptability of a COVID-19 vaccine among adults in the United States: How many people would get vaccinated? Vaccine 2020, 38, 6500–6507. [Google Scholar] [CrossRef] [PubMed]
- Boucher, V.G.; Pelaez, S.; Gemme, C.; Labbe, S.; Lavoie, K.L. Understanding factors associated with vaccine uptake and vaccine hesitancy in patients with rheumatoid arthritis: A scoping literature review. Clin. Rheumatol. 2021, 40, 477–489. [Google Scholar] [CrossRef]
- Doornekamp, L.; Goetgebuer, R.L.; Schmitz, K.S.; Goeijenbier, M.; van der Woude, C.J.; Fouchier, R.; van Gorp, E.C.M.; de Vries, A.C. High immunogenicity to influenza vaccination in crohn’s disease patients treated with ustekinumab. Vaccines 2020, 8, 455. [Google Scholar] [CrossRef]
- Patel, J.; Noureldin, M.; Fakhouri, D.; Farraye, F.A.; Kovar-Gough, I.; Warren, B.; Waljee, A.K.; Piper, M.S. Interventions Increase Vaccination Rates in Inflammatory Bowel Disease and Rheumatoid Arthritis: A Systematic Review and Meta-Analysis. Dig. Dis. Sci. 2023, 68, 2921–2935. [Google Scholar] [CrossRef]
- Swennen, B.; Van Damme, P.; Vellinga, A.; Coppieters, Y.; Depoorter, A.M. Analysis of factors influencing vaccine uptake: Perspectives from Belgium. Vaccine 2002, 20 (Suppl. 1), S5–S7. [Google Scholar] [CrossRef] [PubMed]
- Feng, S.; Lin, S.; Ma, L.; Xu, S.; Chen, Y. Insufficient knowledge and vaccination practice of inflammatory bowel disease patients in the People’s Republic of China. Patient Prefer. Adherence 2020, 14, 1513–1521. [Google Scholar] [CrossRef]
- Li, S.Y.; Li, P.W.; Shen, B.; Zhi, M.; Gu, Y.B.; Wang, X.Y.; Guo, H.; Li, Y.; Fan, Y.H.; Yang, B.L.; et al. Insufficient awareness and vaccination practices for inflammatory bowel disease patients in China: A multi-center survey of Chinese gastroenterologists. J. Dig. Dis. 2020, 21, 46–51. [Google Scholar] [CrossRef]
- Wasan, S.K.; Coukos, J.A.; Farraye, F.A. Vaccinating the inflammatory bowel disease patient: Deficiencies in gastroenterologists knowledge. Inflamm. Bowel Dis. 2011, 17, 2536–2540. [Google Scholar] [CrossRef]
- Gurvits, G.E.; Lan, G.; Tan, A.; Weissman, A. Vaccination practices in patients with inflammatory bowel disease among general internal medicine physicians in the USA. Postgrad. Med. J. 2017, 93, 333–337. [Google Scholar] [CrossRef] [PubMed]
- Ellul, P.; Revés, J.; Abreu, B.; Chaparro, M.; Gisbert, J.P.; Allocca, M.; Fiorino, G.; Barberio, B.; Zingone, F.; Pisani, A.; et al. Implementation and Short-term Adverse Events of Anti-SARS-CoV-2 Vaccines in Inflammatory Bowel Disease Patients: An International Web-based Survey. J. Crohn’s Colitis 2022, 16, 1070–1078. [Google Scholar] [CrossRef] [PubMed]
- Dror, A.A.; Eisenbach, N.; Taiber, S.; Morozov, N.G.; Mizrachi, M.; Zigron, A.; Srouji, S.; Sela, E. Vaccine hesitancy: The next challenge in the fight against COVID-19. Eur. J. Epidemiol. 2020, 35, 775–779. [Google Scholar] [CrossRef] [PubMed]
- Wu, X.; Lin, J.; Buch, H.; Ding, Q.; Zhang, F.; Cui, B.; Ji, G. The COVID-19 Vaccination Hesitancy Among the People With Inflammatory Bowel Disease in China: A Questionnaire Study. Front. Public Health 2021, 9, 731578. [Google Scholar] [CrossRef]
- Ferreiro-Iglesias, R.; Piqueras, M.; Ricart, E.; Sempere, L.; Roca, M.; Martín de Carpi, J.; Benítez, O.; Zabana, Y.; Mañosa, M.; Rodríguez-Moranta, F.; et al. Recommendations of the Spanish Group on Crohn’s Disease and Ulcerative Colitis on the importance, screening and vaccination in inflammatory bowel disease patients. Gastroenterol. Hepatol. 2022, 45, 805–818. [Google Scholar] [CrossRef]
IBD Patients n = 77 (43.3%) | Control Group n = 101 (56.7%) | p-Value | |
---|---|---|---|
Sex, n (%) | 0.327 | ||
Male | 37 (48.1) | 56 (55.4) | |
Female | 40 (51.9) | 45 (44.6) | |
Age (years), mean (±SD) | 49.5 (±15.4) | 51.6 (±18.3) | |
Age group (years), n (%) | 0.128 | ||
18–39 | 19 (24.7) | 29 (30.5) | |
40–59 | 36 (46.8) | 30 (31.6) | |
>60 | 22 (28.5) | 36 (37.9) | |
Highest level of educational attainment, n (%) | 0.973 | ||
Primary school | 3 (3.9) | 4 (4.0) | |
Lower secondary school | 15 (19.5) | 18 (18.0) | |
Upper secondary school | 41 (53.3) | 58 (58.0) | |
Higher education | 18 (23.3) | 20 (20.0) | |
Occupation, n (%) | 0.050 | ||
Student | 1 (1.3) | 6 (6.2) | |
Worker | 46 (59.7) | 46 (47.4) | |
Retired | 12 (15.6) | 9 (9.3) | |
Unemployed | 18 (23.4) | 36 (37.1) | |
Self-perceived health | 0.071 | ||
Poor | 11 (14.3) | 15 (14.9) | |
Fair | 41 (53.2) | 37 (36.6) | |
Good | 19 (24.7) | 43 (42.6) | |
Very good | 6 (7.8) | 6 (5.9) |
Diagnosis, n (%) | ||
---|---|---|
Crohn’s disease | 37 (48.1) | |
Ulcerative colitis | 40 (51.9) | |
Years of disease, mean (±SD) | 13.7 (±11.2) | |
Years of disease range, n (%) | ||
<1 | 3 (3.9) | |
1–5 | 26 (33.8) | |
6–10 | 8 (10.4) | |
11–15 | 12 (15.6) | |
16–20 | 6 (7.8) | |
>20 | 22 (28.5) | |
CD location, n (%) | ||
Ileal | 10 (27.0) | |
Colonic | 4 (10.8) | |
Ileocolonic | 23 (62.2) | |
Isolated upper disease | 0 (0.0) | |
UC extent, n (%) | ||
Proctitis | 1 (2.5) | |
Left-sided | 15 (37.5) | |
Extensive disease | 24 (60.0) | |
Activity, n (%) | CD | UC |
Quiescent | 20 (54.1) | 28 (70) |
Mild | 12 (32.4) | 8 (20.0) |
Moderate | 5 (13.5) | 3 (7.5) |
Severe | 0 (0.0) | 1 (2.5) |
BSG risk grid, n (%) | ||
Lowest risk | 19 (24.7) | |
Moderate risk | 49 (63.6) | |
Highest risk | 9 (11.7) | |
Treatment, n (%) | ||
Biologic therapy | 34 (44.2) | |
Conventional therapy | 43 (55.8) |
IBD Patients n = 77 (43.3%) | Control Group n = 101 (56.7%) | p-Value | |
---|---|---|---|
Tested positive for COVID-19, n (%) | 0.0464 | ||
yes, asymptomatic infection | 3 (3.9) | 2 (2.0) | |
yes, mild symptoms | 4 (5.2) | 22 (22.0) | |
yes, moderate symptoms | 1 (1.3) | 3 (3.0) | |
yes, severe symptoms/hospitalization | 1 (1.3) | 2 (2.0) | |
no | 68 (88.3) | 71 (71.0) | |
Personally knew anyone with COVID-19, n (%) | 0.0886 | ||
Yes | 48 (62.3) | 76 (77.6) | |
No | 29 (37.7) | 23 (22.4) | |
Received COVID-19 vaccine, n (%) | <0.0001 | ||
yes, 1 dose | 8 (10.4) | 92 (91.0) | |
yes, 2 doses | 61 (79.2) | 9 (9.0) | |
yes, 3 doses | 4 (5.2) | 0 (0.0) | |
not been vaccinated | 4 (5.2) | 0 (0.0) | |
Vaccinated for influenza, n (%) | 25 (33.8) | 49 (66.2) | 0.082 |
IBD Patients n = 77 (43.3%) | Control Group n = 101 (56.7%) | Differences between Correlations | |||
---|---|---|---|---|---|
Correlation Estimate (95% CI) | p-Value | Correlation Estimate (95% CI) | p-Value | p-Value | |
I am vaccinated against COVID-19 | 0.16 (−0.06 to 0.38) | 0.1603 | −0.27 (−0.27 to −0.08) | 0.0057 | 0.002 |
Vaccines can prevent severe illness | 0.60 (0.43 to 0.73) | <0.0001 | 0.43 (0.25 to 0.58) | <0.0001 | 0.07 |
COVID-19 vaccination will make the pandemic end sooner | 0.73 (0.60 to 0.83) | <0.0001 | 0.64 (0.50 to 0.75) | <0.0001 | 0.135 |
I believe in COVID-19 vaccine effectiveness | 0.77 (0.65 to 0.85) | <0.0001 | 0.69 (0.57 to 0.78) | <0.0001 | 0.153 |
I’m concerned about the safety of COVID-19 vaccination in IBD | −0.28 (−0.48 to −0.04) | 0.0202 | |||
COVID-19 vaccination may trigger IBD flares | −0.28 (−0.48 to −0.04) | 0.0192 | |||
Type of IBD | 0.07 (−0.16 to−0.30) | 0.5479 | |||
CD location | 0.28 (−0.05 to 0.56) | 0.0962 | |||
UC extension | −0.15 (−0.46 to 0.19) | 0.3902 | |||
Years of disease | 0.12 (−0.11 to 0.35) | 0.2967 | |||
IBD activity | −0.13 (−0.36 to 0.09) | 0.2475 | |||
Treatment | 0.08 (−0.15 to 0.31) | 0.4985 |
IBD Patients n = 77 (43.3%) | Control Group n = 101 (56.7%) | p-Value | |
---|---|---|---|
Physicians’ advice to get COVID-19 vaccine, n (%) | <0.0001 | ||
PCPs | 18 (23.4) | 35 (44.9) | |
Gastroenterologists | 26 (33.8) | 1 (1.3) | |
Other medical field professional/different specialization | 4 (5.1) | 0 (0.0) | |
No one | 23 (33.7) | 42 (53.8) |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Mastrangeli, G.; Vernia, F.; Necozione, S.; Muselli, M.; Frassino, S.; Cesaro, N.; Latella, G.; Fabiani, L. Vaccine Acceptance in Patients with Inflammatory Bowel Disease: Lessons Learned from the COVID-19 Pandemic. Vaccines 2024, 12, 551. https://doi.org/10.3390/vaccines12050551
Mastrangeli G, Vernia F, Necozione S, Muselli M, Frassino S, Cesaro N, Latella G, Fabiani L. Vaccine Acceptance in Patients with Inflammatory Bowel Disease: Lessons Learned from the COVID-19 Pandemic. Vaccines. 2024; 12(5):551. https://doi.org/10.3390/vaccines12050551
Chicago/Turabian StyleMastrangeli, Giada, Filippo Vernia, Stefano Necozione, Mario Muselli, Sara Frassino, Nicola Cesaro, Giovanni Latella, and Leila Fabiani. 2024. "Vaccine Acceptance in Patients with Inflammatory Bowel Disease: Lessons Learned from the COVID-19 Pandemic" Vaccines 12, no. 5: 551. https://doi.org/10.3390/vaccines12050551
APA StyleMastrangeli, G., Vernia, F., Necozione, S., Muselli, M., Frassino, S., Cesaro, N., Latella, G., & Fabiani, L. (2024). Vaccine Acceptance in Patients with Inflammatory Bowel Disease: Lessons Learned from the COVID-19 Pandemic. Vaccines, 12(5), 551. https://doi.org/10.3390/vaccines12050551