Factors Affecting Initial Humoral Immune Response to SARS-CoV-2 Vaccines among Patients with Inflammatory Bowel Diseases

Michael D. Kappelman; Kimberly N. Weaver; Xian Zhang; Xiangfeng Dai; Runa Watkins; Jeremy Adler; Marla C. Dubinsky; Arthur Kastl; Athos Bousvaros; Jenifer A. Strople; Raymond K. Cross; Peter D.R. Higgins; Ryan C. Ungaro; Meenakshi Bewtra; Emanuelle A. Bellaguarda; Francis A. Farraye; Margie E. Boccieri; A. Firestine; Kelly Y. Chun; Manory Fernando; Monique Bastidas; Michael Zikry; Millie D. Long

doi:10.14309/ajg.0000000000001619

Factors Affecting Initial Humoral Immune Response to SARS-CoV-2 Vaccines among Patients with Inflammatory Bowel Diseases

Michael D. Kappelman^*, Kimberly N. Weaver, Xian Zhang, Xiangfeng Dai, Runa Watkins, Jeremy Adler, Marla C. Dubinsky, Arthur Kastl, Athos Bousvaros, Jenifer A. Strople, Raymond K. Cross, Peter D.R. Higgins, Ryan C. Ungaro, Meenakshi Bewtra, Emanuelle A. Bellaguarda, Francis A. Farraye, Margie E. Boccieri, A. Firestine, Kelly Y. Chun, Manory FernandoMonique Bastidas, Michael Zikry, Millie D. Long

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

36 Scopus citations

Abstract

INTRODUCTION:Although an additional coronavirus disease 2019 vaccine dose for immunocompromised persons has been recommended in some countries, further data to guide vaccination strategies for patients with inflammatory bowel disease (IBD) are urgently needed. We sought to identify factors affecting initial humoral immune response to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccines among patients with IBD.METHODS:In this prospective cohort of SARS-CoV-2 immunized patients with IBD, we evaluated associations between participant age, sex, vaccine type, medication use, and the presence of a detectable antireceptor binding domain antibody and quantitative antibody level.RESULTS:In total, 1,909 participants were included (1,123, 692, and 94 received BNT162b2, mRNA-1273, and Ad26.COV2.S, respectively) of whom 96% achieved a positive antibody response. On multivariable analysis, factors associated with lack of antibody response were older age (P = 0.043), BNT162b2 vs mRNA-1273 (odds ratio [OR] 2.1, 95% confidence interval [CI] 1.0-3.9), and combination therapy with anti-TNF and 6MP, azathioprine, or methotrexate (OR 4.2, 95% CI 2.4-7.3). The use of 5-aminosalicylate or sulfasalazine (OR 0.3, 95% CI 0.1-0.8) and ustekinumab (OR 0.2, 95% CI 0.05-0.8) was associated with decreased odds of lacking antibody response.DISCUSSION:Most patients with IBD mount an initial response to SARS-CoV-2 vaccination; however, older patients and those treated with anti-TNF and immunomodulator have blunted responses and may benefit the most from an additional vaccine dose. Patients treated with other classes of immunosuppressive medications have more robust initial immune responses to vaccination. These data should inform key decisions about patient selection for additional coronavirus disease 2019 vaccine doses in patients with IBD.

Original language	English (US)
Pages (from-to)	462-469
Number of pages	8
Journal	American Journal of Gastroenterology
Volume	117
Issue number	3
DOIs	https://doi.org/10.14309/ajg.0000000000001619
State	Published - Mar 1 2022

Funding

Potential competing interests: M.D.K. has consulted for AbbVie, Janssen, Pfizer, and Takeda; is a shareholder in Johnson & Johnson; and has received research support from Pfizer, Takeda, Janssen, AbbVie, Lilly, Genentech, Boehringer Ingelheim, Bristol Myers Squibb, Celltrion, and Arenapharm. K.N.W. has consulted for AbbVie. X.Z., X.D., and R.W.—no disclosures. J.A. has consulted for Janssen and has received research support from the Gary and Rachel Glick Charitable Fund, Shaevsky Family Research Fund for Crohn's Disease, the Crohn's & Colitis Foundation, and the Leona M. and Harry B. Helmsley Charitable Trust. M.C.D.: consultant fees from AbbVie, Arena, Bristol Myers Squibb, Celgene, Eli Lilly, Gilead, Janssen, Pfizer, Prometheus Labs, and Takeda; grant Support from AbbVie, Prometheus Labs; and license fees from Takeda. A.K.—no disclosures. A.B.—has received research support (subinvestigator on protocols) from the following companies in the past 3 years: Janssen, AbbVie, Takeda, Buhlmann, Arena, and Eli Lilly. He has consulted for Arena, Best Doctors, Eli Lilly, and Takeda, and received royalties from UpToDate. J.A.S. reports no disclosures. R.K.C. has participated in advisory boards and consulting with AbbVie, Bristol Myers Squibb, Eli Lilly, Janssen, LabCorp, Pfizer, Samsung Bioepis, and Takeda. P.D.R.H. has consulted for AbbVie, Pfizer, and Takeda and has received grant support from NIH, CCF, AbbVie, Pfizer, Takeda, Genentech, Eli Lilly, Arena, and the Rainin Foundation. R.C.U. has served as an advisory board member or consultant for AbbVie, Bristol Myers Squibb, Eli Lilly, Janssen, Pfizer, and Takeda; research support from AbbVie, Boehringer Ingelheim, and Pfizer. R.C.U. is funded by an NIH Career Development Award (K23KD111995-01A1). M. Bewtra discloses research funding from Janssen, GlaxoSmithKline, and Takeda, having served as a consultant for Janssen, AbbVie, BMS, and Pfizer, and having received honorarium for participation in a CME program sponsored by AbbVie. E.A.B. has consulted for AbbVie, Pfizer, and Bristol Myers Squibb. F.A.F. is a consultant for Arena, BMS, Braintree Labs, Gilead, GI Reviewers, Innovation Pharmaceuticals, Iterative Scopes, Janssen, Pfizer, and Sebela. He sits on a Data Safety Monitoring Board for Lilly and Theravance. M.E.B., A.F., K.Y.C., M.F., M. Bestidas, M.Z.—no disclosures. M.D.L. has received research/grants from Pfizer and has consulted for AbbVie , Bristol Myers Squibb, Calibr, Eli Lilly, Genentech, Gilead Sciences, Janssen Pharmaceuticals, Pfizer , Roche, Takeda, TARGET PharmaSolutions, and Theravance Biopharma. Study Highlights WHAT IS KNOWN

ASJC Scopus subject areas

Hepatology
Gastroenterology

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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Kappelman, M. D., Weaver, K. N., Zhang, X., Dai, X., Watkins, R., Adler, J., Dubinsky, M. C., Kastl, A., Bousvaros, A., Strople, J. A., Cross, R. K., Higgins, P. D. R., Ungaro, R. C., Bewtra, M., Bellaguarda, E. A., Farraye, F. A., Boccieri, M. E., Firestine, A., Chun, K. Y., ... Long, M. D. (2022). Factors Affecting Initial Humoral Immune Response to SARS-CoV-2 Vaccines among Patients with Inflammatory Bowel Diseases. American Journal of Gastroenterology, 117(3), 462-469. https://doi.org/10.14309/ajg.0000000000001619

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title = "Factors Affecting Initial Humoral Immune Response to SARS-CoV-2 Vaccines among Patients with Inflammatory Bowel Diseases",

abstract = "INTRODUCTION:Although an additional coronavirus disease 2019 vaccine dose for immunocompromised persons has been recommended in some countries, further data to guide vaccination strategies for patients with inflammatory bowel disease (IBD) are urgently needed. We sought to identify factors affecting initial humoral immune response to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccines among patients with IBD.METHODS:In this prospective cohort of SARS-CoV-2 immunized patients with IBD, we evaluated associations between participant age, sex, vaccine type, medication use, and the presence of a detectable antireceptor binding domain antibody and quantitative antibody level.RESULTS:In total, 1,909 participants were included (1,123, 692, and 94 received BNT162b2, mRNA-1273, and Ad26.COV2.S, respectively) of whom 96% achieved a positive antibody response. On multivariable analysis, factors associated with lack of antibody response were older age (P = 0.043), BNT162b2 vs mRNA-1273 (odds ratio [OR] 2.1, 95% confidence interval [CI] 1.0-3.9), and combination therapy with anti-TNF and 6MP, azathioprine, or methotrexate (OR 4.2, 95% CI 2.4-7.3). The use of 5-aminosalicylate or sulfasalazine (OR 0.3, 95% CI 0.1-0.8) and ustekinumab (OR 0.2, 95% CI 0.05-0.8) was associated with decreased odds of lacking antibody response.DISCUSSION:Most patients with IBD mount an initial response to SARS-CoV-2 vaccination; however, older patients and those treated with anti-TNF and immunomodulator have blunted responses and may benefit the most from an additional vaccine dose. Patients treated with other classes of immunosuppressive medications have more robust initial immune responses to vaccination. These data should inform key decisions about patient selection for additional coronavirus disease 2019 vaccine doses in patients with IBD.",

author = "Kappelman, {Michael D.} and Weaver, {Kimberly N.} and Xian Zhang and Xiangfeng Dai and Runa Watkins and Jeremy Adler and Dubinsky, {Marla C.} and Arthur Kastl and Athos Bousvaros and Strople, {Jenifer A.} and Cross, {Raymond K.} and Higgins, {Peter D.R.} and Ungaro, {Ryan C.} and Meenakshi Bewtra and Bellaguarda, {Emanuelle A.} and Farraye, {Francis A.} and Boccieri, {Margie E.} and A. Firestine and Chun, {Kelly Y.} and Manory Fernando and Monique Bastidas and Michael Zikry and Long, {Millie D.}",

year = "2022",

month = mar,

day = "1",

doi = "10.14309/ajg.0000000000001619",

language = "English (US)",

volume = "117",

pages = "462--469",

journal = "American Journal of Gastroenterology",

issn = "0002-9270",

publisher = "Wolters Kluwer Health",

number = "3",

}

Kappelman, MD, Weaver, KN, Zhang, X, Dai, X, Watkins, R, Adler, J, Dubinsky, MC, Kastl, A, Bousvaros, A, Strople, JA, Cross, RK, Higgins, PDR, Ungaro, RC, Bewtra, M, Bellaguarda, EA, Farraye, FA, Boccieri, ME, Firestine, A, Chun, KY, Fernando, M, Bastidas, M, Zikry, M & Long, MD 2022, 'Factors Affecting Initial Humoral Immune Response to SARS-CoV-2 Vaccines among Patients with Inflammatory Bowel Diseases', American Journal of Gastroenterology, vol. 117, no. 3, pp. 462-469. https://doi.org/10.14309/ajg.0000000000001619

TY - JOUR

T1 - Factors Affecting Initial Humoral Immune Response to SARS-CoV-2 Vaccines among Patients with Inflammatory Bowel Diseases

AU - Kappelman, Michael D.

AU - Weaver, Kimberly N.

AU - Zhang, Xian

AU - Dai, Xiangfeng

AU - Watkins, Runa

AU - Adler, Jeremy

AU - Dubinsky, Marla C.

AU - Kastl, Arthur

AU - Bousvaros, Athos

AU - Strople, Jenifer A.

AU - Cross, Raymond K.

AU - Higgins, Peter D.R.

AU - Ungaro, Ryan C.

AU - Bewtra, Meenakshi

AU - Bellaguarda, Emanuelle A.

AU - Farraye, Francis A.

AU - Boccieri, Margie E.

AU - Firestine, A.

AU - Chun, Kelly Y.

AU - Fernando, Manory

AU - Bastidas, Monique

AU - Zikry, Michael

AU - Long, Millie D.

PY - 2022/3/1

Y1 - 2022/3/1

N2 - INTRODUCTION:Although an additional coronavirus disease 2019 vaccine dose for immunocompromised persons has been recommended in some countries, further data to guide vaccination strategies for patients with inflammatory bowel disease (IBD) are urgently needed. We sought to identify factors affecting initial humoral immune response to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccines among patients with IBD.METHODS:In this prospective cohort of SARS-CoV-2 immunized patients with IBD, we evaluated associations between participant age, sex, vaccine type, medication use, and the presence of a detectable antireceptor binding domain antibody and quantitative antibody level.RESULTS:In total, 1,909 participants were included (1,123, 692, and 94 received BNT162b2, mRNA-1273, and Ad26.COV2.S, respectively) of whom 96% achieved a positive antibody response. On multivariable analysis, factors associated with lack of antibody response were older age (P = 0.043), BNT162b2 vs mRNA-1273 (odds ratio [OR] 2.1, 95% confidence interval [CI] 1.0-3.9), and combination therapy with anti-TNF and 6MP, azathioprine, or methotrexate (OR 4.2, 95% CI 2.4-7.3). The use of 5-aminosalicylate or sulfasalazine (OR 0.3, 95% CI 0.1-0.8) and ustekinumab (OR 0.2, 95% CI 0.05-0.8) was associated with decreased odds of lacking antibody response.DISCUSSION:Most patients with IBD mount an initial response to SARS-CoV-2 vaccination; however, older patients and those treated with anti-TNF and immunomodulator have blunted responses and may benefit the most from an additional vaccine dose. Patients treated with other classes of immunosuppressive medications have more robust initial immune responses to vaccination. These data should inform key decisions about patient selection for additional coronavirus disease 2019 vaccine doses in patients with IBD.

AB - INTRODUCTION:Although an additional coronavirus disease 2019 vaccine dose for immunocompromised persons has been recommended in some countries, further data to guide vaccination strategies for patients with inflammatory bowel disease (IBD) are urgently needed. We sought to identify factors affecting initial humoral immune response to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccines among patients with IBD.METHODS:In this prospective cohort of SARS-CoV-2 immunized patients with IBD, we evaluated associations between participant age, sex, vaccine type, medication use, and the presence of a detectable antireceptor binding domain antibody and quantitative antibody level.RESULTS:In total, 1,909 participants were included (1,123, 692, and 94 received BNT162b2, mRNA-1273, and Ad26.COV2.S, respectively) of whom 96% achieved a positive antibody response. On multivariable analysis, factors associated with lack of antibody response were older age (P = 0.043), BNT162b2 vs mRNA-1273 (odds ratio [OR] 2.1, 95% confidence interval [CI] 1.0-3.9), and combination therapy with anti-TNF and 6MP, azathioprine, or methotrexate (OR 4.2, 95% CI 2.4-7.3). The use of 5-aminosalicylate or sulfasalazine (OR 0.3, 95% CI 0.1-0.8) and ustekinumab (OR 0.2, 95% CI 0.05-0.8) was associated with decreased odds of lacking antibody response.DISCUSSION:Most patients with IBD mount an initial response to SARS-CoV-2 vaccination; however, older patients and those treated with anti-TNF and immunomodulator have blunted responses and may benefit the most from an additional vaccine dose. Patients treated with other classes of immunosuppressive medications have more robust initial immune responses to vaccination. These data should inform key decisions about patient selection for additional coronavirus disease 2019 vaccine doses in patients with IBD.

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DO - 10.14309/ajg.0000000000001619

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JO - American Journal of Gastroenterology

JF - American Journal of Gastroenterology

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ER -

Factors Affecting Initial Humoral Immune Response to SARS-CoV-2 Vaccines among Patients with Inflammatory Bowel Diseases

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