Advertisement

Digestive Diseases and Sciences

, Volume 63, Issue 6, pp 1532–1540 | Cite as

Lower Sustained Diphtheria and Pertussis Antibody Concentrations in Inflammatory Bowel Disease Patients

  • Freddy Caldera
  • Sumona Saha
  • Arnold Wald
  • Christine A. Garmoe
  • Sue McCrone
  • Bryant Megna
  • Dana Ley
  • Mark Reichelderfer
  • Mary S. Hayney
Original Article

Abstract

Background

Patients with inflammatory bowel disease (IBD) are often immunosuppressed, and those patients receiving anti-tumor necrosis factor α (TNF) therapy can have lower antibody responses to vaccines. Pertussis cases are at their highest levels in the post-vaccine era. There is little data regarding responses to the Tdap (tetanus, diphtheria, and acellular pertussis) vaccine in IBD patients.

Aims

The aim of this study was to compare sustained vaccine-induced Tdap antibody concentrations in a cohort of IBD patients stratified by medication regimens with healthy controls (HC) who had received an adult Tdap booster.

Methods

We performed a cross-sectional study evaluating antibody responses to Tdap vaccine among IBD patients compared to HC. Our study consisted of three patient groups: adults with IBD stratified by maintenance medication regimen: (1) thiopurine monotherapy; (2) anti-TNF monotherapy; and (3) combination therapy (anti-TNF and immunomodulator (thiopurine or methotrexate)).

Results

Ninety IBD patients and 20 HC participated. Pertussis pertactin antibody concentrations were significantly lower in IBD patients (p = 0.021) compared to HC, and those on anti-TNF agents (monotherapy or combination) had lower antibody concentrations compared to those on thiopurine monotherapy (p = 0.028). Diphtheria antibody concentrations were also lower in IBD patients (p < 0.001), and those on anti-TNF agents (monotherapy or combination) had lower antibody concentrations compared to the thiopurine monotherapy group (p < 0.001).

Conclusion

IBD patients on anti-TNF agents had lower antibody concentrations to diphtheria and pertussis. These findings suggest a need for different Tdap booster schedules for IBD patients on anti-TNF therapy.

Clinical Trials Registry NCT02434133.

Keywords

Tetanus Diphtheria Pertussis Immunization Inflammatory bowel disease 

Notes

Acknowledgments

The project described was supported by the Clinical and Translational Science Award (CTSA) program, through the NIH National Center for Advancing Translational Sciences (NCATS), Grant UL1TR000427. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH.

Funding

This work was supported by the Sal Family Foundation, University of Wisconsin Division of Gastroenterology and Hepatology and the University of Wisconsin School of Pharmacy.

Compliance with ethical standards

Conflict of interest

Drs. Caldera, Wald and Reichelderfer and Ms. McCrone, Ms. Garmoe, Mr. Megna, and Ms. Ley declare that they have no competing interests/financial disclosures. Dr. Hayney serves on the speakers’ bureau for Sanofi Pasteur Vaccines. Dr. Saha is a consultant with UCB Biosciences.

References

  1. 1.
    Terdiman JP, Gruss CB, Heidelbaugh JJ, Sultan S, Falck-Ytter YT. American gastroenterological association institute guideline on the use of thiopurines, methotrexate, and anti–TNF-α biologic drugs for the induction and maintenance of remission in inflammatory Crohn’s disease. Gastroenterology. 2013;145:1459–1463.CrossRefPubMedGoogle Scholar
  2. 2.
    Farraye FA, Melmed GY, Lichtenstein GR, Kane SV. ACG clinical guideline: preventive care in inflammatory bowel disease. Am J Gastroenterol. 2017;112:241–258.CrossRefPubMedGoogle Scholar
  3. 3.
    Roush SW, Murphy TV, Vaccine-Preventable Disease Table Working Group a. Historical comparisons of morbidity and mortality for vaccine-preventable diseases in the united states. JAMA. 2007;298:2155–2163.CrossRefPubMedGoogle Scholar
  4. 4.
    Kantsone I, Lucenko I, Perevoscikovs J. More than 20 years after re-emerging in the 1990s diphtheria remains a public health problem in Latvia. Eurosurveillance. 2016;21:30414.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Kim DK, Riley LE, Harriman KH, Hunter P, Bridges CB. Advisory Committee on Immunization Practices recommended immunization schedule for adults aged 19 years or older, United States, 2017. Ann Intern Med. 2017;166:209–219.CrossRefPubMedGoogle Scholar
  6. 6.
    Wagner KS, White JM, Andrews NJ, et al. Immunity to tetanus and diphtheria in the UK in 2009. Vaccine. 2012;30:7111–7117.CrossRefPubMedGoogle Scholar
  7. 7.
    Hammarlund E, Thomas A, Poore EA, et al. Durability of vaccine-induced immunity against tetanus and diphtheria toxins: a cross-sectional analysis clinical infectious. Diseases. 2016;62:1111–1118.Google Scholar
  8. 8.
    Centers for Disease Control and Prevention. Pertussis vaccination: use of acellular pertussis vaccines among infants and young children. Recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recommend Rep.Google Scholar
  9. 9.
    Center for Disease Control. Pertussis cases by year (1922–2015). Available at: https://www.cdc.gov/pertussis/surv-reporting/cases-by-year.html; Accessed 31.10.17.
  10. 10.
    European Centre for Disease Prevention and Control. Annual epidemiological report pertussis 2014 data reported on July 7 2016. Available at: http://ecdc.europa.eu/en/healthtopics/pertussis/Pages/Annual-epidemiological-report-2016.aspx; 2017 Accessed 31.10.17.
  11. 11.
    Winter K, Harriman K, Zipprich J, et al. California pertussis epidemic, 2010. J Pediatr. 2012;161:1091–1096.CrossRefPubMedGoogle Scholar
  12. 12.
    Acosta AM, DeBolt C, Tasslimi A, et al. Tdap vaccine effectiveness in adolescents during the 2012 washington state pertussis epidemic. Pediatr. 2015;135:981–989.CrossRefGoogle Scholar
  13. 13.
    Dotan I, Werner L, Vigodman S, et al. Normal response to vaccines in inflammatory bowel disease patients treated with thiopurines. Inflamm Bowel Dis. 2012;18:261–268.CrossRefPubMedGoogle Scholar
  14. 14.
    Dezfoli S, Horton HA, Thepyasuwan N, et al. Combined immunosuppression impairs immunogenicity to tetanus and pertussis vaccination among patients with inflammatory bowel disease. Inflamm Bowel Dis. 2015;21:1754–1760.CrossRefPubMedGoogle Scholar
  15. 15.
    Cullen G, Bader C, Korzenik JR, Sands BE. Serological response to the 2009 H1N1 influenza vaccination in patients with inflammatory bowel disease. Gut. 2012;61:385–391.CrossRefPubMedGoogle Scholar
  16. 16.
    Banaszkiewicz A, Gawronska A, Klincewicz B, et al. Immunogenicity of pertussis booster vaccination in children and adolescents with inflammatory bowel disease: a controlled study. Inflamm Bowel Dis. 2017;23:847–852.CrossRefPubMedGoogle Scholar
  17. 17.
    Wisconsin Department of Health Services. Wisconsin Immunization Registry (WIR). Available at: https://www.dhs.wisconsin.gov/immunization/wir.htm; 2017 Accessed 31.10.17.
  18. 18.
    Hodder SL, Cherry JD, Mortimer JEA, Ford AB, Gornbein J, Papp K. Antibody responses to Bordetella pertussis antigens and clinical correlations in elderly community residents. Clin Infect Dis. 2000;31:7–14.CrossRefPubMedGoogle Scholar
  19. 19.
    Storsaeter J, Hallander HO, Gustafsson L, Olin P. Levels of anti-pertussis antibodies related to protection after household exposure to Bordetella pertussis. Vaccine. 1998;16:1907–1916.CrossRefPubMedGoogle Scholar
  20. 20.
    Rohde KA, Cunningham KC, Henriquez KM, Nielsen AR, Worzella SL, Hayney MS. A cross-sectional study of tetanus and diphtheria antibody concentrations post vaccination among lung transplant patients compared with healthy individuals. Transpl Inf Dis. 2014;16:871–877.CrossRefGoogle Scholar
  21. 21.
    Plotkin SA. Correlates of protection induced by vaccination. Clin Vaccine Immunol. 2010;17:1055–1065.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Dominicus R, Galtier F, Richard P, Baudin M. Immunogenicity and safety of one dose of diphtheria, tetanus, acellular pertussis and poliomyelitis vaccine (Repevax®) followed by two doses of diphtheria, tetanus and poliomyelitis vaccine (Revaxis®) in adults aged ≥ 40 years not receiving a diphtheria- and tetanus-containing vaccination in the last 20 years. Vaccine. 2014;32:3942–3949.CrossRefPubMedGoogle Scholar
  23. 23.
    John T, Voysey M, Yu LM, et al. Immunogenicity of a low-dose diphtheria, tetanus and acellular pertussis combination vaccine with either inactivated or oral polio vaccine compared to standard-dose diphtheria, tetanus, acellular pertussis when used as a pre-school booster in UK children: a 5-year follow-up of a randomised controlled study. Vaccine. 2015;33:4579–4585.CrossRefPubMedGoogle Scholar
  24. 24.
    Marshall GS, Pool V, Greenberg DP, Johnson DR, Sheng X, Decker MD. Safety and immunogenicity of tetanus-diphtheria-acellular pertussis vaccine administered to children 10 or 11 years of age. Clin Vaccine Immunol. 2014;21:1560–1564.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Weston WM, Friedland LR, Wu X, Howe B. Vaccination of adults 65 years of age and older with tetanus toxoid, reduced diphtheria toxoid and acellular pertussis vaccine (Boostrix®): results of two randomized trials. Vaccine. 2012;30:1721–1728.CrossRefPubMedGoogle Scholar
  26. 26.
    Cleveland NK, Rodriquez D, Wichman A, Pan I, Melmed GY, Rubin DT. Many inflammatory bowel disease patients are not immune to measles or pertussis. Dig Dis Sci. 2016;61:2972–2976.CrossRefPubMedGoogle Scholar
  27. 27.
    Euopean Centre for Disease Prevention and Control. Vaccine Schedule. Available at: http://vaccine-schedule.ecdc.europa.eu/Pages/Scheduler.aspx; 2017 Accessed 31.10.17.
  28. 28.
    Rahier JF, Magro F, Abreu C, et al. Second European evidence-based consensus on the prevention, diagnosis and management of opportunistic infections in inflammatory bowel disease. J Crohn’s Colitis. 2014;8:443–468.CrossRefGoogle Scholar
  29. 29.
    Schwartz KL, Kwong JC, Deeks SL, et al. Effectiveness of pertussis vaccination and duration of immunity CMAJ. Can Med Assoc J. 2016;188:E399–E406.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Freddy Caldera
    • 1
  • Sumona Saha
    • 1
  • Arnold Wald
    • 1
  • Christine A. Garmoe
    • 3
  • Sue McCrone
    • 3
  • Bryant Megna
    • 2
  • Dana Ley
    • 2
  • Mark Reichelderfer
    • 1
  • Mary S. Hayney
    • 3
  1. 1.Department of Medicine, Division of Gastroenterology and HepatologyUniversity of Wisconsin School of Medicine and Public HealthMadisonUSA
  2. 2.School of Medicine and Public HealthUniversity of WisconsinMadisonUSA
  3. 3.School of PharmacyUniversity of WisconsinMadisonUSA

Personalised recommendations