Skip to main content

Advertisement

Log in

Increased risk of herpes zoster infection in patients with inflammatory bowel disease: a meta-analysis of cohort studies

  • Review
  • Published:
European Journal of Clinical Microbiology & Infectious Diseases Aims and scope Submit manuscript

Abstract

Previous studies have shown increased risk of herpes zoster (HZ) infection in patients with inflammatory bowel disease (IBD). The aim of this study is to better characterize this possible association by conducting a meta-analysis. A comprehensive search of relevant literature until April 30, 2019, was performed. Data on HZ infection and medications in patients with IBD and controls were extracted. The relative risk (RR) and 95% confidence interval (CI) were calculated. Subgroup analyses were performed to assess the source of heterogeneity. Seven cohort studies were included that involved more than 1,000,000 participants. The RR of HZ infection in patients with Crohn’s disease (CD) compared with non-CD patients was 1.74 (95% CI 1.57–1.92, p < 0.001). The pooled RR of HZ infection in patients with ulcerative colitis (UC) compared with non-UC was 1.40 (95% CI 1.31–1.50, p < 0.001). Subgroup analyses revealed that age, race, and publication year contribute to heterogeneity. We also found that steroid users were at increased risk of HZ in CD (OR = 1.78, 95% CI 1.10–2.88). Steroid users and anti-TNFα users were at increased risk of HZ in UC, with RRs of 1.99 (95% CI 1.64–2.42) and 2.29 (95% CI 1.52–3.45), respectively. Begg’s test and Egger’s test suggested no publication bias. There was a 74% increased risk of HZ infection in patients with CD and 40% increased risk of HZ infection in patients with UC compared with that in non-IBD. IBD patients with high risk of HZ infection may benefit from an HZ vaccine.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Park JH, Peyrin-Biroulet L, Eisenhut M, Shin JI (2017) IBD immunopathogenesis: a comprehensive review of inflammatory molecules. Autoimmun Rev 16(4):416–426. https://doi.org/10.1016/j.autrev.2017.02.013

    Article  CAS  PubMed  Google Scholar 

  2. Bernstein CN, Fried M, Krabshuis JH, Cohen H, Eliakim R, Fedail S, Gearry R, Goh KL, Hamid S, Khan AG, LeMair AW, Malfertheiner OQ, Rey JF, Sood A, Steinwurz F, Thomsen OO, Thomson A, Watermeyer G (2010) World Gastroenterology Organization practice guidelines for the diagnosis and management of IBD in 2010. Inflamm Bowel Dis 16(1):112–124. https://doi.org/10.1002/ibd.21048

    Article  PubMed  Google Scholar 

  3. Khan N, Patel D, Trivedi C, Shah Y, Lichtenstein G, Lewis J, Yang YX (2018) Overall and comparative risk of herpes zoster with pharmacotherapy for inflammatory bowel diseases: a nationwide cohort study. Clinical gastroenterology and hepatology : the official clinical practice journal of the American Gastroenterological Association 16(12):1919–1927.e1913. https://doi.org/10.1016/j.cgh.2017.12.052

    Article  Google Scholar 

  4. Kirchgesner J, Lemaitre M, Carrat F, Zureik M, Carbonnel F, Dray-Spira R (2018) Risk of serious and opportunistic infections associated with treatment of inflammatory bowel diseases. Gastroenterology 155(2):337–346.e310. https://doi.org/10.1053/j.gastro.2018.04.012

    Article  Google Scholar 

  5. Bonovas S, Fiorino G, Allocca M, Lytras T, Nikolopoulos GK, Peyrin-Biroulet L, Danese S (2016) Biologic therapies and risk of infection and malignancy in patients with inflammatory bowel disease: a systematic review and network meta-analysis. Clinical gastroenterology and hepatology : the official clinical practice journal of the American Gastroenterological Association 14(10):1385–1397.e1310. https://doi.org/10.1016/j.cgh.2016.04.039

    Article  Google Scholar 

  6. Yawn BP, Saddier P, Wollan PC, St Sauver JL, Kurland MJ, Sy LS (2007) A population-based study of the incidence and complication rates of herpes zoster before zoster vaccine introduction. Mayo Clin Proc 82(11):1341–1349

    Article  Google Scholar 

  7. Lin YH, Huang LM, Chang IS, Tsai FY, Lu CY, Shao PL, Chang LY (2010) Disease burden and epidemiology of herpes zoster in pre-vaccine Taiwan. Vaccine 28(5):1217–1220. https://doi.org/10.1016/j.vaccine.2009.11.029

    Article  PubMed  Google Scholar 

  8. Harpaz R, Ortega-Sanchez IR, Seward JF (2008) Prevention of herpes zoster: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR recommendations and reports : morbidity and mortality weekly report recommendations and reports 57(Rr-5):1–30 quiz CE32-34

    PubMed  Google Scholar 

  9. Forbes HJ, Bhaskaran K, Thomas SL, Smeeth L, Clayton T, Langan SM (2014) Quantification of risk factors for herpes zoster: population based case-control study. BMJ (Clinical research ed) 348:g2911. https://doi.org/10.1136/bmj.g2911

    Article  CAS  Google Scholar 

  10. Smitten AL, Choi HK, Hochberg MC, Suissa S, Simon TA, Testa MA, Chan KA (2007) The risk of herpes zoster in patients with rheumatoid arthritis in the United States and the United Kingdom. Arthritis Rheum 57(8):1431–1438. https://doi.org/10.1002/art.23112

    Article  PubMed  Google Scholar 

  11. Cote-Daigneault J, Bessissow T, Nicolae MV, Nie R, Bitton A, Lakatos PL, Brassard P (2018) Herpes zoster incidence in inflammatory bowel disease patients: a population-based study. Inflamm Bowel Dis. https://doi.org/10.1093/ibd/izy311

    Article  Google Scholar 

  12. Gupta G, Lautenbach E, Lewis JD (2006) Incidence and risk factors for herpes zoster among patients with inflammatory bowel disease. Clinical gastroenterology and hepatology : the official clinical practice journal of the American Gastroenterological Association 4(12):1483–1490. https://doi.org/10.1016/j.cgh.2006.09.019

    Article  Google Scholar 

  13. Long MD, Martin C, Sandler RS, Kappelman MD (2013) Increased risk of herpes zoster among 108 604 patients with inflammatory bowel disease. Aliment Pharmacol Ther 37(4):420–429. https://doi.org/10.1111/apt.12182

    Article  CAS  PubMed  Google Scholar 

  14. Soh H, Chun J, Han K, Park S, Choi G, Kim JH, Lee J, Im JP, Kim JS (2018) Increased risk of herpes zoster in young and metabolically healthy patients with inflammatory bowel disease: a nationwide population-based study. Gut and liver. https://doi.org/10.5009/gnl18304

    Article  Google Scholar 

  15. Tsai SY, Yang TY, Lin CL, Tsai YH, Kuo CF, Kao CH (2015) Increased risk of varicella zoster virus infection in inflammatory bowel disease in an Asian population: a nationwide population-based cohort study. Int J Clin Pract 69(2):228–234. https://doi.org/10.1111/ijcp.12508

    Article  PubMed  Google Scholar 

  16. Chang K, Lee HS, Kim YJ, Kim SO, Kim SH, Lee SH, Song EM, Hwang SW, Park SH, Yang DH, Ye BD, Byeon JS, Myung SJ, Yang SK (2018) Increased risk of herpes zoster infection in patients with inflammatory bowel diseases in Korea. Clinical gastroenterology and hepatology : the official clinical practice journal of the American Gastroenterological Association 16(12):1928–1936.e1922. https://doi.org/10.1016/j.cgh.2018.05.024

    Article  Google Scholar 

  17. Marehbian J, Arrighi HM, Hass S, Tian H, Sandborn WJ (2009) Adverse events associated with common therapy regimens for moderate-to-severe Crohn’s disease. Am J Gastroenterol 104(10):2524–2533. https://doi.org/10.1038/ajg.2009.322

    Article  PubMed  Google Scholar 

  18. Stang A (2010) Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 25(9):603–605. https://doi.org/10.1007/s10654-010-9491-z

    Article  Google Scholar 

  19. Siristatidis C, Sergentanis TN, Kanavidis P, Trivella M, Sotiraki M, Mavromatis I, Psaltopoulou T, Skalkidou A, Petridou ET (2013) Controlled ovarian hyperstimulation for IVF: impact on ovarian, endometrial and cervical cancer--a systematic review and meta-analysis. Hum Reprod Update 19(2):105–123. https://doi.org/10.1093/humupd/dms051

    Article  CAS  PubMed  Google Scholar 

  20. Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ (Clinical research ed) 327(7414):557–560. https://doi.org/10.1136/bmj.327.7414.557

    Article  Google Scholar 

  21. Khan N, Trivedi C, Kavani H, Medvedeva E, Lewis J, Yang YX (2018) Efficacy of live attenuated herpes zoster vaccine in patients with inflammatory bowel diseases. Clinical gastroenterology and hepatology : the official clinical practice journal of the American Gastroenterological Association. https://doi.org/10.1016/j.cgh.2018.10.016

    Article  CAS  Google Scholar 

  22. Che H, Lukas C, Morel J, Combe B (2014) Risk of herpes/herpes zoster during anti-tumor necrosis factor therapy in patients with rheumatoid arthritis. Systematic review and meta-analysis. Joint, bone, spine : revue du rhumatisme 81(3):215–221. https://doi.org/10.1016/j.jbspin.2013.07.009

    Article  CAS  Google Scholar 

  23. Marra F, Lo E, Kalashnikov V, Richardson K (2016) Risk of herpes zoster in individuals on biologics, disease-modifying antirheumatic drugs, and/or corticosteroids for autoimmune diseases: a systematic review and meta-analysis. Open forum infectious diseases 3(4):ofw205. https://doi.org/10.1093/ofid/ofw205

    Article  PubMed  PubMed Central  Google Scholar 

  24. Winthrop KL, Baddley JW, Chen L, Liu L, Grijalva CG, Delzell E, Beukelman T, Patkar NM, Xie F, Saag KG, Herrinton LJ, Solomon DH, Lewis JD, Curtis JR (2013) Association between the initiation of anti-tumor necrosis factor therapy and the risk of herpes zoster. Jama 309(9):887–895. https://doi.org/10.1001/jama.2013.1099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Sandborn WJ, Ghosh S, Panes J, Vranic I, Su C, Rousell S, Niezychowski W (2012) Tofacitinib, an oral Janus kinase inhibitor, in active ulcerative colitis. N Engl J Med 367(7):616–624. https://doi.org/10.1056/NEJMoa1112168

    Article  CAS  PubMed  Google Scholar 

  26. Winthrop KL, Melmed GY, Vermeire S, Long MD, Chan G, Pedersen RD, Lawendy N, Thorpe AJ, Nduaka CI, Su C (2018) Herpes zoster infection in patients with ulcerative colitis receiving tofacitinib. Inflamm Bowel Dis 24(10):2258–2265. https://doi.org/10.1093/ibd/izy131

    Article  PubMed  PubMed Central  Google Scholar 

  27. Farraye FA, Melmed GY, Lichtenstein GR, Kane SV (2017) ACG clinical guideline: preventive care in inflammatory bowel disease. Am J Gastroenterol 112(2):241–258. https://doi.org/10.1038/ajg.2016.537

    Article  PubMed  Google Scholar 

  28. Rahier JF, Magro F, Abreu C, Armuzzi A, Ben-Horin S, Chowers Y, Cottone M, de Ridder L, Doherty G, Ehehalt R, Esteve M, Katsanos K, Lees CW, Macmahon E, Moreels T, Reinisch W, Tilg H, Tremblay L, Veereman-Wauters G, Viget N, Yazdanpanah Y, Eliakim R, Colombel JF (2014) Second European evidence-based consensus on the prevention, diagnosis and management of opportunistic infections in inflammatory bowel disease. J Crohns Colitis 8(6):443–468. https://doi.org/10.1016/j.crohns.2013.12.013

    Article  CAS  PubMed  Google Scholar 

  29. Zhang J, Xie F, Delzell E, Chen L, Winthrop KL, Lewis JD, Saag KG, Baddley JW, Curtis JR (2012) Association between vaccination for herpes zoster and risk of herpes zoster infection among older patients with selected immune-mediated diseases. Jama 308(1):43–49. https://doi.org/10.1001/jama.2012.7304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Khan N, Shah Y, Trivedi C, Lewis JD (2017) Safety of herpes zoster vaccination among inflammatory bowel disease patients being treated with anti-TNF medications. Aliment Pharmacol Ther 46(7):668–672. https://doi.org/10.1111/apt.14257

    Article  CAS  PubMed  Google Scholar 

  31. Khan N, Trivedi C, Shah Y, Patel D, Lewis J, Yang YX (2018) The severity of herpes zoster in inflammatory bowel disease patients treated with anti-TNF agents. Inflamm Bowel Dis 24(6):1274–1279. https://doi.org/10.1093/ibd/izx115

    Article  PubMed  Google Scholar 

  32. Wasan SK, Zullow S, Berg A, Cheifetz AS, Ganley-Leal L, Farraye FA (2016) Herpes zoster vaccine response in inflammatory bowel disease patients on low-dose immunosuppression. Inflamm Bowel Dis 22(6):1391–1396. https://doi.org/10.1097/mib.0000000000000743

    Article  PubMed  Google Scholar 

  33. Thomas SL, Hall AJ (2004) What does epidemiology tell us about risk factors for herpes zoster? Lancet Infect Dis 4(1):26–33

    Article  Google Scholar 

  34. Tseng HF, Smith N, Harpaz R, Bialek SR, Sy LS, Jacobsen SJ (2011) Herpes zoster vaccine in older adults and the risk of subsequent herpes zoster disease. Jama 305(2):160–166. https://doi.org/10.1001/jama.2010.1983

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This work was supported by the grants from Medical Science Research Foundation of Health Bureau of Zhejiang Province (WKJ-ZJ-1516).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Guoqiang Xu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Informed consent

Irrelevant due to study design.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ning, L., Liu, R., Li, S. et al. Increased risk of herpes zoster infection in patients with inflammatory bowel disease: a meta-analysis of cohort studies. Eur J Clin Microbiol Infect Dis 39, 219–227 (2020). https://doi.org/10.1007/s10096-019-03706-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-019-03706-9

Keywords

Navigation