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Rheumatologists’ awareness of hepatitis B reactivation before immunosuppressive therapy

  • Bilal TokaEmail author
  • Ahmet Tarik Eminler
  • Emel Gönüllü
  • Mukaddes Tozlu
  • Mustafa Ihsan Uslan
  • Erkan Parlak
  • Oğuz Karabay
  • Aydin Seref Koksal
Observational Research
  • 17 Downloads

Abstract

HBV reactivation (HBVr) is a well-known complication of immunosuppressive (IS) treatment. The aim of this study was to evaluate the awareness of rheumatologists about the risk of HBVr. A survey was sent via e-mail to 270 members of the Turkish Society for Rheumatology. It consisted of fourteen questions on their awareness of the major society guidelines, approach to hepatitis B virus (HBV) screening according to different IS regimens, decision process in screening patients for HBV, knowledge of antiviral treatments for HBV, follow-up strategies, experience and postgraduate training on HBVr. Forty-eight (17.8%) rheumatologists responded to the survey. Of the respondents, 93.8% reported that they screened all patients before IS treatment, while 6.2% screened patients with a high risk of HBV infection only. The screening rate was 95.8% (46/48) in patients undergoing high-risk IS treatment and 35.4% (17/48) in those undergoing low-risk treatment. All respondents screened for HBsAg, and 83.3% (40/48) screened for anti-HBc IgG and anti-HBs. Forty-four (91.7%) rheumatologists had previously initiated antiviral prophylaxis, and 14 (29.2%) had detected HBVr in at least one patient. Rheumatologists had a high awareness of the necessity for HBV screening before IS treatment. However, the screening rates were still lower than desired, especially in patients receiving IS treatments with moderate or low risk of reactivation.

Keywords

Hepatitis B Reactivation Rheumatology Immunosuppressive treatment 

Abbreviations

AASLD

American association for the study of liver diseases

ACG

American College of Rheumatology

AGA

American gastroenterology association

APASL

Asian Pacific association for the study of the liver

DMARD

Disease-modifying antirheumatic drugs

EASL

The European association for the study of the liver

HBV

Hepatitis B virus

HBVr

Hepatitis B virus reactivation

SPSS

Statistical package for social sciences

TRD

Turkish society for rheumatology

USA

United States of America

Notes

Author contributions

Conception or design of the work: BT, ATE, EG, MT, MIU, EP, OK, ASK. Data collection: BT, ATE, EG, MT, MIU and ASK. Data analysis and interpretation: BT, ATE, EG, EP, OK, ASK. Drafting the article: BT, ASK. Critical revision of the article: BT, ATE, EG, EP, OK, ASK. Final approval of the version to be published: BT, ATE, EG, MT, MIU, EP, OK, ASK. All authors approved the final manuscript as submitted. All co-authors take full responsibility of the integrity of the study and all parts of the manuscript.

Funding

The study was funded by the authors.

Compliance with ethical standards

Conflict of interest

Author Toka B., Author Eminler A. T., Author Gönüllü E., Author Tozlu M., Author Uslan M. I., Author Parlak E., Author Karabay O. and Author Köksal A. Ş. have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

References

  1. 1.
    Reynolds JA, Manch RA, Gish RG (2015) Medical interventions associated with HBV reactivation: Common and less common. Clin Liver Dis 5:32–34CrossRefGoogle Scholar
  2. 2.
    Lunel-Fabiani F, Masson C, Ducancelle A (2014) Systemic diseases and biotherapies: understanding, evaluating, and preventing the risk of hepatitis B reactivation. Joint Bone Spine 81:478–484CrossRefGoogle Scholar
  3. 3.
    Perrillo RP, Gish R, Falck-Ytter YT (2015) American Gastroenterological Association Institute technical review on prevention and treatment of hepatitis B virus reactivation during immunosuppressive drug therapy. Gastroenterology 148:221–244CrossRefGoogle Scholar
  4. 4.
    Hoofnagle JH (2009) Reactivation of hepatitis B. Hepatology 49:156–165CrossRefGoogle Scholar
  5. 5.
    EASL clinical practice guidelines (2012) Management of chronic hepatitis B virus infection. J Hepatol 57:167–185CrossRefGoogle Scholar
  6. 6.
    Liaw YF, Kao JH, Piratvisuth T, Chan HL, Chien RN, Liu CJ, Gane E, Locarnini S, Lim SG, Han KH, Amarapurkar D, Cooksley G, Jafri W, Mohamed R, Hou JL, Chuang WL, Lesmana LA, Sollano JD, Suh DJ, Omata M (2012) Asian-Pacific consensus statement on the management of chronic hepatitis B: a 2012 update. Hepatol Int 6:531–561CrossRefGoogle Scholar
  7. 7.
    Terrault NA, Lok ASF, McMahon BJ, Chang KM, Hwang JP, Jonas MM, Brown RS Jr, Bzowej NH, Wong JB (2018) Update on prevention, diagnosis, and treatment of chronic hepatitis B: AASLD 2018 hepatitis B guidance. Hepatology 67:1560–1599CrossRefGoogle Scholar
  8. 8.
    Artz AS, Somerfield MR, Feld JJ, Giusti AF, Kramer BS, Sabichi AL, Zon RT, Wong SL (2010) American society of clinical oncology provisional clinical opinion: chronic hepatitis B virus infection screening in patients receiving cytotoxic chemotherapy for treatment of malignant diseases. J Clin Oncol 28:3199–3202CrossRefGoogle Scholar
  9. 9.
    Saag KG, Teng GG, Patkar NM, Anuntiyo J, Finney C, Curtis JR, Paulus HE, Mudano A, Pisu M, Elkins-Melton M, Outman R, Allison JJ, Suarez Almazor M, Bridges SL Jr, Chatham WW, Hochberg M, MacLean C, Mikuls T, Moreland LW, O’Dell J, Turkiewicz AM, Furst DE (2008) American College of Rheumatology 2008 recommendations for the use of nonbiologic and biologic disease-modifying antirheumatic drugs in rheumatoid arthritis. Arthritis Rheum 59:762–784CrossRefGoogle Scholar
  10. 10.
    Singh JA, Saag KG, Bridges SL Jr, Akl EA, Bannuru RR, Sullivan MC, Vaysbrot E, McNaughton C, Osani M, Shmerling RH, Curtis JR, Furst DE, Parks D, Kavanaugh A, O’Dell J, King C, Leong A, Matteson EL, Schousboe JT, Drevlow B, Ginsberg S, Grober J, St Clair EW, Tindall E, Miller AS, McAlindon T (2016) 2015 American College of rheumatology guideline for the treatment of rheumatoid arthritis. Arthritis Care Res 68:1–25CrossRefGoogle Scholar
  11. 11.
    Tran TT, Rakoski MO, Martin P, Poordad F (2010) Screening for hepatitis B in chemotherapy patients: survey of current oncology practices. Aliment Pharmacol Ther 31:240–246Google Scholar
  12. 12.
    Day FL, Link E, Thursky K, Rischin D (2011) Current hepatitis B screening practices and clinical experience of reactivation in patients undergoing chemotherapy for solid tumors: a nationwide survey of medical oncologists. J Oncol Pract 7:141–147CrossRefGoogle Scholar
  13. 13.
    Jaffari F, Perl A, Allam F (2017) Rheumatologists’ compliance with screening for viral hepatitis B and C prior to initiation of methotrexate treatment needs quality improvement [abstract]. Arthritis Rheumatol 69(suppl 10)Google Scholar
  14. 14.
    Stine JG, Khokhar OS, Charalambopoulos J, Shanmugam VK, Lewis JH (2010) Rheumatologists’ awareness of and screening practices for hepatitis B virus infection prior to initiating immunomodulatory therapy. Arthritis Care Res 62:704–711CrossRefGoogle Scholar
  15. 15.
    Stine JG, Bass M, Ibrahim D, Khokhar OS, Lewis JH (2011) Dermatologists’ awareness of and screening practices for hepatitis B virus infection before initiating tumor necrosis factor-α inhibitor therapy. South Med J 104:781–788CrossRefGoogle Scholar
  16. 16.
    Khokhar OS, Farhadi A, McGrail L, Lewis JH (2009) Oncologists and hepatitis B: a survey to determine current level of awareness and practice of antiviral prophylaxis to prevent reactivation. Chemotherapy 55:69–75CrossRefGoogle Scholar
  17. 17.
    Sampedro B, Hernández-López C, Ferrandiz JR, Illaro A, Fábrega E, Cuadrado A, Iruzubieta P, Menéndez S, Cabezas J, Crespo J (2014) Computerized physician order entry-based system to prevent HBV reactivation in patients treated with biologic agents: the PRESCRIB project. Hepatology 60:106–113CrossRefGoogle Scholar
  18. 18.
    Zeisel MB, Lucifora J, Mason WS, Sureau C, Beck J, Levrero M, Kann M, Knolle PA, Benkirane M, Durantel D, Michel ML, Autran B, Cosset FL, Strick-Marchand H, Trépo C, Kao JH, Carrat F, Lacombe K, Schinazi RF, Barré-Sinoussi F, Delfraissy JF, Zoulim F (2015) Towards an HBV cure: state-of-the-art and unresolved questions-report of the ANRS workshop on HBV cure. Gut 64:1–13CrossRefGoogle Scholar
  19. 19.
    Paul S, Saxena A, Terrin N, Viveiros K, Balk EM, Wong JB (2016) Hepatitis B virus reactivation and prophylaxis during solid tumor chemotherapy: a systematic review and meta-analysis. Ann Intern Med 164:30–40CrossRefGoogle Scholar
  20. 20.
    Lee YH, Bae SC, Song GG (2013) Hepatitis B virus reactivation in HBsAg-positive patients with rheumatic diseases undergoing anti-tumor necrosis factor therapy or DMARDs. Int J Rheum Dis 16:527–531CrossRefGoogle Scholar
  21. 21.
    Urata Y, Uesato R, Tanaka D, Kowatari K, Nitobe T, Nakamura Y, Motomura S (2011) Prevalence of reactivation of hepatitis B virus replication in rheumatoid arthritis patients. Mod Rheumatol 21:16–23CrossRefGoogle Scholar
  22. 22.
    Pattullo V (2015) Hepatitis B reactivation in the setting of chemotherapy and immunosuppression - prevention is better than cure. World J Hepatol 7:954–967CrossRefGoogle Scholar
  23. 23.
    Hsu C, Hsiung CA, Su IJ, Hwang WS, Wang MC, Lin SF, Lin TH, Hsiao HH, Young JH, Chang MC, Liao YM, Li CC, Wu HB, Tien HF, Chao TY, Liu TW, Cheng AL, Chen PJ (2008) A revisit of prophylactic lamivudine for chemotherapy-associated hepatitis B reactivation in non-Hodgkin’s lymphoma: a randomized trial. Hepatology 47:844–853CrossRefGoogle Scholar
  24. 24.
    Sarin SK, Kumar M, Lau GK, Abbas Z, Chan HL, Chen CJ, Chen DS, Chen HL, Chen PJ, Chien RN, Dokmeci AK, Gane E, Hou JL, Jafri W, Jia J, Kim JH, Lai CL, Lee HC, Lim SG, Liu CJ, Locarnini S, Al Mahtab M, Mohamed R, Omata M, Park J, Piratvisuth T, Sharma BC, Sollano J, Wang FS, Wei L, Yuen MF, Zheng SS, Kao JH (2016) Asian-Pacific clinical practice guidelines on the management of hepatitis B: a 2015 update. Hepatol Int 10:1–98CrossRefGoogle Scholar
  25. 25.
    De Clercq E, Férir G, Kaptein S, Neyts J (2010) Antiviral treatment of chronic hepatitis B virus (HBV) infections. Viruses 2:1279–1305CrossRefGoogle Scholar
  26. 26.
    Voican CS, Mir O, Loulergue P, Dhooge M, Brezault C, Dréanic J, Chaussade S, Pol S, Coriat R (2016) Hepatitis B virus reactivation in patients with solid tumors receiving systemic anticancer treatment. Ann Oncol 27:2172–2184CrossRefGoogle Scholar
  27. 27.
    Pattullo V (2016) Prevention of Hepatitis B reactivation in the setting of immunosuppression. Clin Mol Hepatol 22:219–237CrossRefGoogle Scholar
  28. 28.
    Sanagawa A, Kuroda J, Shiota A, Kito N, Takemoto M, Kawade Y, Esaki T, Kimura K (2015) Outcomes of the implementation of the computer-assisted HBView system for the prevention of hepatitis B virus reactivation in chemotherapy patients: a retrospective analysis. J Pharm Health Care Sci 1:29CrossRefGoogle Scholar
  29. 29.
    Visram A, Chan KK, McGee P, Boro J, Hicks LK, Feld JJ (2015) Poor recognition of risk factors for hepatitis B by physicians prescribing immunosuppressive therapy: a call for universal rather than risk-based screening. PLoS One 10:e0120749CrossRefGoogle Scholar
  30. 30.
    Tozun N, Ozdogan O, Cakaloglu Y, Idilman R, Karasu Z, Akarca U, Kaymakoglu S, Ergonul O (2015) Seroprevalence of hepatitis B and C virus infections and risk factors in Turkey: a fieldwork TURHEP study. Clin Microbiol Infect 21:1020–1026CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Gastroenterology, Faculty of MedicineSakarya UniversitySakaryaTurkey
  2. 2.Department of Rheumatology, Faculty of MedicineSakarya UniversitySakaryaTurkey
  3. 3.Department of Infectious Diseases, Faculty of MedicineSakarya UniversitySakaryaTurkey

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