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Hepatitis B carrier state among SLE patients: case–control study

  • Therapeutic Aspects in Autoimmunity
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Abstract

The association between hepatitis B and autoimmune disorders has been intriguing for decades. Many reports have speculated on the possible linkage between these two conditions, yet never before data driven from a large national database was utilized in order to investigate this issue. The objective of this study was to investigate the association between SLE and hepatitis B carrier state. Patients with SLE were compared with age- and sex-matched controls regarding the proportion of hepatitis B carrier state in a case–control study. Chi-square and t tests were used for univariate analysis, and a logistic regression model was used for multivariate analysis. The study was performed utilizing the medical database of Clalit Health Services. The study included 5018 lupus patients over the age of 20 years and 25,090 age- and sex-frequency-matched controls without SLE. The proportion of hepatitis B carriers was higher in SLE patients as compared to controls (0.9 and 0.56 %, respectively; p < 0.001). A significant association was also observed among patients in lower socioeconomic status. In a multivariate logistic regression analysis, SLE was significantly associated with hepatitis B (OR = 1.828, 95 % CI = 1.291–2.590). Patients with SLE have a greater proportion of hepatitis B carrier state than matched controls.

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References

  1. Borchers AT, Naguwa SM, Shoenfeld Y, Gershwin ME. The geoepidemiology of systemic lupus erythematosus. Autoimmun Rev. 2010;9(5):A277–87.

    Article  CAS  PubMed  Google Scholar 

  2. Borchers AT, Leibushor N, Naguwa SM, Cheema GS, Shoenfeld Y, Gershwin ME. Lupus nephritis: a critical review. Autoimmun Rev. 2012;12(2):174–94.

    Article  PubMed  Google Scholar 

  3. Danchenko N, Satia JA, Anthony MS. Epidemiology of systemic lupus erythematosus: a comparison of worldwide disease burden. Lupus. 2006;15(5):308–18.

    Article  CAS  PubMed  Google Scholar 

  4. Ingvarsson RF, Bengtsson AA, Jönsen A. Variations in the epidemiology of systemic lupus erythematosus in southern Sweden. Lupus. 2016. doi:10.1177/0961203316635288.

    PubMed  Google Scholar 

  5. Pons-Estel GJ, Alarcon GS, Scofield L, Reinlib L, Cooper GS. Understanding the epidemiology and progression of systemic lupus erythematosus. Semin Arthritis Rheum. 2010;39(4):257–68.

    Article  PubMed  Google Scholar 

  6. Guy A, Tiosano S, Comaneshter D, Tekes-Manova D, Shovman O, Cohen AD et al. Aortic aneurysm association with SLE - a case-control study. Lupus. 2016. doi:10.1177/0961203316628999.

    PubMed  Google Scholar 

  7. Petri M. Epidemiology of systemic lupus erythematosus. Best Pract Res Clin Rheumatol. 2002;16(5):847–58.

    Article  PubMed  Google Scholar 

  8. Dienstag JL. Hepatitis B virus infection. N Engl J Med. 2008;359(14):1486–500.

    Article  CAS  PubMed  Google Scholar 

  9. Ganem D, Prince AM. Hepatitis B virus infection—natural history and clinical consequences. N Engl J Med. 2004;350(11):1118–29.

    Article  CAS  PubMed  Google Scholar 

  10. Merrill RM, Hunter BD. Seroprevalence of markers for hepatitis B viral infection. Int J Infect Dis. 2011;15(2):e78–121.

    Article  PubMed  Google Scholar 

  11. Yim HJ, Lok AS. Natural history of chronic hepatitis B virus infection: what we knew in 1981 and what we know in 2005. Hepatology. 2006;43(2 Suppl 1):S173–81.

    Article  CAS  PubMed  Google Scholar 

  12. Bar-Shany S, Green MS, Slepon R, Gilon E. Ethnic differences in the prevalence of hepatitis B surface antigen among Israeli blood donors: changes between 1972 and 1988. Int J Epidemiol. 1991;20(1):271–5.

    Article  CAS  PubMed  Google Scholar 

  13. Bogomolski-Yahalom V, Granot E, Linder N, Adler R, Korman S, Manny N, et al. Prevalence of HBsAg carriers in native and immigrant pregnant female populations in Israel and passive/active vaccination against HBV of newborns at risk. J Med Virol. 1991;34(4):217–22.

    Article  CAS  PubMed  Google Scholar 

  14. El-Serag HB. Hepatocellular carcinoma. N Engl J Med. 2011;365(12):1118–27.

    Article  CAS  PubMed  Google Scholar 

  15. Bonafede RP, van Staden M, Klemp P. Hepatitis B virus infection and liver function in patients with systemic lupus erythematosus. J Rheumatol. 1986;13(6):1050–2.

    CAS  PubMed  Google Scholar 

  16. Chen X, Hong L, Zhang W, Yuan M, Yang Q, Mao H, et al. Hepatitis B Virus infection rate and distribution in Chinese systemic lupus erythematosus patients. Med Sci Monit. 2015;21:1955–9.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Lai KN, Lai FM, Lo S, Leung A. Is there a pathogenetic role of hepatitis B virus in lupus nephritis? Arch Pathol Lab Med. 1987;111(2):185–8.

    CAS  PubMed  Google Scholar 

  18. Marinchev L, Antonov K, Peytcheva V, Kolarov Z. Outcome in a patient with systemic lupus erythematosus and concurrent chronic hepatitis B infection. BMJ Case Rep. 2010;2010. doi:10.1136/bcr.09.2009.2273.

    Article  Google Scholar 

  19. Shorey J, Cheatum DE, Combes B, Ziff M. Hepatitis B antigen and antibody in patients with systemic lupus erythematosus. Arthritis Rheum. 1974;17(5):583–9.

    Article  CAS  PubMed  Google Scholar 

  20. Wang Z, Li M, Zeng X, Liu X. Hepatitis B virus-associated antigen deposition in renal tissue from patients with systemic lupus erythematosus. J Rheumatol. 2012;39(5):974–8.

    Article  CAS  PubMed  Google Scholar 

  21. Zhao J, Qiu M, Li M, Lu C, Gu J. Low prevalence of hepatitis B virus infection in patients with systemic lupus erythematosus in southern China. Rheumatol Int. 2010;30(12):1565–70.

    Article  PubMed  Google Scholar 

  22. Bieber V, Cohen AD, Freud T, Agmon-Levin N, Gertel S, Amital H. Autoimmune smoke and fire—coexisting rheumatoid arthritis and chronic obstructive pulmonary disease: a cross-sectional analysis. Immunol Res. 2013;56(2–3):261–6.

    Article  PubMed  Google Scholar 

  23. Farhi A, Cohen AD, Shovman O, Comaneshter D, Amital H, Amital D. Bipolar disorder associated with rheumatoid arthritis: a case-control study. J Affect Disord. 2016;189:287–9.

    Article  PubMed  Google Scholar 

  24. Houri LE, Watad A, Whitby A, Tiosano S, Comaneshter D, Cohen AD, et al. Coexistence of ischemic heart disease and rheumatoid arthritis patients—a case control study. Autoimmun Rev. 2016;15(4):393–6.

    Article  Google Scholar 

  25. Saeki Y, Ishihara K. Infection-immunity liaison: pathogen-driven autoimmune-mimicry (PDAIM). Autoimmun Rev. 2014;13(10):1064–9.

    Article  PubMed  Google Scholar 

  26. Palazzi C, Buskila D, D’Angelo S, D’Amico E, Olivieri I. Autoantibodies in patients with chronic hepatitis C virus infection: pitfalls for the diagnosis of rheumatic diseases. Autoimmun Rev. 2012;11(9):659–63.

    Article  CAS  PubMed  Google Scholar 

  27. Marcos M, Alvarez F, Brito-Zeron P, Bove A, Perez-De-Lis M, Diaz-Lagares C, et al. Chronic hepatitis B virus infection in Sjogren’s syndrome. Prevalence and clinical significance in 603 patients. Autoimmun Rev. 2009;8(7):616–20.

    Article  PubMed  Google Scholar 

  28. Berkun Y, Zandman-Goddard G, Barzilai O, Boaz M, Sherer Y, Larida B, et al. Infectious antibodies in systemic lupus erythematosus patients. Lupus. 2009;18(13):1129–35.

    Article  CAS  PubMed  Google Scholar 

  29. Doaty S, Agrawal H, Bauer E, Furst DE. Infection and lupus: Which causes which? Curr Rheumatol Rep. 2016;18(3):13.

    Article  PubMed  Google Scholar 

  30. James WH. A potential explanation of the reported low prevalence of hepatitis B virus infection in patients with systemic lupus erythematosus. Rheumatol Int. 2012;32(3):835.

    Article  PubMed  Google Scholar 

  31. Vergani D, Mieli-Vergani G. Autoimmune manifestations in viral hepatitis. Semin Immunopathol. 2013;35(1):73–85.

    Article  CAS  PubMed  Google Scholar 

  32. Yamashita H, Shimizu A, Tsuchiya H, Takahashi Y, Kaneko H, Kano T, et al. Chronic active Epstein-Barr virus infection mimicking autoimmune hepatitis exacerbation in a patient with systemic lupus erythematosus. Lupus. 2014;23(8):833–6.

    Article  CAS  PubMed  Google Scholar 

  33. Zafrir Y, Agmon-Levin N, Paz Z, Shilton T, Shoenfeld Y. Autoimmunity following hepatitis B vaccine as part of the spectrum of ‘Autoimmune (Auto-inflammatory) Syndrome induced by Adjuvants’ (ASIA): analysis of 93 cases. Lupus. 2012;21(2):146–52.

    Article  CAS  PubMed  Google Scholar 

  34. Zandman-Goddard G, Berkun Y, Barzilai O, Boaz M, Blank M, Ram M, et al. Exposure to Epstein-Barr virus infection is associated with mild systemic lupus erythematosus disease. Ann NY Acad Sci. 2009;1173:658–63.

    Article  CAS  PubMed  Google Scholar 

  35. Doria A, Sarzi-Puttini P, Shoenfeld Y. Infections, rheumatism and autoimmunity: the conflicting relationship between humans and their environment. Autoimmun Rev. 2008;8(1):1–4.

    Article  PubMed  Google Scholar 

  36. Aytac MB, Kasapcopur O, Aslan M, Erener-Ercan T, Cullu-Cokugras F, Arisoy N. Hepatitis B vaccination in juvenile systemic lupus erythematosus. Clin Exp Rheumatol. 2011;29(5):882–6.

    PubMed  Google Scholar 

  37. Chng HH, Fock KM, Chew CN, Guan R, Feng PH, Boey ML, et al. Hepatitis B virus infection in patients with systemic lupus erythematosus. Singap Med J. 1993;34(4):325–6.

    CAS  Google Scholar 

  38. Ram M, Shoenfeld Y. Hepatitis B: infection, vaccination and autoimmunity. Isr Med Assoc J. 2008;10(1):61–4.

    PubMed  Google Scholar 

  39. Soylu S, Gul U, Gonul M, Kilic A, Cakmak SK, Demiriz M. An uncommon presentation of the co-existence of morphea and vitiligo in a patient with chronic hepatitis B virus infection: Is there a possible association with autoimmunity? Am J Clin Dermatol. 2009;10(5):336–8.

    Article  PubMed  Google Scholar 

  40. Watanabe R, Ishii T, Nakamura K, Shirai T, Tajima Y, Fujii H, et al. Prevalence and time course of hepatitis B virus infection in patients with systemic lupus erythematosus under immunosuppressive therapy. Mod Rheumatol. 2013;23(6):1094–100.

    Article  CAS  PubMed  Google Scholar 

  41. Looi LM, Prathap K. Hepatitis B virus surface antigen in glomerular immune complex deposits of patients with systemic lupus erythematosus. Histopathology. 1982;6(2):141–7.

    Article  CAS  PubMed  Google Scholar 

  42. Ram M, Anaya JM, Barzilai O, Izhaky D, Katz BSP, Blank M, et al. The putative protective role of hepatitis B virus (HBV) infection from autoimmune disorders. Autoimmun Rev. 2008;7(8):621–5.

    Article  CAS  PubMed  Google Scholar 

  43. Lu CL, Tsai ST, Chan CY, Hwang SJ, Tsai CY, Wu JC, et al. Hepatitis B infection and changes in interferon-alpha and -gamma production in patients with systemic lupus erythematosus in Taiwan. J Gastroenterol Hepatol. 1997;12(4):272–6.

    Article  CAS  PubMed  Google Scholar 

  44. Mercado U, Avendano-Reyes M, Araiza-Casillas R, Diaz-Molina R. Prevalance of antibodies against hepatitis C and B viruses in patients with systemic lupus erythematosus. Rev Gastroenterol Mex. 2005;70(4):399–401.

    PubMed  Google Scholar 

  45. Abu-Shakra M, El-Sana S, Margalith M, Sikuler E, Neumann L, Buskila D. Hepatitis B and C viruses serology in patients with SLE. Lupus. 1997;6(6):543–4.

    Article  CAS  PubMed  Google Scholar 

  46. Alarcon-Segovia D, Fishbein E, Diaz-Jouanen E. Presence of hepatitis-associated antigen in systemic lupus erythematosus. Clin Exp Immunol. 1972;12(1):9–19.

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Permin H, Aldershvile J, Nielsen JO. Hepatitis B virus infection in patients with rheumatic diseases. Ann Rheum Dis. 1982;41(5):479–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Takahashi T, de la Garza L, Ponce-de-Leon S, Palacios-Macedo A, Contreras JL, Sanchez-Guerrero J, et al. Risk factors for operative morbidity in patients with systemic lupus erythematosus: an analysis of 63 surgical procedures. Am Surg. 1995;61(3):260–4.

    CAS  PubMed  Google Scholar 

  49. Pagliaccetti NE, Robek MD. Interferon-lambda in the immune response to hepatitis B virus and hepatitis C virus. J Interferon Cytokine Res. 2010;30(8):585–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Meyer O. Interferon-alpha as a treatment target in systemic lupus erythematosus. Jt Bone Spine. 2012;79(2):113–6.

    Article  Google Scholar 

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Authors and Affiliations

  1. Department of Medicine ‘B’, Zabludowicz Center for Autoimmune Diseases, Sheba Medical Center, 5262100, Tel-Hashomer, Israel

    Omer Gendelman, Naim Mahroum & Howard Amital

  2. Sackler Faculty of Medicine, Tel-Aviv University, Tel Aviv-Yafo, Israel

    Omer Gendelman, Naim Mahroum & Howard Amital

  3. Siaal Research Center for Family Medicine and Primary Care, Faculty of Health Sciences, Ben Gurion University of the Negev, Beer Sheva, Israel

    Doron Comaneshter & Arnon D. Cohen

  4. Metabolic Bone Disease Service, Meir Medical Center, Kfar-Saba, Israel

    Pnina Rotman-Pikielny

  5. Chief Physician’s Office, Clalit Health Services, Tel Aviv, Israel

    Arnon D. Cohen

  6. Central Management, Clalit Health Services, Tel Aviv, Israel

    Michael Sherf

  7. Department of Public Health, Faculty of Health Sciences, Ben-Gurion University of Negev, Beer Sheva, Israel

    Michael Sherf

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  1. Omer Gendelman
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  2. Naim Mahroum
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  6. Howard Amital
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  7. Michael Sherf
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Correspondence to Howard Amital.

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Gendelman, O., Mahroum, N., Comaneshter, D. et al. Hepatitis B carrier state among SLE patients: case–control study. Immunol Res 65, 257–261 (2017). https://doi.org/10.1007/s12026-016-8834-6

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  • DOI: https://doi.org/10.1007/s12026-016-8834-6

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