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Erschienen in: Immunologic Research 1/2017

16.07.2016 | Therapeutic Aspects in Autoimmunity

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

verfasst von: Omer Gendelman, Naim Mahroum, Doron Comaneshter, Pnina Rotman-Pikielny, Arnon D. Cohen, Howard Amital, Michael Sherf

Erschienen in: Immunologic Research | Ausgabe 1/2017

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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.
Literatur
1.
Zurück zum Zitat Borchers AT, Naguwa SM, Shoenfeld Y, Gershwin ME. The geoepidemiology of systemic lupus erythematosus. Autoimmun Rev. 2010;9(5):A277–87.CrossRefPubMed Borchers AT, Naguwa SM, Shoenfeld Y, Gershwin ME. The geoepidemiology of systemic lupus erythematosus. Autoimmun Rev. 2010;9(5):A277–87.CrossRefPubMed
2.
Zurück zum Zitat Borchers AT, Leibushor N, Naguwa SM, Cheema GS, Shoenfeld Y, Gershwin ME. Lupus nephritis: a critical review. Autoimmun Rev. 2012;12(2):174–94.CrossRefPubMed Borchers AT, Leibushor N, Naguwa SM, Cheema GS, Shoenfeld Y, Gershwin ME. Lupus nephritis: a critical review. Autoimmun Rev. 2012;12(2):174–94.CrossRefPubMed
3.
Zurück zum Zitat Danchenko N, Satia JA, Anthony MS. Epidemiology of systemic lupus erythematosus: a comparison of worldwide disease burden. Lupus. 2006;15(5):308–18.CrossRefPubMed Danchenko N, Satia JA, Anthony MS. Epidemiology of systemic lupus erythematosus: a comparison of worldwide disease burden. Lupus. 2006;15(5):308–18.CrossRefPubMed
5.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
7.
Zurück zum Zitat Petri M. Epidemiology of systemic lupus erythematosus. Best Pract Res Clin Rheumatol. 2002;16(5):847–58.CrossRefPubMed Petri M. Epidemiology of systemic lupus erythematosus. Best Pract Res Clin Rheumatol. 2002;16(5):847–58.CrossRefPubMed
9.
Zurück zum Zitat Ganem D, Prince AM. Hepatitis B virus infection—natural history and clinical consequences. N Engl J Med. 2004;350(11):1118–29.CrossRefPubMed Ganem D, Prince AM. Hepatitis B virus infection—natural history and clinical consequences. N Engl J Med. 2004;350(11):1118–29.CrossRefPubMed
10.
Zurück zum Zitat Merrill RM, Hunter BD. Seroprevalence of markers for hepatitis B viral infection. Int J Infect Dis. 2011;15(2):e78–121.CrossRefPubMed Merrill RM, Hunter BD. Seroprevalence of markers for hepatitis B viral infection. Int J Infect Dis. 2011;15(2):e78–121.CrossRefPubMed
11.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
12.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
13.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
15.
Zurück zum Zitat 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.PubMed 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.PubMed
16.
Zurück zum Zitat 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
17.
Zurück zum Zitat 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.PubMed 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.PubMed
19.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
20.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
21.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
22.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
23.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
24.
Zurück zum Zitat 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.CrossRef 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.CrossRef
25.
Zurück zum Zitat Saeki Y, Ishihara K. Infection-immunity liaison: pathogen-driven autoimmune-mimicry (PDAIM). Autoimmun Rev. 2014;13(10):1064–9.CrossRefPubMed Saeki Y, Ishihara K. Infection-immunity liaison: pathogen-driven autoimmune-mimicry (PDAIM). Autoimmun Rev. 2014;13(10):1064–9.CrossRefPubMed
26.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
27.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
28.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
29.
Zurück zum Zitat Doaty S, Agrawal H, Bauer E, Furst DE. Infection and lupus: Which causes which? Curr Rheumatol Rep. 2016;18(3):13.CrossRefPubMed Doaty S, Agrawal H, Bauer E, Furst DE. Infection and lupus: Which causes which? Curr Rheumatol Rep. 2016;18(3):13.CrossRefPubMed
30.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
31.
Zurück zum Zitat Vergani D, Mieli-Vergani G. Autoimmune manifestations in viral hepatitis. Semin Immunopathol. 2013;35(1):73–85.CrossRefPubMed Vergani D, Mieli-Vergani G. Autoimmune manifestations in viral hepatitis. Semin Immunopathol. 2013;35(1):73–85.CrossRefPubMed
32.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
33.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
34.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
35.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
36.
Zurück zum Zitat 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 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
37.
Zurück zum Zitat 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. 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.
38.
Zurück zum Zitat Ram M, Shoenfeld Y. Hepatitis B: infection, vaccination and autoimmunity. Isr Med Assoc J. 2008;10(1):61–4.PubMed Ram M, Shoenfeld Y. Hepatitis B: infection, vaccination and autoimmunity. Isr Med Assoc J. 2008;10(1):61–4.PubMed
39.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
40.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
41.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
42.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
43.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
44.
Zurück zum Zitat 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 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
45.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
46.
Zurück zum Zitat 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.PubMedPubMedCentral 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.PubMedPubMedCentral
47.
48.
Zurück zum Zitat 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.PubMed 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.PubMed
49.
Zurück zum Zitat 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
50.
Zurück zum Zitat Meyer O. Interferon-alpha as a treatment target in systemic lupus erythematosus. Jt Bone Spine. 2012;79(2):113–6.CrossRef Meyer O. Interferon-alpha as a treatment target in systemic lupus erythematosus. Jt Bone Spine. 2012;79(2):113–6.CrossRef
Metadaten
Titel
Hepatitis B carrier state among SLE patients: case–control study
verfasst von
Omer Gendelman
Naim Mahroum
Doron Comaneshter
Pnina Rotman-Pikielny
Arnon D. Cohen
Howard Amital
Michael Sherf
Publikationsdatum
16.07.2016
Verlag
Springer US
Erschienen in
Immunologic Research / Ausgabe 1/2017
Print ISSN: 0257-277X
Elektronische ISSN: 1559-0755
DOI
https://doi.org/10.1007/s12026-016-8834-6

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