Skip to main content

Advertisement

SpringerLink
Log in

Detection of HBV genome in the plasma and peripheral blood mononuclear cells of Iranian HBsAg negative patients with HIV infection: occult HBV infection

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

The presence of hepatitis B virus (HBV) DNA in the absence of traceable hepatitis B surface antigen (HBsAg) in the plasma specimen of patients is defined as occult HBV infection (OBI). This study aimed to detect HBV-DNA in the plasma and peripheral blood mononuclear cells (PBMCs) of Iranian HBsAg negative patients with human immunodeficiency virus (HIV) infection. This cross-sectional study was conducted on 172 patients with HIV infection from September 2015 to August 2017. The patients were tested for serological parameters (HBsAg, HBcAb, HBeAg and HBeAb) against HBV infection. Moreover, they were tested for HBV viral load (using COBAS TaqMan 48 Kit, Roche, USA) in plasma and the presence of the HBV genome in PBMC specimens using real-time PCR. The mean age of the patients was 35.4 ± 13.4 years. Of the 172 studied patients, 109 (63.4%) were male. In this study, 151 (87.8%) patients were negative for HBsAg, 111 (64.5%) patients were negative for all HBV infection serological markers, 9 (5.2%) patients were only positive for HBsAg and 29 (16.9%) patients were only positive for HBcAb. Moreover, five (3.3%) patients with HBsAg negative had OBI (in the plasma sample of four patients and PBMC specimens of all five patients, HBV-DNA was detected). The present study revealed that 3.3% of the patients with HIV infection had occult HBV infection. Presumably, designing prospective studies to identify this infection in patients with HIV infection is informative and valuable.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Chen GF, Wang C, Lau G (2017) Treatment of chronic hepatitis B infection-2017. Liver Int 37(S1):59–66

    Article  PubMed  CAS  Google Scholar 

  2. Amitis R, Mohammad B, Ali E, Masoomeh S, Arezoo A (2012) Occult hepatitis B infection in different high risk patients. Hepat Mon 2012:467–468

    Google Scholar 

  3. Chemin I, Trepo C (2005) Clinical impact of occult HBV infections. J Clin Virol 34:S15–S21

    Article  PubMed  Google Scholar 

  4. Raimondo G, Allain J-P, Brunetto MR, Buendia M-A, Chen D-S, Colombo M et al (2008) Statements from the Taormina expert meeting on occult hepatitis B virus infection. J Hepatol 49(4):652–657

    Article  PubMed  Google Scholar 

  5. Hu KQ (2002) Occult hepatitis B virus infection and its clinical implications. J Viral Hepat 9(4):243–257

    Article  PubMed  Google Scholar 

  6. Sood A, Pangotra C, Manrai M (2016) Prevalence of occult hepatitis B infection in patients visiting tertiary care hospital. Medi J Armed Forces India. 72(2):140–144

    Article  CAS  Google Scholar 

  7. Bokharaei-Salim F, Keyvani H, Monavari SH, Esghaei M, Fakhim S, Ataei Pirkooh A et al (2014) Distribution of hepatitis B virus genotypes in azerbaijani patients with chronic hepatitis B infection. Hepat Mon 14(12):e25105

    Article  PubMed  PubMed Central  Google Scholar 

  8. Gupta S, Singh S (2010) Occult hepatitis B virus infection in ART-naive HIV-infected patients seen at a tertiary care centre in north India. BMC Infect Dis 10(1):53

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. hio CL, editor Hepatitis B in the human immunodeficiency virus-infected patient: epidemiology, natural history, and treatment. In: Seminars in liver disease; 2003: Copyright© 2002 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA. Tel.:+ 1 (212) 584-4662.

  10. Diop-Ndiaye H, Touré-Kane C, Etard J-F, Lo G, Diaw P, Ngom-Gueye N et al (2008) Hepatitis B, C seroprevalence and delta viruses in HIV-1 Senegalese patients at HAART initiation (retrospective study). J Med Virol 80(8):1332–1336

    Article  PubMed  CAS  Google Scholar 

  11. Peters MG (2007) Diagnosis and management of hepatitis B virus and HIV coinfection. Topics HIV Med Publ Int AIDS Soc USA 15(5):163

    Google Scholar 

  12. Hofer M, Joller-Jemelka H, Grob P, Lüthy R, Opravil M (1998) Frequent chronic hepatitis B virus infection in HIV-infected patients positive for antibody to hepatitis B core antigen only. Eur J Clin Microbiol Infect Dis 17(1):6–13

    Article  PubMed  CAS  Google Scholar 

  13. Piroth L, Binquet C, Vergne M, Minello A, Livry C, Bour J-B et al (2002) The evolution of hepatitis B virus serological patterns and the clinical relevance of isolated antibodies to hepatitis B core antigen in HIV infected patients. J Hepatol 36(5):681–686

    Article  PubMed  CAS  Google Scholar 

  14. Bloquel B, Jeulin H, Burty C, Letranchant L, Rabaud C, Venard V (2010) Occult hepatitis B infection in patients infected with HIV: report of two cases of hepatitis B reactivation and prevalence in a hospital cohort. J Med Virol 82(2):206–212

    Article  PubMed  CAS  Google Scholar 

  15. Vallet-Pichard A, Pol S (2006) Natural history and predictors of severity of chronic hepatitis C virus (HCV) and human immunodeficiency virus (HIV) co-infection. J Hepatol 44:S28–S34

    Article  PubMed  Google Scholar 

  16. Tramuto F, Maida CM, Colomba GM, Di Carlo P, Mazzola G, Vecchi VL et al (2013) Occult hepatitis B infection in the immigrant population of sicily, Italy. J Immigr Minor Health 15(4):725–731

    Article  PubMed  Google Scholar 

  17. Yousif M, Mudawi H, Hussein W, Mukhtar M, Nemeri O, Glebe D et al (2014) Genotyping and virological characteristics of hepatitis B virus in HIV-infected individuals in Sudan. Int J Infect Dis 29:125–132

    Article  PubMed  Google Scholar 

  18. Allain J-P (2017) Global epidemiology of occult HBV infection. Ann Blood. 2(7):1–13

    Google Scholar 

  19. Kremsdorf D, Soussan P, Paterlini-Brechot P, Brechot C (2006) Hepatitis B virus-related hepatocellular carcinoma: paradigms for viral-related human carcinogenesis. Oncogene. 25(27):3823–3833

    Article  PubMed  CAS  Google Scholar 

  20. Tramuto F, Maida CM, Colomba GM, Di Carlo P, Mazzola G, Vecchi VL et al (2013) Occult hepatitis B infection in the immigrant population of sicily, Italy. J Immigr Minority Health. 15(4):725–731

    Article  Google Scholar 

  21. Tajik Z, Keyvani H, Bokharaei-Salim F, Zolfaghari MR, Fakhim S, Keshvari M et al (2015) Detection of Hepatitis B virus covalently closed circular DNA in the plasma of Iranian HBeAg-negative patients with chronic hepatitis B. Hepat Mon. 15(9):e30790

    Article  PubMed  PubMed Central  Google Scholar 

  22. Garson JA, Grant PR, Ayliffe U, Ferns RB, Tedder RS (2005) Real-time PCR quantitation of hepatitis B virus DNA using automated sample preparation and murine cytomegalovirus internal control. J Virol Methods. 126(1–2):207–213

    Article  PubMed  CAS  Google Scholar 

  23. Keyvani H, Taghinezhad Saroukalaei S, Mohseni AH (2016) Assessment of the human cytomegalovirus UL97 gene for identification of resistance to ganciclovir in iranian immunosuppressed patients. Jundishapur J Microbiol 9(5):e31733

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Zuckerman AJ (2000) Effect of hepatitis B virus mutants on efficacy of vaccination. Lancet. 355(9213):1382–1384

    Article  PubMed  CAS  Google Scholar 

  25. Pollicino T, Squadrito G, Cerenzia G, Cacciola I, Raffa G, Craxi A et al (2004) Hepatitis B virus maintains its pro-oncogenic properties in the case of occult HBV infection. Gastroenterology. 126(1):102–110

    Article  PubMed  CAS  Google Scholar 

  26. Twu SJ, Detels R, Nelson K, Visscher BR, Kaslow R, Palenicek J et al (1993) Relationship of hepatitis B virus infection to human immunodeficiency virus type 1 infection. J Infect Dis 167(2):299–304

    Article  PubMed  CAS  Google Scholar 

  27. Treitinger A, Spada C, Silva EL, Miranda A, Oliveira OV, Silveira M et al (1999) Prevalence of serologic markers of HBV and HCV infection in HIV-1 seropositive patients in Florianópolis, Brazil. Braz J Infect Dis. 3(1):1–5

    PubMed  CAS  Google Scholar 

  28. Souza MGd, Passos ADC, Machado AA, Figueiredo JFDC, Esmeraldino LE (2004) HIV and hepatitis B virus co-infection: prevalence and risk factors. Revista da Sociedade Brasileira de Medicina Tropical. 37(5):391–395

    Article  PubMed  Google Scholar 

  29. Araujo NM, Branco-Vieira M, Silva A, Pilotto JH, Grinsztejn B, De Almeida AJ et al (2008) Occult hepatitis B virus infection in HIV-infected patients: evaluation of biochemical, virological and molecular parameters. Hepatol Res. 38(12):1194–1203

    PubMed  CAS  Google Scholar 

  30. Monteiro MRDCC, Nascimento MMPD, Passos ADC, Figueiredo JFDC (2004) Soroepidemiological survey of hepatitis B virus among HIV/AIDS patients in Belém, Pará-Brasil. Revista da Sociedade Brasileira de Medicina Tropical. 37:27–32

    Article  PubMed  Google Scholar 

  31. de Almeida Pereira RAR, Mussi ADH, e Silva VCDA, Souto FJD (2006) Hepatitis B Virus infection in HIV-positive population in Brazil: results of a survey in the state of Mato Grosso and a comparative analysis with other regions of Brazil. BMC Infect Dis 6(1):34

    Article  PubMed  PubMed Central  Google Scholar 

  32. Koblin BA, Taylor PE, Rubinstein P, Stevens CE (1992) Effect of duration of hepatitis B virus infection on the association between human immunodeficiency virus type-1 and hepatitis B viral replication. Hepatology. 15(4):590–592

    Article  PubMed  CAS  Google Scholar 

  33. Colin JF, Cazals-Hatem D, Loriot MA, Martinot-Peignoux M, Pham BN, Auperin A et al (1999) Influence of human immunodeficiency virus infection on chronic hepatitis B in homosexual men. Hepatology. 29(4):1306–1310

    Article  PubMed  CAS  Google Scholar 

  34. Sadeghi A, Shirvani-Dastgerdi E, Tacke F, Yagmur E, Poortahmasebi V, Poorebrahim M et al (2017) HBsAg mutations related to occult hepatitis B virus infection in HIV-positive patients result in a reduced secretion and conformational changes of HBsAg. J Med Virol 89(2):246–256

    Article  PubMed  CAS  Google Scholar 

  35. Jahanbakhsh A, Farzinepoor Z, Mansouri F, Vaziri S, Afsharian M (2017) Prevalence of Occult Hepatitis B in HIV Positive Patients (Adolescents and Adults) in Kermanshah-Iran. Int J Pediatrics. 5(9):5797–5803

    Google Scholar 

  36. Aghakhani A, Mohraz M, Aghasadeghi MR, Banifazl M, Vahabpour R, Karami A et al (2016) Occult hepatitis B virus infection and S gene escape mutants in HIV-infected patients after hepatitis B virus vaccination. Int J STD AIDS. 27(11):967–972

    Article  PubMed  CAS  Google Scholar 

  37. Honarmand A, Pourahmad M, Solhjoo K, Kohan M, Davami MH, Mostafavi Zadeh SK (2014) Occult hepatitis B demonstrated by anti-HBc and HBV DNA in HIV-positive patients. Reports Biochem Mol Biol 3(1):38–42

    Google Scholar 

  38. Ramezani A, Banifazl M, Eslamifar A, Aghakhani A (2010) Serological pattern of anti-HBc alone infers occult hepatitis B virus infection in high-risk individuals in Iran. J Infect Dev Ctries. 4(10):658–661

    PubMed  Google Scholar 

  39. Azadmanesh K, Mohraz M, Aghakhani A, Edalat R, Jam S, Eslamifar A et al (2008) Occult hepatitis B virus infection in HIV-infected patients with isolated hepatitis B core antibody. Intervirology. 51(4):270–274

    Article  PubMed  CAS  Google Scholar 

  40. Schaefer S (2007) Hepatitis B virus taxonomy and hepatitis B virus genotypes. World J Gastroenterol 13(1):14–21

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Köck J, Theilmann L, Galle P, Schlicht H (1996) Hepatitis B virus nucleic acids associated with human peripheral blood mononuclear cells do not originate from replicating virus. Hepatology. 23(3):405–413

    PubMed  Google Scholar 

  42. Cassini R, De Mitri M, Gibellini D, Urbinati L, Bagaglio S, Morsica G et al (2013) A novel stop codon mutation within the hepatitis B surface gene is detected in the liver but not in the peripheral blood mononuclear cells of HIV-infected individuals with occult HBV infection. J Viral Hepat 20(1):42–49

    Article  PubMed  CAS  Google Scholar 

  43. Nebbia G, Garcia-Diaz A, Ayliffe U, Smith C, Dervisevic S, Johnson M et al (2007) Predictors and kinetics of occult hepatitis B virus infection in HIV-infected persons. J Med Virol 79(10):1464–1471

    Article  PubMed  CAS  Google Scholar 

  44. Filippini P, Coppola N, Pisapia R, Scolastico C, Marrocco C, Zaccariello A et al (2006) Impact of occult hepatitis B virus infection in HIV patients naive for antiretroviral therapy. Aids. 20(9):1253–1260

    Article  PubMed  Google Scholar 

  45. Shire NJ, Rouster SD, Rajicic N, Sherman KE (2004) Occult hepatitis B in HIV-infected patients. JAIDS J Acquir Immune Defic Syndr 36(3):869–875

    Article  PubMed  Google Scholar 

  46. Fabbri G, Mastrorosa I, Vergori A, Mazzotta V, Pinnetti C, Grisetti S et al (2017) Reactivation of occult HBV infection in an HIV/HCV Co-infected patient successfully treated with sofosbuvir/ledipasvir: a case report and review of the literature. BMC Infect Dis. 17(1):182

    Article  PubMed  PubMed Central  Google Scholar 

  47. Opaleye OO, Oluremi AS, Atiba AB, Adewumi MO, Mabayoje OV, Donbraye E et al (2014) Occult Hepatitis B Virus infection among HIV positive patients in Nigeria. J Trop Med. 2014:796121

    Article  PubMed  PubMed Central  Google Scholar 

  48. Panigrahi R, Majumder S, Gooptu M, Biswas A, Datta S, Chandra PK et al (2012) Occult HBV infection among anti-HBc positive HIV-infected patients in apex referral centre, Eastern India. Ann Hepatol 11(6):870–875

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors of the present research would like to thank all the candidates who enrolled in this study.

Funding

The current study was financially supported by Research Deputy of Iran University of Medical Sciences (grant number: 27008).

Author information

Authors and Affiliations

  1. HIV Laboratory of National Center, Iran University of Medical Sciences, Tehran, Iran

    Zahra Tajik, Farah Bokharaei-Salim, Saba Garshasbi & Tahereh Donyavi

  2. Department of Virology, School of Medicine, Iran University of Medical Sciences, Tehran, Iran

    Farah Bokharaei-Salim, Saied Ghorbani, Hossein Keyvani, Maryam Esghaei, Seyed Hamidreza Monavari & Angila Ataei-Pirkooh

  3. Department of Architectural Engineering, Faculty of Engineering, Islamic Azad University, South Tehran Branch, Tehran, Iran

    Atousa Fakhim

Authors
  1. Zahra Tajik
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Farah Bokharaei-Salim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Saied Ghorbani
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hossein Keyvani
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Maryam Esghaei
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Seyed Hamidreza Monavari
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Angila Ataei-Pirkooh
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Saba Garshasbi
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Tahereh Donyavi
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Atousa Fakhim
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Farah Bokharaei-Salim.

Ethics declarations

Conflicts of interest

The authors of the current research declare no conflict(s) of interest.

Ethical considerations

Ethical approval for the current study was received from the local ethics committee of the Iran University of Medical Sciences (IUMS), Tehran, Iran. All of the participants were informed about the present research, with a written consent form obtained from them prior to their enrollment. All the experiments were done in the HIV Laboratory of National Centre, Vice Chancellor for Health, IUMS, Tehran, Iran.

Additional information

Handling Editor: Li Wu.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tajik, Z., Bokharaei-Salim, F., Ghorbani, S. et al. Detection of HBV genome in the plasma and peripheral blood mononuclear cells of Iranian HBsAg negative patients with HIV infection: occult HBV infection. Arch Virol 163, 1559–1566 (2018). https://doi.org/10.1007/s00705-018-3740-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-018-3740-y

Search

Navigation