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GBV-C/HIV-1 coinfection is associated with low HIV-1 viral load and high CD4+ T lymphocyte count

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Abstract

GB virus C (GBV-C) is a lymphotropic virus with a low level or non-existent replication in the liver. The interaction between HIV-1 and GBV-C apparently reduces the progression of HIV-1 infection to AIDS and improves the quality of life of HIV-1 infected individuals. A cross-sectional study was established to determine the possible effect of HIV-1/GBV-C coinfection on HIV-1 viral load and CD4+ T lymphocyte counts. Samples from 313 HIV-1 infected persons from the Virus Laboratory of the Federal University of Pará as well as demographic and clinical information were obtained from medical records. This study used a nested PCR method to determine GBV-C viremia. The prevalence of HIV-1/GBV-C coinfection was 17%. There were no significant differences in the distribution according to age, sex or ethnicity between the groups. The differences in HIV-1 viral load and CD4+ T lymphocyte count between the HIV-1 and HIV-1/GBV-C groups were highly significant, indicating that coinfection results in lower viral loads and higher CD4+ T lymphocyte counts compared to HIV-1 mono-infection. The results indicate a protective effect among coinfected individuals.

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References

  1. Simons JN, Pilot-Matias TJ, Leary TP, Dawson GJ, Desai SM, Schlauder GG et al (1995) Identification of two flavivirus-like genomes in the GB hepatitis agent. Proc Natl Acad Sci USA 92:3401–3405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Linnen J, Wages J, Zhang-Keck ZY, Fry KE, Krawczynski KZ, Alter H et al (1996) Molecular cloning and disease association of Hepatitis G virus: a transfusion-transmissible agent. Science 271:505–508

    Article  CAS  PubMed  Google Scholar 

  3. Alter HJ (1996) The cloning and clinical implications of HGV and HGBV-C. N Engl J Med 334:1536–1537

    Article  CAS  PubMed  Google Scholar 

  4. Tucker TJ, Smuts HE (2001) Review of the epidemiology, molecular characterization and tropism of the hepatitis G virus/GBV-C. Clin Lab 47:239–248

    CAS  PubMed  Google Scholar 

  5. AbuOdeh RO, Al-Absi E, Ali NH, Khalili M, Al-Mawlawi N, Hadwan TA et al (2015) Detection and phylogenetic analysis of human pegivirus (GBV-C) among blood donors and patients infected with Hepatitis B virus (HBV) in Qatar. J Med Virol 87:2074–2081

    Article  PubMed  Google Scholar 

  6. Odeh RA, Yasin S, Nasrallah G, Babi Y (2010) Rates of infection and phylogenetic analysis of GB virus-C among Kuwaiti and Jordanian blood donors. Intervirology 53:402–407

    Article  PubMed  Google Scholar 

  7. Supapol WB, Remis RS, Raboud J, Millson M, Tappero J, Kaul R et al (2011) Prevalence and correlates of GB virus C infection in HIV-infected and HIV-uninfected pregnant women in Bangkok, Thailand. J Med Virol 83:33–44

    Article  Google Scholar 

  8. Liu Z, Li L, Chen Z, Xu M, Zhang T, Jiao Y et al (2012) Prevalence of GB virus type C viraemia in MSM with or without HIV-1 infection in Beijing, China. Epidemiol Infect 140:2199–2209

    Article  CAS  PubMed  Google Scholar 

  9. Rodriguez AK, Garzaro DJ, Loureiro CL, Gutierrez CR, Ameli G, Jaspe RC et al (2014) HIV-1 and GBV-C co-infection in Venezuela. J Infect Dev Ctries 8:863–868

    Article  PubMed  Google Scholar 

  10. Alcalde R, Nishiya A, Casseb J, Inocencio L, Fonseca LA, Duarte AJ (2010) Prevalence and distribution of the GBV-C/HGV among HIV-1-infected patients under anti-retroviral therapy. Virus Res 151:148–152

    Article  CAS  PubMed  Google Scholar 

  11. Keys JR, Leone PA, Eron JJ, Alexander K, Brinson M, Swanstrom R (2014) Large scale screening of human sera for HCV RNA and GBV-C RNA. J Med Virol 86:473–477

    Article  PubMed  Google Scholar 

  12. Blackard JT, Ma G, Welge JA, King CC, Taylor LE, Mayer KH et al (2014) GB virus C (GBV-C) infection in Hepatitis C virus (HCV) seropositive women with or at risk for HIV infection. PLoS One 9:e114467

    Article  PubMed  PubMed Central  Google Scholar 

  13. Claret G, Noguera A, Gonzalez-Cuevas A, Garcia-Garcia JJ, Fortuny C, Munoz-Almagro C (2008) The prevalence of GB virus C/Hepatitis G virus RNA among healthy and HCV-infected Catalan children. Eur J Pediatr 167:991–994

    Article  CAS  PubMed  Google Scholar 

  14. Tenckhoff S, Kaiser T, Bredeek F, Donfield S, Menius E, Lail A et al (2012) Role of GB virus C in human immunodeficiency virus type-1- and Hepatitis C virus-infected hemophiliac children and adolescents. J Acquir Immune Defic Syndr 61:243–248

    Article  PubMed  Google Scholar 

  15. Muerhoff AS, Dawson GJ, Desai SM (2006) A previously unrecognized sixth genotype of GB virus C revealed by analysis of 5′-untranslated region sequences. J Med Virol 78:105–111

    Article  CAS  PubMed  Google Scholar 

  16. Smith DB, Cuceanu N, Davidson F, Jarvis LM, Mokili JL, Hamid S et al (1997) Discrimination of Hepatitis G virus/GBV-C geographical variants by analysis of the 5′ non-coding region. J Gen Virol 78:1533–1542

    Article  CAS  PubMed  Google Scholar 

  17. Muerhoff AS, Leary TP, Sathar MA, Dawson GJ, Desai SM (2005) African origin of GB virus C determined by phylogenetic analysis of a complete genotype 5 genome from South Africa. J Gen Virol 86:1729–1735

    Article  CAS  PubMed  Google Scholar 

  18. Souza IE, Zhang W, Diaz RS, Chaloner K, Klinzman D, Stapleton JT (2006) Effect of GB virus C on response to antiretroviral therapy in HIV-infected Brazilians. HIV Med 7:25–31

    Article  CAS  PubMed  Google Scholar 

  19. Tillmann HL, Heiken H, Knapik-Botor A, Heringlake S, Ockenga J, Wilber JC et al (2001) Infection with GB virus C and reduced mortality among HIV-infected patients. N Engl J Med 345:715–724

    Article  CAS  PubMed  Google Scholar 

  20. Williams CF, Klinzman D, Yamashita TE, Xiang J, Polgreen PM, Rinaldo C et al (2004) Persistent GB virus C infection and survival in HIV-infected men. N Engl J Med 350:981–990

    Article  CAS  PubMed  Google Scholar 

  21. Zhang W, Chaloner K, Tillmann HL, Williams CF, Stapleton JT (2006) Effect of early and late GB virus C viraemia on survival of HIV-infected individuals: a meta-analysis. HIV Med 7:173–180

    Article  CAS  PubMed  Google Scholar 

  22. Hattori J, Okumura N, Yamazaki Y, Uchiyama M, Hamaguchi M, Nishiyama Y et al (2007) Beneficial effect of GB virus C co-infection in Human Immunodeficiency Virus type 1-infected individuals. Microbiol Immunol 51:193–200

    Article  CAS  PubMed  Google Scholar 

  23. Lefrère JJ, Ferec C, Roudot-Thoraval F, Loiseau P, Cantaloube J, Biagini P et al (1999) GBV-C/Hepatitis G virus (HGV) RNA load in immunodeficient individuals and in immunocompetent individuals. J Med Virol 59:32–37

    Article  PubMed  Google Scholar 

  24. Xiang J, Wunschmann S, Diekema DJ, Klinzman D, Patrick KD, George SL et al (2001) Effect of coinfection with GB virus C on survival among patients with HIV infection. N Engl J Med 345:707–714

    Article  CAS  PubMed  Google Scholar 

  25. Yeo AE, Matsumoto A, Hisada M, Shih JW, Alter HJ, Goedert JJ (2000) Effect of Hepatitis G virus infection on progression of HIV infection in patients with hemophilia. Multicenter Hemophilia Cohort Study. Ann Intern Med 132:959–963

    Article  CAS  PubMed  Google Scholar 

  26. Xiang J, George SL, Wunschmann S, Chang Q, Klinzman D, Stapleton JT (2004) Inhibition of HIV-1 replication by GB virus C infection through increases in RANTES, MIP-1alpha, MIP-1beta, and SDF-1. Lancet 363:2040–2046

    Article  CAS  PubMed  Google Scholar 

  27. Jung S, Knauer O, Donhauser N, Eichenmuller M, Helm M, Fleckenstein B et al (2005) Inhibition of HIV strains by GB virus C in cell culture can be mediated by CD4 and CD8 T-lymphocyte derived soluble factors. AIDS 19:1267–1272

    Article  CAS  PubMed  Google Scholar 

  28. Nunnari G, Nigro L, Palermo F, Attanasio M, Berger A, Doerr HW et al (2003) Slower progression of HIV-1 infection in persons with GB virus C co-infection correlates with an intact T-helper 1 cytokine profile. Ann Intern Med 139:26–30

    Article  PubMed  Google Scholar 

  29. Siegal F (2003) Interferon-producing plasmacytoid dendritic cells and the pathogenesis of AIDS. Res Initiat Treat Action 8:10–13

    PubMed  Google Scholar 

  30. Capobianchi M, Lalle E, Martini F, Poccia F, D’Offizi G, Antonucci G et al (2006) Influence of GBV-C infection on the endogenous activation of the IFN system in HIV-1 co-infected patients. Cell Mol Biol 52:3–8

    CAS  PubMed  Google Scholar 

  31. Brasil. Ministério da Saúde (2015) Departamento de Vigilância, Prevenção e Controle das IST, do HIV/Aids e das Hepatites Virais, 2015. Protocolo Clínico e Diretrizes Terapêuticas para Manejo da Infecção pelo HIV em Adultos. http://www.aids.gov.br/sites/default/files/anexos/publicacao/2013/55308/protocolofinal_31_7_2015_pdf_31327.pdf. Accessed 26 Jun 2017

  32. Ayres M, Ayres M, Ayres D, Santos A (2007) BioEstat 5.0: aplicações estatísticas nas áreas das ciências biológicas e médicas. Instituto de Desenvolvimento Sustentável Mamirauá - IDSM/MCT/CNPq, vol 1. p 364

  33. Rey D, Vidinic-Moularde J, Meyer P, Schmitt C, Fritsch S, Lang JM et al (2000) High prevalence of GB virus C/Hepatitis G virus RNA and antibodies in patients infected with human immunodeficiency virus type 1. Eur J Clin Microbiol Infect Dis 19:721–724

    Article  CAS  PubMed  Google Scholar 

  34. Rendina D, Vigorita E, Bonavolta R, D’Onofrio M, Iura A, Pietronigro MT et al (2001) HCV and GBV-c/HGV infection in HIV positive patients in southern Italy. Eur J Epidemiol 17:801–807

    Article  CAS  PubMed  Google Scholar 

  35. Gutierrez RA, Dawson GJ, Knigge MF, Melvin SL, Heynen CA, Kyrk CR et al (1997) Seroprevalence of GB virus C and persistence of RNA and antibody. J Med Virol 53:167–173

    Article  CAS  PubMed  Google Scholar 

  36. Ribeiro-dos-Santos G, Nishiya A, Nascimento C, Bassit L, Chamone D, Focaccia R et al (2002) Prevalence of GB virus C (Hepatitis G virus) and risk factors for infection in Sao Paulo, Brazil. Eur J Clin Microbiol Infect Dis 21:438–443

    Article  CAS  PubMed  Google Scholar 

  37. Levi JE, Contri DG, Lima LP, Takaoka DT, Garrini RH, Santos W et al (2003) High prevalence of GB virus C/Hepatitis G virus RNA among Brazilian blood donors. Rev Inst Med Trop Sao Paulo 45:75–78

    Article  PubMed  Google Scholar 

  38. Amarante MK, Miranda HC, de Oliveira CEC, de Oliveira KB, Watanabe MAE (2004) Detecção do RNA HGV/GBV-C em indivíduos saudáveis não portadores de HBV, HIV-1/2 e HCV. Semina: Ciências Biológicas e da Saúde 25:39–44

  39. Ramezani A, Mohraz M, Vahabpour R, Jam S, Banifazl M, Eslamifar A et al (2008) Frequency of Hepatitis G virus infection among HIV positive subjects with parenteral and sexual exposure. J Gastrointestin Liver Dis 17:269–272

    PubMed  Google Scholar 

  40. Scallan MF, Clutterbuck D, Jarvis LM, Scott GR, Simmonds P (1998) Sexual transmission of GB virus C/hepatitis G virus. J Med Virol 55:203–208

    Article  CAS  PubMed  Google Scholar 

  41. Jarvis L, Davidson F, Hanley J, Yap P, Ludlam C, Simmonds P (1996) Infection with Hepatitis G virus among recipients of plasma products. Lancet 348:1352–1355

    Article  CAS  PubMed  Google Scholar 

  42. Hekmat S, Mohraz M, Vahabpour R, Jam S, Bahramali G, Banifazl M et al (2008) Frequency and genotype of GB virus C among Iranian patients infected with HIV. J Med Virol 80:1941–1946

    Article  CAS  PubMed  Google Scholar 

  43. Brasil. Ministério da Saúde, Secretaria de Vigilância em Saúde (2015) Programa nacional de DST e AIDS. Boletim epidemiológico—AIDS

  44. Toyoda H, Fukuda Y, Hayakawa T, Takamatsu J, Saito H (1998) Effect of GB virus C/Hepatitis G virus coinfection on the course of HIV infection in hemophilia patients in Japan. J Acquir Immune Defic Syndr Hum Retrovirol 17:209–213

    Article  CAS  PubMed  Google Scholar 

  45. Lefrère JJ, Roudot-Thoraval F, Morand-Joubert L, Petit JC, Lerable J, Thauvin M et al (1999) Carriage of GB virus C/Hepatitis G virus RNA is associated with a slower immunologic, virologic, and clinical progression of human immunodeficiency virus disease in coinfected persons. J Infect Dis 179:783–789

    Article  PubMed  Google Scholar 

  46. Martinez-Picado J, Deeks SG (2016) Persistent HIV-1 replication during antiretroviral therapy. Curr Opin HIV AIDS 11:417–423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Koedel Y, Eissmann K, Wend H, Fleckenstein B, Reil H (2011) Peptides derived from a distinct region of GB Virus C glycoprotein E2 mediate strain specific HIV-1 entry inhibition. J Virol 85:7037–7047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. George SL, Varmaz D, Tavis JE, Chowdhury A (2012) The GB virus C (GBV-C) NS3 serine protease inhibits HIV-1 replication in a CD4+ T lymphocyte cell line without decreasing HIV receptor expression. PLoS One 7:e30653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Tillmann HL, Manns MP, Claes C, Heiken H, Schmidt RE, Stoll M (2004) GB virus C infection and quality of life in HIV-positive patients. AIDS Care 16:736–743

    Article  CAS  PubMed  Google Scholar 

  50. Ruiz V, Espínola L, Mathet VL, Perandones CE, Oubiña JR (2006) Design, development and evaluation of a competitive RT-PCR for quantitation of GBV-C RNA. J Virol Methods 136:58–64

    Article  CAS  PubMed  Google Scholar 

  51. Mosam A, Sathar MA, Dawood H, Cassol E, Esterhuizen TM, Coovadia HM (2007) Effect of GB virus C co-infection on response to generic HAART in African patients with HIV-1 clade C infection. AIDS 21:1377–1379

    Article  CAS  PubMed  Google Scholar 

  52. Li C, Collini P, Danso K, Owusu-Ofori S, Dompreh A, Candotti D, Opare-Sem O, Allain JP (2006) Gb virus C And Hiv-1 Rna load in single virus and co-infected west african individuals. Aids 20:379–386

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank all patients who agreed to participate in the study.

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Authors and Affiliations

  1. Virus Laboratory, Institute of Biological Sciences, Federal University of Pará (Universidade Federal do Pará), Belem, Para, Brazil

    Bárbara Katharine Barbosa de Miranda, Keyla Santos Guedes de Sá, Andrea Nazaré Rangel da Silva, Rosimar Neris Martins Feitosa, Izaura Maria Vieira Cayres-Vallinoto, Ricardo Ishak & Antonio Carlos Rosário Vallinoto

Authors
  1. Bárbara Katharine Barbosa de Miranda
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  2. Keyla Santos Guedes de Sá
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  3. Andrea Nazaré Rangel da Silva
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  4. Rosimar Neris Martins Feitosa
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  5. Izaura Maria Vieira Cayres-Vallinoto
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  6. Ricardo Ishak
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  7. Antonio Carlos Rosário Vallinoto
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Corresponding author

Correspondence to Antonio Carlos Rosário Vallinoto.

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Conflict of interest

The authors declare that there are no conflicts of interest.

Ethical approval

The ethical approval of the present research was received from the Research Ethics Committee of the João de Barros Barreto Hospital of the Federal University of Pará in compliance with resolution 466/2012 (Protocol no. 2092/05).

Funding

The present study was funded by the National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq; process # 302582/2013-4).

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Funding source(s) had no involvement for the conduct of the research and/or preparation of the article.

Informed consent

All individuals in the study population were informed about the current study, with a written consent form taken from each before her or his enrolment in the present study.

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de Miranda, B.K.B., de Sá, K.S.G., da Silva, A.N.R. et al. GBV-C/HIV-1 coinfection is associated with low HIV-1 viral load and high CD4+ T lymphocyte count. Arch Virol 162, 3431–3438 (2017). https://doi.org/10.1007/s00705-017-3514-y

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