Integrated HIV surveillance finds recent adult hepatitis B virus (HBV) transmission and intermediate HBV prevalence among military in uncharacterized Caribbean country

Autoři: Siobhan M. O’Connor aff001;  Tonya Mixson-Hayden aff001;  Lilia Ganova-Raeva aff001;  Djeneba Audrey Djibo aff002;  Matthew Brown aff003;  Guo-Liang Xia aff001;  Saleem Kamili aff001;  Marni Jacobs aff002;  Maxia Dong aff004;  Anne G. Thomas aff002;  Marc Bulterys aff002;  Braden Hale aff002
Působiště autorů: Division of Viral Hepatitis, National Center for HIV/AIDS, Viral Hepatitis, STD and TB Prevention, United States Centers for Disease Control and Prevention, Atlanta, GA, United States of America aff001;  Department of Defense HIV/AIDS Prevention Program, United States Naval Health Research Center, San Diego, CA, United States of America aff002;  Division of Global HIV and Tuberculosis, Center for Global Health, United States Centers for Disease Control and Prevention, Atlanta, GA, United States of America aff003;  Division of Global HIV and Tuberculosis, United States Centers for Disease Control and Prevention, CDC Guyana, Georgetown, Guyana aff004
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article



Guyana expanded its HIV response in 2005 but the epidemiology of hepatitis B virus (HBV) and hepatitis C virus (HCV) infections has not been characterized.


The 2011 Seroprevalence and Behavioral Epidemiology Risk Survey for HIV and STIs collected biologic specimens with demographic and behavioral data from a representative sample of Guyana military personnel. Diagnostics included commercial serum: HIV antibody; total antibody to hepatitis B core (anti-HBc); IgM anti-HBc; hepatitis B surface antigen (HBsAg); anti-HBs; antibody to HCV with confirmatory testing; and HBV DNA sequencing with S gene fragment phylogenetic analysis. Chi-square, p-values and prevalence ratios determined statistical significance.


Among 480 participants providing serologic specimens, 176 (36.7%) tested anti-HBc-positive. Overall, 19 (4.0%) participants tested HBsAg-positive; 17 (89.5%) of the HBsAg-positive participants also had detectable anti-HBc, including 1 (5.3%) IgM anti-HBc-positive male. Four (6.8%) females with available HBV testing were HBsAg-positive, all aged 23–29 years. Sixteen (16, 84.2%) HBsAg-positive participants had sufficient specimen for DNA testing. All 16 had detectable HBV DNA, 4 with viral load >2x104IU/ml. Sequencing found: 12 genotype (gt) A1 with 99.9% genetic identity between 1 IgM anti-HBc-positive and 1 anti-HBc-negative; 2 gtD1; and 2 with insufficient specimen. No statistically significant associations between risk factors and HBV infection were identified.


Integrated HIV surveillance identified likely recent adult HBV transmission, current HBV infection among females of reproductive age, moderate HBV infection prevalence (all gtA1 and D1), no HCV infections and low HIV frequency among Guyana military personnel. Integrated HIV surveillance helped characterize HBV and HCV epidemiology, including probable recent transmission, prompting targeted responses to control ongoing HBV transmission and examination of hepatitis B vaccine policies.

Klíčová slova:

Hepatitis B virus – Hepatitis C virus – HIV epidemiology – Military personnel – Sexually transmitted diseases – Guyana – Hepatitis B


1. UNAIDS. WHO Epidemiological Fact Sheet– 2004 Update. Available at: Accessed 26 September 2013.

2. UNAIDS. Global Report. UNAIDS report on the global HIV epidemic 2013. Available at: Accessed 10 January 2014.

3. Ministry of Health Guyana. Behavioral Surveillance Survey, Executive Summary, Round I: 2003/2004. Available at: Accessed 01 April 2014.

4. Guyana Ministry of Health, National AIDS Programme. 2009. Guyana Behavioral Surveillance Surveys: 2008/2009 Report, including a Comparative Analysis with 2003/2004 BSS Results.

5. Government of Guyana-United Nations General Assembly Special Session on HIV/AIDS Progress Report, 2008–2009. Available at: Accessed 01 April 2014.

6. Ministry of Health, Guyana. Guyana National HIV/AIDS Strategy 2007–2011. Available at: Accessed 02 March 2014.

7. Lloyd J, Papworth E, Grant L, Beyrer C, Baral S. Systematic review and meta-analysis of HIV prevalence among men in militaries in low income and middle income countries. Sex Transm Infect 2014 Aug;90(5):382–387. doi: 10.1136/sextrans-2013-051463 24711546

8. Stahlman S, Javanbakht M, Cochran S, Hamilton AB, Shoptaw S, Gorbach PM. Self-reported sexually transmitted infections and sexual risk behaviors in the U.S. Military: how sex influences risk. Sex Transm Dis 2014 Jun;41(6):359–64. doi: 10.1097/OLQ.0000000000000133 24825331

9. Anastario M, Manzanero R, Blanco R, Reyes E, Jaramillio R, Black L, et al. HIV infection, sexual risk behaviour and condom use in the Belize defense force. Int J STD AIDS 2011 Feb;22(2):73–9. doi: 10.1258/ijsa.2010.010274 21427427

10. Global Hepatitis Report 2017. Geneva: World Health Organization; 2017. Licence: CC BY-NC-SA 3.0 IGO.

11. Schweitzer A, Horn J, Mikolajczyk RT, Krause G, Ott JJ. Estimations of worldwide prevalence of chronic hepatitis B virus infection: a systematic review of data published between 1965 and 2013. Lancet 2015 Oct 17;386(10003):1546–55. doi: 10.1016/S0140-6736(15)61412-X 26231459

12. Alvarado-Mora MV, Pinho JR. Epidemiological update of hepatitis B, C and delta in Latin America. Antivir Ther 2013;18(3part B):429–33.

13. Brichler S, Lagathu G, Chekaraou MA, Le Gal F, Edouard A, Dény P, et al. African, Amerindian and European hepatitis B virus strains circulate on the Caribbean Island of Martinique. J Gen Virol 2013 Oct;94(Pt 10):2318–29. doi: 10.1099/vir.0.055459-0 23884366

14. Couto CA, Levy C, Morris CJ, Hill M, de Medina M, Sanborn MR, et al. High frequency of genotype D and spontaneous hepatitis B virus genomic mutations among Haitians in a multiethnic North American population. J Clin Gastroenterol 2013 Jan;47(1):83–8. doi: 10.1097/MCG.0b013e318268003b 23059410

15. Crispim MAE, Fraiji NA, Campello SC, Schriefer NA, Stefani MM, Kiesslich D. Molecular epidemiology of hepatitis B and hepatitis delta viruses circulating in the Western Amazon region, North Brazil. BMC Infectious Diseases 2014 Feb 21;14:94. Available at Accessed 27 August 2015. doi: 10.1186/1471-2334-14-94 24555665

16. Barros LM, Gomes-Gouvêa MS, Kramvis A, Mendes-Corrêa MC, dos Santos A, Souza LA, et al. High prevalence of hepatitis B virus subgenotypes A1 and D4 in Maranhão state, Northeast Brazil. Infect Genet Evol 2014 Jun;24:68–75. doi: 10.1016/j.meegid.2014.03.007 24642137

17. Alvarado-Mora MV, Pinho JR. Distribution of HBV genotypes in Latin America. Antivir Ther 2013;18(3 Pt B):459–65.

18. Hanafiah KM, Groeger J, Flaxman AD, Wiersma ST. Global epidemiology of hepatitis C virus infection: New estimates of age-specific antibody to HCV seroprevalence. Hepatology 2013 Apr;57(4):1333–42. doi: 10.1002/hep.26141 23172780

19. Alonso M, Gutzman A, Mazin R, Pinzon CE, Reveiz L, Ghidinelli M. Hepatitis C in key populations in Latin America and the Caribbean: systematic review and meta-analysis. Int J Public Health 2015 Nov;60(7):789–98. doi: 10.1007/s00038-015-0708-5 26298439

20. Perz JF, Armstrong GL, Farrington LA, Hutin YJ, Bell BP. The contributions of hepatitis B virus and hepatitis C virus infections to cirrhosis and primary liver cancer worldwide. J Hepatol 2006 Oct;45(4):529–38. doi: 10.1016/j.jhep.2006.05.013 16879891

21. Chun HM, Roediger MP, Hullsiek KH, Thio CL, Agan BK, Bradley WP, et al. Hepatitis B virus coinfection negatively impacts HIV outcomes in HIV seroconverters. J Infect Dis 2012 Jan 15;205(2):185–93. doi: 10.1093/infdis/jir720 22147794

22. Thio CL, Smeaton L, Saulynas M, Hwang H, Saravanan S, Kulkarni S, et al. Characterization of HIV-HBV coinfection in a multinational HIV-infected cohort. AIDS 2013 Jan 14;27(2):191–201. doi: 10.1097/QAD.0b013e32835a9984 23032418

23. Berenguer J, Alejos B, Hernando V, Viciana P, Salavert M, Santos I, et al. Trends in mortality according to hepatitis C virus serostatus in the era of combination antiretroviral therapy. AIDS 2012 Nov 13;26(17):2241–6. doi: 10.1097/QAD.0b013e3283574e94 22781223

24. Tsuchiya N, Pathipvanich P, Rojanawiwat A, Wichukchinda N, Koga I, Koga M, et al. Chronic hepatitis B and C virus co-infection increased all-cause mortality in HAART-naïve HIV patients in northern Thailand. Epidemiol Infect 2013 Sep;141(9):1840–8. doi: 10.1017/S0950268812002397 23114262

25. Tedaldi EM, Baker RK, Moorman AC, Alzola CF, Furher J, McCabe RE, et al. Influence of coinfection with hepatitis C virus on morbidity and mortality due to human immunodeficiency virus in the era of highly active antiretroviral therapy. Clin Infect Dis 2003 Feb 1;36(3): 363–7. doi: 10.1086/345953 12539079

26. Macera C, Ito SI, Hale BR, Shaffer RA, Thomas AG, Dickieson J. A Strategy for Conducting an HIV Seroprevalence and Behavioral Epidemiology Risk Survey (SABERS) among Partner Military Populations. Curr HIV Res 2017;15(2):82–9. doi: 10.2174/1570162X15666170516164521 28521715

27. Ministry of Health (MOH), Bureau of Statistics (BOS) and ICF Macro. 2010. Guyana Demographic and Health Survey 2009. Georgetown, Guyana: MOH, BOS and ICF Macro. Available at: Accessed 01 April 2015.

28. Ministry of Health, Guyana. National Guidelines for Management of HIV-Infected and HIV-Exposed Adults and Children. August 2006 Revision. Available at: Accessed 01 April 2015.

29. Ramachandran S, Zhai X, Thai H, Campos DS, Xia G, Ganova-Raeva LM, et al. Evaluation of intra-host variants of the entire hepatitis B virus genome. PLoS One 2011 Sep 20;6(9):e25232. Accessed 27 August 2015. doi: 10.1371/journal.pone.0025232 21949887

30. Forbi JC, Vaughan G, Purdy MA, Campo DS, Xia DL, Ganova-Raeva LM, et al. Epidemic History and Evolutionary Dynamics of Hepatitis B Virus Infection in Two Remote Communities in Rural Nigeria. PLoS One 2010 Jul 19;5(7):e11615. Accessed 27 August 2015. doi: 10.1371/journal.pone.0011615 20657838

31. Tamura K, Nei M, Kumar S. Prospects for inferring very large phylogenies by using the neighbor-joining method. 2004. Proc Natl Acad Sci U S A 2004 (Jul 27);101(30):11030–5. doi: 10.1073/pnas.0404206101 15258291

32. Lock G, Dirscherl M, Obermeier F, Gelbmann CM, Hellerbrand C, Knöll A, et al. Hepatitis C—contamination of toothbrushes: myth or reality? J Viral Hepat 2006 Sep;13(9):571–3. doi: 10.1111/j.1365-2893.2006.00735.x 16907842

33. Quereshi H, Arif A, Riaz K, Alam SE, Ahmed W, Mujeeb SA. Determination of risk factors for hepatitis B and C in male patients suffering from chronic hepatitis. BMC Res Notes 2009 Oct 23;2:212. Accessed 15 Jun 2018 doi: 10.1186/1756-0500-2-212 19852780

34. World Health Organization. Hepatitis B vaccines. WHO position paper. Wkly Epidemiol Rec 2017 July 7;92(27):369–92. 28685564

35. Kourtis AP, Bulterys M, Hu DJ, Jamieson DJ. HIV-HBV coinfection—a global challenge. N Engl J Med 2012 May 10;366(19):1749–52. doi: 10.1056/NEJMp1201796 22571198

36. World Health Organization. Immunizations, vaccines and biologicals. Available at: Accessed 26 August 2016.

37. World Health Organization. Guidelines for the prevention, care and treatment of persons with chronic hepatitis B infection, March 2015. Available at: Accessed 26 August 2016.

38. Republic of Guyana. 2015 Guyana AIDS Response Progress Report. Reporting Period: January-December 2014. Available from Accessed 08 June 2019.

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