Hepatitis B and C virus infection among HIV patients within the public and private healthcare systems in Chile: A cross-sectional serosurvey

Autoři: Thomas Weitzel aff001;  Fernanda Rodríguez aff003;  Luis Miguel Noriega aff004;  Alejandra Marcotti aff004;  Luisa Duran aff004;  Carla Palavecino aff005;  Lorena Porte aff001;  Ximena Aguilera aff006;  Marcelo Wolff aff003;  Claudia P. Cortes aff003
Působiště autorů: Laboratorio Clínico, Clínica Alemana de Santiago, Facultad de Medicina Clínica Alemana, Universidad del Desarrollo, Santiago, Chile aff001;  Instituto de Ciencias e Innovación en Medicina (ICIM), Facultad de Medicina Clínica Alemana, Universidad del Desarrollo, Santiago, Chile aff002;  Fundación Arriarán, Santiago, Chile aff003;  Departamento de Medicina Interna, Clínica Alemana de Santiago, Facultad de Medicina Clínica Alemana, Universidad del Desarrollo, Santiago, Chile aff004;  Departamento de Medicina, Facultad de Medicina, Universidad de Chile, Santiago, Chile aff005;  Centro de Epidemiología y Políticas de Salud, Facultad de Medicina Clínica Alemana, Universidad del Desarrollo, Santiago, Chile aff006
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: 10.1371/journal.pone.0227776



Coinfections of HIV patients with hepatitis B virus (HBV) and hepatitis C virus (HCV) are mayor public health problems, contributing to the emerging burden of HIV-associated hepatic mortality. Coinfection rates vary geographically, depending on various factors such as predominant transmission modes, HBV vaccination rates, and prevalence of HBV and HCV in the general population. In South America, the epidemiology of coinfections is uncertain, since systematic studies are scarce. Our study aimed to analyze rates of HBV and HCV infection in people living with HIV attending centers of the public and private health system in Chile.


We performed a cross-sectional study including a public university hospital and a private health center in Santiago, Metropolitan Region in Chile. Serum samples were used to determine serological markers of hepatitis B (HBsAg, anti-HBs, anti-HBc total, HBeAg, anti-HBe) and anti-HCV. Demographic, clinical and laboratory data were obtained from medical records.


399 patients were included (353 from public, 46 from private health center). Most (92.8%) were male, with a median age of 38.3 years; 99.4% acquired HIV through sexual contact (75.0% MSM); 25.7% had AIDS and 90.4% were on ART. In 78.9%, viral loads were <40 cps/mL; the median CD4 cell count was 468 cells/mm3. According to their serological status, 37.6% of patients were HBV naïve (susceptible), 6.5% were vaccinated, 43.6% had resolved HBV infection, and 5.8% were chronically infected. The rate of vaccination was 4.5% in the public and 21.7% in the private system. HCV coinfection was found in 1.0% of all patients.


HBV coinfection rate was within the range of other South American countries, but lower than in non-industrialized regions in Asia and Africa. A low percentage of patients were HBV vaccinated, especially within the public system. HCV coinfection rate was very low, most probably due to the rareness of injecting drug use.

Klíčová slova:

Co-infections – Hepatitis B – Hepatitis B virus – Hepatitis C virus – HIV – Chile (country) – Serology – Vaccination and immunization


1. UNAIDS. Country Factsheet Chile 2018. Available from: https://www.unaids.org/es/regionscountries/countries/chile

2. Ministerio de Desarrollo Social y Familia. Encuesta CASEN 2017 [Internet]. Available from: http://observatorio.ministeriodesarrollosocial.gob.cl.

3. Beltrán C, Zitko P, Wolff M, Bernal F, Asenjo A, Fernández AM, et al. Evolución de las características epidemiológicas y clínicas de pacientes adultos del programa nacional al inicio de la terapia anti-retroviral en la Cohorte Chilena de SIDA, 2001–2015. Rev Chilena Infectol. 2016;33:2–10. doi: 10.4067/S0716-10182016000700001 28453022

4. Wolff MJ, Beltran CJ, Vasquez P, Ayala MX, Valenzuela M, Berrios G, et al. The Chilean AIDS cohort: a model for evaluating the impact of an expanded access program to antiretroviral therapy in a middle-income country—organization and preliminary results. J Acquir Immune Defic Syndr. 2005;40:551–7. doi: 10.1097/01.qai.0000185573.98472.f8 16284531

5. Wolff MJ, Cortes CP, Shepherd BE, Beltran CJ. Long-term outcomes of a national expanded access program to antiretroviral therapy: the Chilean AIDS cohort. J Acquir Immune Defic Syndr. 2010;55:368–74. doi: 10.1097/QAI.0b013e3181eb4fb9 20683194

6. Isapres de Chile. Informe VIH/SIDA. Cobertura GES y estadísticas 2018 [Internet] November 2018. Available from: https://www.isapre.cl/PDF/2018.11%20Informe%20VIH.pdf.

7. Ceballos ME, Rojas A, Donato P, Huilcaman M, Rivera G, Lopez T, et al. Virological and immunological outcomes to antiretroviral therapy in HIV-infected patients of an academic medical center in Chile. Rev Chilena Infectol. 2016;33:531–6. doi: 10.4067/S0716-10182016000500007 28112336

8. Morlat P, Roussillon C, Henard S, Salmon D, Bonnet F, Cacoub P, et al. Causes of death among HIV-infected patients in France in 2010 (national survey): trends since 2000. AIDS. 2014;28:1181–91. doi: 10.1097/QAD.0000000000000222 24901259

9. Smith C, Sabin CA, Lundgren JD, Thiebaut R, Weber R, Law M, et al. Factors associated with specific causes of death amongst HIV-positive individuals in the D:A:D Study. AIDS. 2010;24(10):1537–48. doi: 10.1097/QAD.0b013e32833a0918 20453631

10. Crowell TA, Berry SA, Fleishman JA, LaRue RW, Korthuis PT, Nijhawan AE, et al. Impact of hepatitis coinfection on healthcare utilization among persons living with HIV. J Acquir Immune Defic Syndr. 2015;68:425–31. doi: 10.1097/QAI.0000000000000490 25559601

11. Miro JM, Grossi PA, Durand CM. Challenges in solid organ transplantation in people living with HIV. Intensive Care Med. 2019;45:398–400. doi: 10.1007/s00134-019-05524-1 30637443

12. World Health Organization. WHO. Global Hepatitis Report 2017. Geneva: World Health Organization: 2017. License: CC BY-NC-SA 3.0 IGO.

13. European Centre for Disease Prevention and Control. Public health guidance on HIV, hepatitis B and C testing in the EU/EEA: An integrated approach. Stockholm: ECDC; 2018.

14. World Health Organization [Internet]. Factsheet Hepatitis B. Available from: https://www.who.int/news-room/fact-sheets/detail/hepatitis-b.

15. Alter MJ. Epidemiology of viral hepatitis and HIV co-infection. J Hepatol. 2006;44(1 Suppl):S6–9.

16. Singh KP, Crane M, Audsley J, Avihingsanon A, Sasadeusz J, Lewin SR. HIV-hepatitis B virus coinfection: epidemiology, pathogenesis, and treatment. AIDS. 2017;31):2035–52. doi: 10.1097/QAD.0000000000001574 28692539

17. Martins S, Livramento A, Andrigueti M, Kretzer IF, Machado MJ, Spada C, et al. The prevalence of hepatitis B virus infection markers and socio-demographic risk factors in HIV-infected patients in Southern Brazil. Rev Soc Bras Med Trop. 2014;47:552–8. doi: 10.1590/0037-8682-0109-2014 25467254

18. Kourtis AP, Bulterys M, Hu DJ, Jamieson DJ. HIV-HBV coinfection—a global challenge. New Engl J Med. 2012;366:1749–52. doi: 10.1056/NEJMp1201796 22571198

19. O'Hara GA, McNaughton AL, Maponga T, Jooste P, Ocama P, Chilengi R, et al. Hepatitis B virus infection as a neglected tropical disease. PLoS Negl Trop Dis. 2017;11:e0005842. doi: 10.1371/journal.pntd.0005842 28981505

20. Tengan FM, Abdala E, Nascimento M, Bernardo WM, Barone AA. Prevalence of hepatitis B in people living with HIV/AIDS in Latin America and the Caribbean: a systematic review and meta-analysis. BMC Infect Dis. 2017;17:587. doi: 10.1186/s12879-017-2695-z 28836955

21. Perez CC, Ceron AI, Fuentes LG, Zanartu SC, Balcells MM, Ajenjo HC, et al. Hepatitis B, C, Treponema pallidum and Toxoplasma gondii co-infections in HIV infected patients. Rev Chilena Infectol. 2009;137:641–8.

22. Otto-Knapp R, Cortes CP, Saavedra F, Wolff M, Weitzel T. Hepatitis B prevalence and influence on HIV treatment outcome and mortality in the Chilean AIDS Cohort. Int J Infect Dis. 2013;17:e919–24. doi: 10.1016/j.ijid.2013.05.009 23849398

23. Soriano V, Vispo E, Labarga P, Medrano J, Barreiro P. Viral hepatitis and HIV co-infection. Antiviral Res. 2010;85:303–15. doi: 10.1016/j.antiviral.2009.10.021 19887087

24. Sun HY, Sheng WH, Tsai MS, Lee KY, Chang SY, Hung CC. Hepatitis B virus coinfection in human immunodeficiency virus-infected patients: a review. World J Gastroenterol. 2014;20:14598–614. doi: 10.3748/wjg.v20.i40.14598 25356024

25. Colin JF, Cazals-Hatem D, Loriot MA, Martinot-Peignoux M, Pham BN, Auperin A, et al. Influence of human immunodeficiency virus infection on chronic hepatitis B in homosexual men. Hepatology. 1999;29:1306–10. doi: 10.1002/hep.510290447 10094979

26. Bodsworth NJ, Cooper DA, Donovan B. The influence of human immunodeficiency virus type 1 infection on the development of the hepatitis B virus carrier state. J Infect Dis. 1991;163:1138–40. doi: 10.1093/infdis/163.5.1138 2019762

27. Thio CL, Seaberg EC, Skolasky R Jr., Phair J, Visscher B, Munoz A, et al. HIV-1, hepatitis B virus, and risk of liver-related mortality in the Multicenter Cohort Study (MACS). Lancet. 2002;360:1921–6. doi: 10.1016/s0140-6736(02)11913-1 12493258

28. Hoofnagle JH. Reactivation of hepatitis B. Hepatology. 2009;49(5 Suppl):S156–65.

29. Idoko J, Meloni S, Muazu M, Nimzing L, Badung B, Hawkins C, et al. Impact of hepatitis B virus infection on human immunodeficiency virus response to antiretroviral therapy in Nigeria. Clin Infect Dis. 2009;49:1268–73. doi: 10.1086/605675 19772386

30. Konopnicki D, Mocroft A, de Wit S, Antunes F, Ledergerber B, Katlama C, et al. Hepatitis B and HIV: prevalence, AIDS progression, response to highly active antiretroviral therapy and increased mortality in the EuroSIDA cohort. AIDS. 2005;19:593–601. doi: 10.1097/01.aids.0000163936.99401.fe 15802978

31. Omland LH, Weis N, Skinhoj P, Laursen A, Christensen PB, Nielsen HI, et al. Impact of hepatitis B virus co-infection on response to highly active antiretroviral treatment and outcome in HIV-infected individuals: a nationwide cohort study. HIV Med. 2008;9:300–6. doi: 10.1111/j.1468-1293.2008.00564.x 18400077

32. Rockstroh JK. Influence of viral hepatitis on HIV infection. J Hepatol. 2006;44(1 Suppl):S25–7.

33. Tohme RA, Holmberg SD. Is sexual contact a major mode of hepatitis C virus transmission? Hepatology. 2010;52:1497–505. doi: 10.1002/hep.23808 20635398

34. McFaul K, Maghlaoui A, Nzuruba M, Farnworth S, Foxton M, Anderson M, et al. Acute hepatitis C infection in HIV-negative men who have sex with men. J Viral Hepat. 2015;22:535–8. doi: 10.1111/jvh.12366 25412826

35. Tengan FM, Ibrahim KY, Dantas BP, Manchiero C, Magri MC, Bernardo WM. Seroprevalence of hepatitis C virus among people living with HIV/AIDS in Latin America and the Caribbean: a systematic review. BMC Infect Dis. 2016;16:663. doi: 10.1186/s12879-016-1988-y 27829381

36. Fainboim H, Gonzalez J, Fassio E, Martinez A, Otegui L, Eposto M, et al. Prevalence of hepatitis viruses in an anti-human immunodeficiency virus-positive population from Argentina. A multicentre study. J Viral Hepat. 1999;6:53–7.

37. Ibarra V H. Cambios en la epidemiología de las hepatitis virales en Chile y consideraciones en estrategias de prevención. Rev Med Chile. 2007;135:229–39. doi: 10.4067/s0034-98872007000200013

38. Soza A, Lopez-Lastra M. Hepatitis C in Chile: burden of the disease. Rev Med Chile. 2006;134(6):777–88. doi: 10.4067/s0034-98872006000600016 17130955

39. Kang W, Tong HI, Sun Y, Lu Y. Hepatitis C virus infection in patients with HIV-1: epidemiology, natural history and management. Expert Rev Gastroenterol Hepatol. 2014;8:247–66. doi: 10.1586/17474124.2014.876357 24450362

40. Portocarrero Nunez JA, Gonzalez-Garcia J, Berenguer J, Gallego MJV, Loyarte JAI, Metola L, et al. Impact of co-infection by hepatitis C virus on immunological and virological response to antiretroviral therapy in HIV-positive patients. Medicine. 2018;97(38):e12238. doi: 10.1097/MD.0000000000012238 30235668

41. Weis N, Lindhardt BO, Kronborg G, Hansen AB, Laursen AL, Christensen PB, et al. Impact of hepatitis C virus coinfection on response to highly active antiretroviral therapy and outcome in HIV-infected individuals: a nationwide cohort study. Clin Infect Dis. 2006;42:1481–7. doi: 10.1086/503569 16619163

42. Cortés CP, Lizana D, Northland R, Wolff R. M. Evolución de mortalidad, abandono, traslado y retención a corto, mediano y largo plazo en pacientes con infección por VIH: Fundación Arriarán 1990–2015. Rev Med Chile. 2018;146:290–9. doi: 10.4067/s0034-98872018000300290

43. World Health Organization. Hepatitis B. Geneva, Switzerland: World Health Organization; 2002. Available from: https://apps.who.int/iris/handle/10665/67746

44. From the Centers for Disease Control and Prevention. 1993 revised classification system for HIV infection and expanded surveillance case definition for AIDS among adolescents and adults. JAMA. 1993;269:729–30. 8093740

45. Caceres-Burton K. Report: Epidemiological situation of sexually transmitted infections in Chile, 2017. Rev Chilena Infectol. 2019;36:221–33. doi: 10.4067/S0716-10182019000200221 31344158

46. Ministerio de Salud de Chile, Organización Panamericana de la Salud. Vigilancia y Monitoreo de las Hepatitis Virales B y C, exploración y análisis de datos, 1st Ed. Santiago: Organizacion Panamericana de la Salud, Ministerio de Salud: 2015.

47. Sampaio AS, Alencar LCA, Moura PMMF, Correia JB, Barreto SB, Castelo A. Prevalencia de la co-infección con hepatitis B y C en pacientes HIV positivos y factores de riesgo asociados. Actualizaciones en SIDA. 2009;17:12–7.

48. Ott JJ, Stevens GA, Groeger J, Wiersma ST. Global epidemiology of hepatitis B virus infection: New estimates of age-specific HBsAg seroprevalence and endemicity. Vaccine. 2012;30:2212–9. doi: 10.1016/j.vaccine.2011.12.116 22273662

49. Vargas JI, Jensen D, Sarmiento V, Peirano F, Acuna P, Fuster F, et al. Presence of anti-HBc is associated to high rates of HBV resolved infection and low threshold for Occult HBV Infection in HIV patients with negative HBsAg in Chile. J Med Virol. 2016;88:639–46. doi: 10.1002/jmv.24384 26381185

50. Liang SH, Chen TJ, Lee SS, Tseng FC, Huang CK, Lai CH, et al. Risk factors of isolated antibody against core antigen of hepatitis B virus: association with HIV infection and age but not hepatitis C virus infection. J Acquir Immune Defic Syndr. 2010;54:122–8. doi: 10.1097/QAI.0b013e3181daafd5 20386111

51. Witt MD, Lewis RJ, Rieg G, Seaberg EC, Rinaldo CR, Thio CL. Predictors of the isolated hepatitis B core antibody pattern in HIV-infected and -uninfected men in the multicenter AIDS cohort study. Clin Infect Dis. 2013;56:606–12. doi: 10.1093/cid/cis908 23090927

52. Chang JJ, Mohtashemi N, Bhattacharya D. Significance and Management of Isolated Hepatitis B Core Antibody (Anti-HBc) in HIV and HCV: Strategies in the DAA Era. Curr HIV/AIDS Rep. 2018;15:172–81. doi: 10.1007/s11904-018-0379-y 29572624

53. Jansen K, Thamm M, Bock CT, Scheufele R, Kucherer C, Muenstermann D, et al. High Prevalence and High Incidence of Coinfection with Hepatitis B, Hepatitis C, and Syphilis and Low Rate of Effective Vaccination against Hepatitis B in HIV-Positive Men Who Have Sex with Men with Known Date of HIV Seroconversion in Germany. PloS ONE. 2015;10:e0142515. doi: 10.1371/journal.pone.0142515 26555244

54. Zunino ME. Epidemiología de la hepatitis B en Chile y esquemas de vacunación en Latinoamérica. Rev Chilena Infectol. 2002;19:140–55.

55. World Health Organization. WHO vaccine-preventable diseases: monitoring system. 2019 global summary [Internet]. WHO. 2019. Available from: http://apps.who.int/immunization_monitoring/globalsummary.

56. Ministerio de Salud. Sindrome de inmunodeficiencia adquirida VIH/SIDA. In: Ministerio de Salud (Ed.). Serie Guias Clínicas MINSAL. 2nd ed. Santiago: 2013.

57. Ministerio de Salud. Chile MdSd. Listado de Prestaciones Específico [Internet]. Santiago: 2016. Available from: https://diprece.minsal.cl/wrdprss_minsal/wp-content/uploads/2018/03/Lep_incluye-Decreto-8-de-2018.pdf.

58. Ramirez OC, Fernandez AD, Valderrama BS, Gomez QC, Tamara RJ, Alvarez MC. Hepatitis B vaccine in patients with human immunodeficiency virus infection. Rev Chilena Infectol. 2009;26:26–33. 19350156

59. Tedaldi EM, Baker RK, Moorman AC, Wood KC, Fuhrer J, McCabe RE, et al.; HIV Outpatient Study (HOPS) Investigators. Hepatitis A and B Vaccination Practices for Ambulatory Patients Infected with HIV. Clin Infect Dis. 2004;38:1478–84. doi: 10.1086/420740 15156488

60. Bailey CL, Smith V, Sands M. Hepatitis B vaccine: a seven-year study of adherence to the immunization guidelines and efficacy in HIV-1-positive adults. Int J Infect Dis. 2008;12:e77–e83. doi: 10.1016/j.ijid.2008.05.1226 18723381

61. Rock C, Barra Ed, Sadlier C, Kelly S, Dowling C, McNally C, et al. Impact of a new vaccine clinic on hepatitis B vaccine completion and immunological response rates in an HIV-positive cohort. J Infect Public Health. 2013;6:173–8. doi: 10.1016/j.jiph.2012.11.001 23668461

62. Panel on Opportunistic Infections in Adults and Adolescents with HIV. Guidelines for the prevention and treatment of opportunistic infections in adults and adolescents with HIV: recommendations from the Centers for Disease Control and Prevention, the National Institutes of Health, and the HIV Medicine Association of the Infectious Diseases Society of America. 2019 [Internet]. Available from: http://aidsinfo.nih.gov/contentfiles/lvguidelines/adult_oi.pdf.

63. European AIDS Clinical Society (EACS). Guidelines version 9.1, October 2018 [Internet]. Available from: http://www.eacsociety.org/files/2018_guidelines-9.1-english.pdf.

64. Centers for Disease Control and Prevention [Internet]. Epidemiology and Prevention of HIV and Viral Hepatitis 2019. Available from: https://www.cdc.gov/hepatitis/populations/hiv.htm.

65. Peters L, Mocroft A, Lundgren J, Grint D, Kirk O, Rockstroh J. HIV and hepatitis C co-infection in Europe, Israel and Argentina: a EuroSIDA perspective. BMC Infect Dis. 2014;14(Suppl 6):S13.

66. Servicio Nacional para la Prevención y Rehabilitación del Consumo de Drogas y Alcohol (SENDA). Quinto Estudio Nacional de Drogas en Población General de Chile, 2002. Santiago, Chile: Servicio Nacional para la Prevención y Rehabilitación del Consumo de Drogas y Alcohol (SENDA); 2003.

67. Anonymous. History of the health care system in Chile. Am J Public Health. 1977;67:31–6. doi: 10.2105/ajph.67.1.31 318809

68. Castillo-Laborde C A-SX, Hirmas-Adauy M, Matute WI, Delgado-Becerra I, Nájera-De Ferrari M, Olea-Normandin A, et al. Health insurance scheme performance and effects on health and health inequalities in Chile. MEDICC Review. 2017;19:57–64.

69. Aguilera X, Castillo-Laborde C, Ferrari MN, Delgado I, Ibanez C. Monitoring and evaluating progress towards universal health coverage in Chile. PLoS Med. 2014;11:e1001676. doi: 10.1371/journal.pmed.1001676 25244581

70. Goic G A. El Sistema de Salud de Chile: una tarea pendiente. Rev Med Chile. 2015;143:774–86. doi: 10.4067/S0034-98872015000600011 26230561

71. Vasquez F, Paraje G, Estay M. Income-related inequality in health and health care utilization in Chile, 2000–2009. Rev Panam Salud Publica. 2013;33:98–106. doi: 10.1590/s1020-49892013000200004 23525339

72. Alarcon AM, Chahin C, Munoz S, Wolff M, Northland R. Persons living with HIV/AIDS: ethnic and sociocultural differences in Chile. Rev Chilena Infectol. 2018;35:276–82. doi: 10.4067/s0716-10182018000300276 30534907

Článek vyšel v časopise


2020 Číslo 1