Abstract
Intravenous drug users (IDUs) have been demonstrated to be highly vulnerable to HIV/AIDS. Nevertheless, the prevalence of Kaposi’s sarcoma associated herpesvirus (KSHV), an important co-infected agent with HIV, among this population remained obscure. We conducted a systematic review on the epidemiological features of KSHV among IDUs worldwide. Eligible studies were retrieved from 6 electronic databases (PubMed, EMBASE, Web of Science, CBM, CNKI and Wanfang). We calculated the pooled prevalence and 95% confidence interval (CI) overall and among subgroups using either random-effects model or fixed-effects model depending on between-study heterogeneity. The potential publication bias was assessed by the Egger’s test. A meta-regression analysis was performed to explore the sources of heterogeneity. Finally, twenty-two studies with a total sample of 7881 IDUs were included in the analysis. The pooled prevalence of KSHV was 14.71% (95% CI 11.12%–19.46%) among IDUs. Specifically, KSHV prevalence was 10.86% (95% CI 6.95%–16.96%) in HIV-negative IDUs, and 13.56% (95% CI 10.57%–17.38%) in HIV-positive IDUs. Moreover, prevalence among IDUs from the three continents involved in the current study was similar: 16.10% (95%CI 7.73%–33.54%) in Asia; 14.22% (95%CI 8.96%–22.57%) in Europe and 14.06% (95%CI 11.38%–17.37%) in America. Globally, IDUs are at higher risk of the KSHV infection when compared with the general population, regardless of geographical region or HIV-infection status.
Electronic Supplementary Material
Supplementary material is available for this article at 10.1007/s12250-017-4051-2 and is accessible for authorized users.
Keywords: Kaposi’s sarcoma-associated herpesvirus (KSHV), prevalence, intravenous drug users (IDUs)
Electronic supplementary material
Prevalence of kaposi’s sarcoma-associated herpesvirus among intravenous drug users: a systematic review and meta-analysis
Acknowledgments
This work was supported by the Natural Science Foundation of Shanghai (17ZR1401400), the Natural Science Foundation of China (grant no. 81772170, U603117) and the Doctoral Fund of Ministry of Education of China (Grant No. 20120071120050).
Footnotes
These authors contributed equally to this work.
Contributor Information
Yan Zeng, Email: yzeng910@163.com.
Tiejun Zhang, Email: tjzhang@shmu.edu.cn.
References
- Ahmadi Ghezeldasht S, Hassannia T, Rafatpanah H, Hekmat R, Valizadeh N G, Mobarhan M, Rezaee SA. Oncogenic Virus Infections in the General Population and End-stage Renal Disease Patients With Special Emphasis on Kaposi’s Sarcoma Associated Herpes Virus (KSHV) in Northeast of Iran. Jundishapur J Microbiol. 2015;8:e14920. doi: 10.5812/jjm.14920. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Atkinson J, Edlin BR, Engels EA, Kral AH, Seal K, Gamache CJ, Whitby D, O’Brien TR. Seroprevalence of human herpesvirus 8 among injection drug users in San Francisco. J Infect Dis. 2003;187:974–981. doi: 10.1086/368332. [DOI] [PubMed] [Google Scholar]
- Bagni R, Whitby D. Kaposi’s sarcoma-associated herpesvirus transmission and primary infection. Curr Opin HIV AIDS. 2009;4:22–26. doi: 10.1097/COH.0b013e32831add5a. [DOI] [PubMed] [Google Scholar]
- Bernstein KT, Jacobson LP, Jenkins FJ, Vlahov D, Armenian HK. Factors associated with human herpesvirus type 8 infection in an injecting drug user cohort. Sex Transm Dis. 2003;30:199–204. doi: 10.1097/00007435-200303000-00004. [DOI] [PubMed] [Google Scholar]
- Biryahwaho B, Dollard SC, Pfeiffer RM, Shebl FM, Munuo S, Amin MM, Hladik W, Parsons R, Mbulaiteye SM. Sex and geographic patterns of human herpesvirus 8 infection in a nationally representative population-based sample in Uganda. J Infect Dis. 2010;202:1347–1353. doi: 10.1086/656525. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Butler LM, Dorsey G, Hladik W, Rosenthal PJ, Brander C, Neilands TB, Mbisa G, Whitby D, Kiepiela P, Mosam A, Mzolo S, Dollard SC, Martin JN. Kaposi sarcoma-associated herpesvirus (KSHV) seroprevalence in population-based samples of African children: evidence for at least 2 patterns of KSHV transmission. J Infect Dis. 2009;200:430–438. doi: 10.1086/600103. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cannon MJ, Dollard SC, Smith DK, Klein RS, Schuman P, Rich JD, Vlahov D, Pellett PE. Blood-borne and sexual transmission of human herpesvirus 8 in women with or at risk for human immunodeficiency virus infection. N Engl J Med. 2001;344:637–643. doi: 10.1056/NEJM200103013440904. [DOI] [PubMed] [Google Scholar]
- Chang Y, Cesarman E, Pessin MS, Lee F, Culpepper J, Knowles DM, Moore PS. Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi’s sarcoma. Science. 1994;266:1865–1869. doi: 10.1126/science.7997879. [DOI] [PubMed] [Google Scholar]
- Diamond C, Thiede H, Perdue T, MacKellar D, Valleroy LA, Corey L. Seroepidemiology of human herpesvirus 8 among young men who have sex with men. Sex Transm Dis. 2001;28:176–183. doi: 10.1097/00007435-200103000-00010. [DOI] [PubMed] [Google Scholar]
- Gambus G, Bourboulia D, Esteve A, Lahoz R, Rodriguez C, Bolao F, Sirera G, Muga R, Del RJ, Boshoff C, Whitby D, Casabona J. Prevalence and distribution of HHV-8 in different subpopulations, with and without HIV infection, in Spain. AIDS. 2001;15:1167–1174. doi: 10.1097/00002030-200106150-00012. [DOI] [PubMed] [Google Scholar]
- Goedert JJ, Charurat M, Blattner WA, Hershow RC, Pitt J, Diaz C, Mofenson LM, Green K, Minkoff H, Paul ME, Thomas DL, Whitby D. Risk factors for Kaposi’s Sarcoma-associated herpesvirus infection among HIV-1-infected pregnant women in the USA. AIDS. 2003;17:425–433. doi: 10.1097/00002030-200302140-00017. [DOI] [PubMed] [Google Scholar]
- Greenblatt RM, Jacobson LP, Levine AM, Melnick S, Anastos K, Cohen M, DeHovitz J, Young MA, Burns D, Miotti P, Koelle DM. Human herpesvirus 8 infection and Kaposi’s sarcoma among human immunodeficiency virus-infected and -uninfected women. J Infect Dis. 2001;183:1130–1134. doi: 10.1086/319270. [DOI] [PubMed] [Google Scholar]
- Kakavand-Ghalehnoei R, Shoja Z, Najafi A, Mollahoseini MH, Shahmahmoodi S, Marashi SM, Nejati A, Jalilvand S. Prevalence of human herpesvirus-8 among HIV-infected patients, intravenous drug users and the general population in Iran. Sex Health. 2016;13:295–298. doi: 10.1071/SH15192. [DOI] [PubMed] [Google Scholar]
- Kedes DH, Operskalski E, Busch M, Kohn R, Flood J, Ganem D. The seroepidemiology of human herpesvirus 8 (Kaposi’s sarcoma-associated herpesvirus): distribution of infection in KS risk groups and evidence for sexual transmission. Nat Med. 1996;2:918–924. doi: 10.1038/nm0896-918. [DOI] [PubMed] [Google Scholar]
- Khajedaluee M, Babaei A, Vakili R, Valizade N H, Shandiz F, Alavian S S, Nozadi M, Jazayeri SM, Hassannia T. Sero-Prevalence of Bloodborne Tumor Viruses (HCV, HBV, HTLV-I and KSHV Infections) and Related Risk Factors among Prisoners in Razavi Khorasan Province, Iran, in 2008. Hepat Mon. 2016;16:e31541. doi: 10.5812/hepatmon.31541. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Larocca L, Leto D, Celesta BM, Maccarone S, Mazza C, Cacopardo B, Nigro L. Prevalence of antibodies to HHV-8 in the general population and in individuals at risk for sexually transmitted and blood-borne infections in Catania, Eastern Sicily. Infez Med. 2005;13:79–85. [PubMed] [Google Scholar]
- Lee YM, Chuang SY, Wang SF, Lin YT, Chen YMA. Epidemiology of human herpesvirus type 8 and parvovirus B19 infections and their association with HIV-1 among men who have sex with men and injection drug users in Taiwan. J Microbiol Immunol Infect. 2014;47:233–238. doi: 10.1016/j.jmii.2013.01.006. [DOI] [PubMed] [Google Scholar]
- Liu Z, Fang Q, Zhou S, Minhas V, Wood C, He N, Zhang T. Seroprevalence of Kaposi’s sarcoma-associated herpesvirus among HIV-infected Uygurs in Xinjiang, China. J Med Virol. 2017;89:1629–1635. doi: 10.1002/jmv.24804. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liu Z, Fang Q, Zuo J, Wang J, Chen Y, Minhas V, Wood C, He N, Zhang T. High seroprevalence of human herpesvirus 8 and herpes simplex virus 2 infections in men who have sex with men in Shanghai, China. J Med Virol. 2017;89:887–894. doi: 10.1002/jmv.24718. [DOI] [PubMed] [Google Scholar]
- Luo ML, Tan HZ, Zhou Q, Wang SY, Cai C, Guo YW, Shen L. Realizing the Meta-Analysis of Single Rate in R Software. EBM. 2013;13:181. [Google Scholar]
- Minhas V, Wood C. Epidemiology and transmission of Kaposi’s sarcoma-associated herpesvirus. Viruses. 2014;6:4178–4194. doi: 10.3390/v6114178. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Moore PS. The emergence of Kaposi’s sarcoma-associated herpesvirus (human herpesvirus 8) N Engl J Med. 2000;343:1411–1413. doi: 10.1056/NEJM200011093431912. [DOI] [PubMed] [Google Scholar]
- Parisi SG, Sarmati L, Pappagallo M, Mazzi R, Carolo G, Farchi F, Nicastri E, Concia E, Rezza G, Andreoni M. Prevalence trend and correlates of HHV-8 infection in HIV-infected patients. J Acquir Immune Defic Syndr. 2002;29:295–299. doi: 10.1097/00126334-200203010-00011. [DOI] [PubMed] [Google Scholar]
- Perna AM, Bonura F, Vitale F, Viviano E D, Benedetto MA, Ajello F, Villafrate MR, Prestileo T, Mancuso S, Goedert JJ, Romano N. Antibodies to human herpes virus type 8 (HHV8) in general population and in individuals at risk for sexually transmitted diseases in Western Sicily. Int J Epidemiol. 2000;29:175–179. doi: 10.1093/ije/29.1.175. [DOI] [PubMed] [Google Scholar]
- Razonable RR. Rare, unusual, and less common virus infections after organ transplantation. Curr Opin Organ Transplant. 2011;16:580–587. doi: 10.1097/MOT.0b013e32834cdaf2. [DOI] [PubMed] [Google Scholar]
- Renwick N, Halaby T, Weverling GJ, Dukers NHTM, Simpson GR, Coutinho RA, Lange JMA, Schulz TF, Goudsmit J. Seroconversion for human herpesvirus 8 during HIV infection is highly predictive of Kaposi’s sarcoma. AIDS. 1998;12:2481–2488. doi: 10.1097/00002030-199818000-00018. [DOI] [PubMed] [Google Scholar]
- Rezza G, Andreoni M, Dorrucci M, Pezzotti P, Monini P, Zerboni R, Salassa B, Colangeli V, Sarmati L, Nicastri E, Barbanera M, Pristera R, Aiuti F, Ortona L, Ensoli B. Human herpesvirus 8 seropositivity and risk of Kaposi’s sarcoma and other acquired immunodeficiency syndrome-related diseases. J Natl Cancer Inst. 1999;91:1468–1474. doi: 10.1093/jnci/91.17.1468. [DOI] [PubMed] [Google Scholar]
- Rezza G, Lennette ET, Giuliani M, Pezzotti P, Caprilli F, Monini P, Butto S, Lodi G D, Carlo A, Levy JA, Ensoli B. Prevalence and determinants of anti-lytic and anti-latent antibodies to human herpesvirus-8 among Italian individuals at risk of sexually and parenterally transmitted infections. Int J Cancer. 1998;77:361–365. doi: 10.1002/(sici)1097-0215(19980729)77:3<361::aid-ijc9>3.0.co;2-m. [DOI] [PubMed] [Google Scholar]
- Rohner E, Wyss N, Heg Z, Faralli Z, Mbulaiteye SM, Novak U, Zwahlen M, Egger M, Bohlius J. HIV and human herpesvirus 8 co-infection across the globe: Systematic review and meta-analysis. Int J Cancer. 2016;138:45–54. doi: 10.1002/ijc.29687. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schwartz RA. Kaposi’s sarcoma: an update. J Surg Oncol. 2004;87:146–151. doi: 10.1002/jso.20090. [DOI] [PubMed] [Google Scholar]
- Schwartz RA, Micali G, Nasca MR, Scuderi L. Kaposi sarcoma: a continuing conundrum. J Am Acad Dermatol. 2008;59:179–206. doi: 10.1016/j.jaad.2008.05.001. [DOI] [PubMed] [Google Scholar]
- Simpson GR, Schulz TF, Whitby D, Cook PM, Boshoff C, Rainbow L, Howard MR, Gao SJ, Bohenzky RA, Simmonds P, Lee C D, Ruiter A, Hatzakis A, Tedder RS, Weller IVD, Weiss RA, Moore PS. Prevalence of Kaposi’s sarcoma associated herpesvirus infection measured by antibodies to recombinant capsid protein and latent immunofluorescence antigen. Lancet. 1996;349:1133–1138. doi: 10.1016/S0140-6736(96)07560-5. [DOI] [PubMed] [Google Scholar]
- Sosa C, Benetucci J, Hanna C, Sieczkowski L, Deluchi G, Canizal AM, Mantina H, Klaskala W, Baum M, Wood C. Human Herpes virus 8 can be transmitted through blood in drug addicts. Medicina. 2001;61:291–294. [PubMed] [Google Scholar]
- Stiller CA, Trama A, Brewster DH, Verne J, Bouchardy C, Navarro C, Chirlaque MD, Marcos-Gragera R, Visser O, Serraino D, Weiderpass E D, Tos AP, Ascoli V. Descriptive epidemiology of Kaposi sarcoma in Europe. Report from the RARECARE project. Cancer Epidemiol. 2014;38:670–678. doi: 10.1016/j.canep.2014.09.009. [DOI] [PubMed] [Google Scholar]
- Syvertsen JL, Agot K, Ohaga S, Strathdee SA, Camlin CS, Omanga E, Odonde P, Rota G, Akoth K, Peng J, Wagner KD. Evidence of injection drug use in Kisumu, Kenya: Implications for HIV prevention. Drug Alcohol Depend. 2015;151:262–266. doi: 10.1016/j.drugalcdep.2015.02.037. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tornesello ML, Biryahwaho B, Downing R, Hatzakis A, Alessi E, Cusini M, Ruocco V, Katongole-Mbidde E, Loquercio G, Buonaguro L, Buonaguro FM. Human herpesvirus type 8 variants circulating in Europe, Africa and North America in classic, endemic and epidemic Kaposi’s sarcoma lesions during pre-AIDS and AIDS era. Virology. 2010;398:280–289. doi: 10.1016/j.virol.2009.12.005. [DOI] [PubMed] [Google Scholar]
- Vitale F, Viviano E, Perna AM, Bonura F, Mazzola G, Ajello F, Romano N. Serological and virological evidence of nonsexual transmission of human herpesvirus type 8 (HHV8) Epidemiol Infect. 2000;125:671–675. doi: 10.1017/s0950268800004726. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wang Y, Zhu B, Zhao X, Zhang X. Seroprevalence of Kaposi’s sarcoma associated herpesvirus infection among drug users. National Medical Journal of China. 2000;80:597–598. [Google Scholar]
- Whitby D, Luppi M, Barozzi P, Boshoff C, Weiss RA, Torelli G. Human herpesvirus 8 seroprevalence in blood donors and lymphoma patients from different regions of Italy. J Natl Cancer Inst. 1998;90:395–397. doi: 10.1093/jnci/90.5.395. [DOI] [PubMed] [Google Scholar]
- Yang PR, Tan XH, Guo SX, Yang L. Research of Kaposi’s Sarcoma-associated herpesvirus in drug users in one city of Xinjiang. Modern Preventive Medicine. 2010;37:107–109. [Google Scholar]
- Zavitsanou A, Malliori M, Sypsa V, Petrodaskalaki M, Psichogiou M, Rokka C, Giannopoulos A, Kalapothaki V, Whitby D, Hatzakis A. Seroepidemiology of human herpesvirus 8 (HHV-8) infection in injecting drug users. Epidemiol Infect. 2010;138:403–408. doi: 10.1017/S0950268809990628. [DOI] [PubMed] [Google Scholar]
- Zhang T, Liu Y, Zhang Y, Wang J, Minhas V, Wood C, He N. Seroprevalence of human herpesvirus 8 and hepatitis C virus among drug users in Shanghai, China. Viruses. 2014;6:2519–2530. doi: 10.3390/v6062519. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhang T, Liu Z, Wang J, Minhas V, Wood C, Clifford GM, He N, Franceschi S. Seroprevalence of antibodies against Kaposi’s sarcoma-associated herpesvirus among HIV-negative people in China. Infect Agent Cancer. 2017;12:32. doi: 10.1186/s13027-017-0142-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhang T, Shao X, Chen Y, Zhang T, Minhas V, Wood C, He N. Human herpesvirus 8 seroprevalence, China. Emerg Infect Dis. 2012;18:150–152. doi: 10.3201/eid1801.102070. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhang T, Wang L. Epidemiology of Kaposi’s sarcoma-associated herpesvirus in Asia: Challenges and opportunities. J Med Virol. 2017;89:563–570. doi: 10.1002/jmv.24662. [DOI] [PubMed] [Google Scholar]
- Zhang T, Yang Y, Yu F, Zhao Y, Lin F, Minhas V, Wood C, He N. Kaposi’s sarcoma associated herpesvirus infection among female sex workers and general population women in Shanghai, China: a cross-sectional study. BMC Infect Dis. 2014;14:58. doi: 10.1186/1471-2334-14-58. [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Prevalence of kaposi’s sarcoma-associated herpesvirus among intravenous drug users: a systematic review and meta-analysis
