Incidence of putative HIV superinfection and sexual practices among HIV-infected men who have sex with men
Mohsin M. Sidat A , Anne M. Mijch B , Sharon R. Lewin B C , Jennifer F. Hoy B C , Jane Hocking A and Christopher K. Fairley A D EA School of Population Health, The University of Melbourne, Vic. 3010, Australia.
B Department of Medicine, Monash University, Vic. 3800, Australia.
C Infectious Diseases Unit, The Alfred Hospital, Vic. 3078, Australia.
D Melbourne Sexual Health Centre, 580 Swanston Street, Carlton, Vic. 3053, Australia.
E Corresponding author. Email: cfairley@unimelb.edu.au
Sexual Health 5(1) 61-67 https://doi.org/10.1071/SH07041
Submitted: 19 June 2007 Accepted: 27 November 2007 Published: 22 February 2008
Abstract
Objectives: To determine the upper limit for the incidence of clinically important HIV superinfection among HIV-infected men who have sex with men (MSM) and its relationship with engagement in unsafe sexual practices. Methods: This was a retrospective cohort and nested case-control study. Electronic files of all HIV-infected MSM not on antiretroviral therapy were reviewed. Those clients with sudden, unexplained and sustained declines in CD4 T-cell counts and increases in plasma HIV RNA were considered as being putatively superinfected with HIV and were recruited as cases, whereas those without these features were recruited as controls (four per case) to answer a self-administered questionnaire. Results: Ten cases were identified from 145 eligible MSM (7%, 95% confidence interval 3–11%), comprising a rate of 3.6 per 100 person-years at risk. Cases had an annual decline in CD4 T-cell counts of 201 cells µL–1 compared with 9 cells µL–1 for controls. There were no statistically significant differences between cases and controls with regard to sexual practices that may have exposed them to acquisition of HIV superinfection (P-value ≥ 0.4), nor in their perceptions or beliefs of HIV superinfection (P-value ≥ 0.3). Only a minority reported no previous knowledge of HIV superinfection (17%, 5/30). Overall, both cases and controls were engaging frequently in unsafe sexual practices with casual partners who were HIV infected (80 and 52%, respectively; P-value = 0.4) or whose HIV serostatus was unknown (40 and 50%, respectively; P-value = 1.0). Conclusions: Despite considerable unsafe sexual practices occurring among this cohort of sexually active MSM the incidence of clinically significant HIV superinfection was likely to be less than 4% per year.
Additional keywords: HIV superinfection, men who have sex with men, unsafe sexual practices.
Acknowledgements
The authors would like to express their thanks to all of the staff at the HIV Referral Clinic at Melbourne Sexual Health Centre as well as all of the staff from the HIV Clinic at The Alfred Hospital for assisting in recruiting participants for this study. In particular we would like to thank Kerrie Watson (from the Infectious Diseases Unit, The Alfred Hospital) and Tim Kuo (from the Melbourne Sexual Health Centre) for their valuable assistance at different stages of this study. Many thanks also to all participants who cordially agreed to take part in this study. Lastly, but not least, thank you to The Capacity Building Project (Higher Education) of the University Eduardo Mondlane (Maputo, Mozambique) for providing a scholarship to Mohsin Sidat for his PhD studies at The University of Melbourne (Australia). SRL is an NHMRC practitioner fellow.
[1]
[2] Volk JE, Prestage G, Jin F, Kaldor J, Ellard J, Kippax S, et al. Risk factors for HIV seroconversion in homosexual men in Australia. Sex Health 2006; 3 45–51.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[3] Blackard JT, Mayer KH. HIV superinfection in the era of increased sexual risk-taking. Sex Transm Dis 2004; 31 201–4.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[4] Smith DM, Richman DD, Little SJ. HIV superinfection. J Infect Dis 2005; 192 438–44.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[5] Steain MC, Wang B, Dwyer DE, Saksena NK. HIV-1 co-infection, superinfection and recombination. Sex Health 2004; 1 239–50.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[6] Allen TM, Altfeld M. HIV-1 superinfection. J Allergy Clin Immunol 2003; 112 829–35.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[7] Chan DJ. HIV-1 superinfection: evidence and impact. Curr HIV Res 2004; 2 271–4.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[8] Gottlieb GS, Nickle DC, Jensen MA, Wong KG, Grobler J, Li F, et al. Dual HIV-1 infection associated with rapid disease progression. Lancet 2004; 363 619–22.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[9] Grobler J, Gray CM, Rademeyer C, Seoighe C, Ramjee G, Karim SA, et al. Incidence of HIV-1 dual infection and its association with increased viral load set point in a cohort of HIV-1 subtype C-infected female sex workers. J Infect Dis 2004; 190 1355–9.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[10] Fang G, Weiser B, Kuiken C, Philpott SM, Rowland-Jones S, Plummer F, et al. Recombination following superinfection by HIV-1. AIDS 2004; 18 153–9.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[11] Chohan B, Lavreys L, Rainwater SMJ, Overbaugh J. Evidence of frequent reinfection with human immunodeficiency virus type 1 of a different subtype. J Virol 2005; 79 10701–8.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[12] Manigart O, Courgnaud V, Sanou O, Valéa D, Nagot N, Meda N, et al. HIV-1 superinfection in a cohort of commercial sex workers in Burkina Faso as assessed by an autologous heteroduplex mobility procedure. AIDS 2004; 18 1645–51.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[13] Tsui R, Herring BL, Barbour JD, Grant RM, Bacchetti P, Kral A, et al. Human immunodeficiency virus type 1 superinfection was not detected following 215 years of injection drug user exposure. J Virol 2004; 78 94–103.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[14] Yerly S, Jost S, Monnat M, Telenti A, Cavassini M, Chave JP, et al. HIV-1 co/superinfection in intravenous drug users. AIDS 2004; 18 1413–21.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[15] Smith DM, Wong JK, Daar ES, Richman DD, Little SJ. Incidence of HIV superinfection following primary infection. JAMA 2004; 292 1177–8.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[16] Gonzales MJ, Delwart EL, Rhee S, Tsui R, Zolopa AR, Taylor J,, et al. Lack of detectable human immunodeficiency virus type 1 superinfection during 1072 person-years of observation. J Infect Dis 2003; 188 397–405.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[17]
[18] Koelsch KK, Smith DM, Little SJ, Ignacio CC, Macaranas TR, Brown AJ, et al. Clade B HIV-1 superinfection with wild-type virus after primary infection with drug-resistant clade B virus. AIDS 2003; 17 F11–6.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[19] Smith DM, Wong JK, Hightower GK, Ignacio CC, Koelsch KK, Petropoulos CJ, et al. HIV drug resistance acquired through superinfection. AIDS 2005; 19 1251–6.
| PubMed |
[20] Brenner B, Routy JP, Quan Y, Moisi D, Oliveira M, Turner D, et al. Persistence of multidrug-resistant HIV-1 in primary infection leading to superinfection. AIDS 2004; 18 1653–60.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[21] Yang OO, Daar ES, Jamieson BD, Balamurugan A, Smith DM, Pitt JA, et al. Human immunodeficiency virus type 1 clade B superinfection: evidence for differential immune containment of distinct clade B strains. J Virol 2005; 79 860–8.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[22] Chakraborty B, Kiser P, Rangel HR, Weber J, Mirza M, Marotta ML, et al. Can HIV-1 superinfection compromise antiretroviral therapy? AIDS 2004; 18 132–4.
| PubMed |
[23] Colfax GN, Guzman R, Wheeler S, Mansergh G, Marks G, Rader M, et al. Beliefs about HIV reinfection (superinfection) and sexual behavior among a diverse sample of HIV-positive men who have sex with men. J Acquir Immune Defic Syndr 2004; 36 990–2.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[24]
[25] Kippax S, Noble J, Prestage G, Crawford JM, Campbell D, Baxter D, et al. Sexual negotiation in the AIDS era: negotiated safety revisited. AIDS 1997; 11 191–7.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[26]
[27] Buchbinder SP, Vittinghoff E, Heagerty PJ, Celum CL, Seage GR, Judson FN, et al. Sexual risk, nitrite inhalant use, and lack of circumcision associated with HIV seroconversion in men who have sex with men in the United States. J Acquir Immune Defic Syndr 2005; 39 82–9.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[28] Sutmoller F, Penna TL, de Souza C, Lambert J, Oswaldo Cruz Foundation STD/HIV Prevention Group. Human immunodeficiency virus incidence and risk behavior in the ‘Projecto Rio’: results of the first 5 years of the Rio de Janeiro open cohort of homosexual and bisexual men, 1994–98. Int J Infect Dis 2002; 6 259–65.
| Crossref | GoogleScholarGoogle Scholar |
[29]
[30] Gross KL, Porco TC, Grant RM. HIV-1 superinfection and viral diversity. AIDS 2004; 18 1513–20.
| Crossref | GoogleScholarGoogle Scholar |
[31] Altfeld M, Allen TM, Yu XG, Johnston MN, Agrawal D, Korber BT, et al. HIV-1 superinfection despite broad CD8+ T-cell responses containing replication of the primary virus. Nature 2002; 420 434–9.
| Crossref | GoogleScholarGoogle Scholar |
[32] Blackard JT, Cohen DE, Mayer KH. Human immunodeficiency virus superinfection and recombination: current state of knowledge and potential clinical consequences. Clin Infect Dis 2002; 34 1108–14.
| Crossref | GoogleScholarGoogle Scholar |
[33] van Kesteren N, Hospers HJ, Kok G, van Empelen P. Sexuality and sexual risk behavior in HIV-positive men who have sex with men. Qual Health Res 2005; 15 145–68.
| Crossref | GoogleScholarGoogle Scholar |
[34] Adam BD, Husbands W, Murray J, Maxwell J. Risk construction in the reinfection discourses of HIV-positive men. Health Risk Soc 2005; 7 63–71.
| Crossref | GoogleScholarGoogle Scholar |
[35] Jost S, Bernard MC, Kaiser L, Yerly S, Hirschel B, Samri A, et al. A patient with HIV-1 superinfection. N Engl J Med 2002; 347 731–6.
| Crossref | GoogleScholarGoogle Scholar |
[36] van der Kuyl A, Kozaczynska K, van den Burg R, Zorgdrager F, Back N, Jurriaans S, et al. Triple HIV-1 infection. N Engl J Med 2005; 352 2557–9.
| Crossref | GoogleScholarGoogle Scholar |
[37] McCutchan FE, Hoelscher M, Tovanabutra S, Piyasirisilp S, Sanders-Buell E, Ramos G, et al. In-depth analysis of a heterosexually acquired human immunodeficiency virus type 1 superinfection: evolution, temporal fluctuation, and intercompartment dynamics from the seronegative window period through 30 months postinfection. J Virol 2005; 79 11 693–704.
| Crossref | GoogleScholarGoogle Scholar |
[38] Deeks SG, Kitchen CMR, Liu L, Guo H, Gascon R, Narváez AB, et al. Immune activation set point during early HIV infection predicts subsequent CD4+ T-cell changes independent of viral load. Blood 2004; 104 942–7.
| Crossref | GoogleScholarGoogle Scholar |
[39] Lewin S, Ribeiro RM, Kaufmann GR, Smith D, Zaunders J, Law M, et al. Dynamics of T cells and TCR excision circles differ after treatment of acute and chronic HIV infection. J Immunol 2002; 169 4657–66.
[40] Buchacz K, Patel P, Taylor M, Kerndt PR, Byers RH, Holmberg SD, et al. Syphilis increases HIV viral load and decreases CD4 cell counts in HIV-infected patients with new syphilis infections. AIDS 2004; 18 2075–9.
| Crossref | GoogleScholarGoogle Scholar |
[41] Vassend O, Eskild A. Psychological distress, coping, and disease progression in HIV-positive homosexual men. J Health Psychol 1998; 3 243–57.
[42] Burack JH, Barrett DC, Stall RD, Chesney MA, Ekstrand ML, Coates TJ. Depressive symptoms and CD4 lymphocyte decline among HIV-infected men. JAMA 1993; 270 2568–73.
| Crossref | GoogleScholarGoogle Scholar |
[43] Stanley SK, Ostrowski MA, Justement JS, Gantt K, Hedayati S, Mannix M, et al. Effect of immunization with a common recall antigen on viral expression in patients infected with human immunodeficiency virus type 1. N Engl J Med 1996; 334 1222–30.
| Crossref | GoogleScholarGoogle Scholar |
[44] Connor RI, Sheridan KE, Ceradini D, Choe S, Landau NR. Change in coreceptor use correlates with disease progression in HIV-1-infected individuals. J Exp Med 1997; 185 621–8.
| Crossref | GoogleScholarGoogle Scholar |
[45] Tersmette M, Gruters RA, de Wolf F, de Goede RE, Lange JM, Schellekens PT, et al. Evidence for a role of virulent human immunodeficiency virus (HIV) variants in the pathogenesis of acquired immunodeficiency syndrome: studies on sequential HIV isolates. J Virol 1989; 63 2118–25.
[46] Schuitemaker H, Koot M, Kootstra NA, Dercksen MW, de Goede RE, van Steenwijk RP, et al. Biological phenotype of human immunodeficiency virus type 1 clones at different stages of infection: progression of disease is associated with a shift from monocytotropic to T-cell-tropic virus population. J Virol 1992; 66 1354–60.
[47] Moore JP, Kitchen SG, Pugach P, Zack JA. The CCR5 and CXCR4 coreceptors – central to understanding the transmission and pathogenesis of human immunodeficiency virus type 0 infection. AIDS Res Hum Retroviruses 2004; 20 111–26.
| Crossref | GoogleScholarGoogle Scholar |
[48] Keet IP, Krol A, Koot M, Roos MT, de Wolf F, Miedema F, et al. Predictors of disease progression in HIV-infected homosexual men with CD4+ cells < 200 × 10–6 L but free of AIDS-defining clinical disease. AIDS 1994; 8 1577–84.
| Crossref | GoogleScholarGoogle Scholar |
