Phylogenetic inferences on HIV-1 transmission: Implications for the design of prevention and treatment interventions

AIDS

Volumn 27, Issue 7, 2013, Pages 1045-1057

  Brenner, Bluma ^a   Wainberg, Mark A ^a   Roger, Michel ^b  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Hiv 1 transmission; Phylogenetics; Primary infection; Treatment as prevention

Indexed keywords

EPIDEMIC; GENE CLUSTER; GEOGRAPHY; HETEROSEXUALITY; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; MEN WHO HAVE SEX WITH MEN; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROPHYLAXIS; REVIEW; VIRUS GENE; VIRUS TRANSMISSION;

ACQUIRED IMMUNODEFICIENCY SYNDROME; ANTI-INFECTIVE AGENTS; ANTIRETROVIRAL THERAPY, HIGHLY ACTIVE; CLUSTER ANALYSIS; DRUG RESISTANCE, MULTIPLE, VIRAL; EPIDEMICS; EVOLUTION, MOLECULAR; FEMALE; HEALTH SERVICES ACCESSIBILITY; HIV INFECTIONS; HIV-1; HUMANS; INFECTIOUS DISEASE TRANSMISSION, VERTICAL; MALE; MEDICATION ADHERENCE; PHYLOGENY; SEX WORKERS; SEXUAL BEHAVIOR; TRANSIENTS AND MIGRANTS;

EID: 84879109024     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0b013e32835cffd9     Document Type: Review

References (187)

1. Tebit DM, Arts EJ. Tracking a century of global expansion and evolution of HIV to drive understanding and to combat disease. Lancet Infect Dis 2011; 11:45-56.
2. Lihana RW, Ssemwanga D, Abimiku A, Ndembi N. Update on HIV-1 diversity in Africa: a decade in review. AIDS Rev 2012; 14:83-100
3. Beyrer C, Baral SD, van Griensven F, Goodreau SM, Chariyalertsak S, Wirtz AL, et al. Global epidemiology of HIV infection in men who have sex with men. Lancet 2012; 380:367-377.
4. Beyrer C, Sullivan PS, Sanchez J, Dowdy D, Altman D, Trapence G, et al. A call to action for comprehensive HIV services for men who have sex with men. Lancet 2012; 380:424-438.
5. Wainberg MA, Zaharatos GJ, Brenner BG. Development of antiretroviral drug resistance. N Engl J Med 2011; 365:637-646.
6. Hemelaar J, Gouws E, Ghys PD, Osmanov S. Global trends in molecular epidemiology of HIV-1 during 2000-2007. AIDS 2011; 25:679-689.
7. Castro-Nallar E, Perez-Losada M, Burton GF, Crandall KA. The evolution of HIV: inferences using phylogenetics. Mol Phylogenet Evol 2012; 62:777-792.
8. Donnell D, Baeten JM, Kiarie J, Thomas KK, Stevens W, Cohen CR, et al. Heterosexual HIV-1 transmission after initiation of antiretroviral therapy: a prospective cohort analysis. Lancet 2010; 375:2092-2098.
9. Novitsky V, Essex M. Using HIV viral load to guide treatment-for- prevention interventions. Curr Opin HIV AIDS 2012; 7:117-124.
10. Cohen MS, Chen YQ, McCauley M, Gamble T, Hosseinipour MC, Kumarasamy N, et al. Prevention of HIV-1 infection with early antiretroviral therapy. N Engl J Med 2011; 365:493-505.
11. Reynolds SJ, Makumbi F, Nakigozi G, Kagaayi J, Gray RH, Wawer M, et al. HIV-1 transmission among HIV-1 discordant couples before and after the introduction of antiretroviral therapy. AIDS 2011; 25:473-477.
12. Das M, Chu PL, Santos GM, Scheer S, Vittinghoff E, McFarland W, et al. Decreases in community viral load are accompanied by reductions in new HIV infections in San Francisco. PLoS One 2010; 5:e11068.
13. Grant RM, Lama JR, Anderson PL, McMahan V, Liu AY, Vargas L, et al. Preexposure chemoprophylaxis for HIV prevention in men who have sex with men. N Engl J Med 2010; 363:2587-2599.
14. Abdool Karim Q, Abdool Karim SS, Frohlich JA, Grobler AC, Baxter C, Mansoor LE, et al. Effectiveness and safetyoftenofovir gel, an antiretroviral microbicide, for the prevention of HIV infection in women. Science 2010; 329:1168-1174.
15. Thompson MA, Aberg JA, Hoy JF, Telenti A, Benson C, Cahn P, et al. Antiretroviral treatment of adult HIV infection: 2012 recommendations of the International Antiviral Society-USA Panel. JAMA 2012; 308:387-402.
16. Labarga P. New DHHS guidelines recommend antiretroviral therapy to all HIV-infected persons. AIDS Rev 2012; 14:154.
17. Baeten JM, Donnell D, Ndase P, Mugo NR, Campbell JD, Wangisi J, et al. Antiretroviral prophylaxis for HIV prevention in heterosexual men and women. N Engl J Med 2012.
18. Montaner JS, Lima VD, Barrios R, Yip B, Wood E, Kerr T, et al. Association of highly active antiretroviral therapy coverage, population viral load, and yearly new HIV diagnoses in British Columbia, Canada: a population-based study. Lancet 2010; 376:532-539.
19. Bendavid E, Grant P, Talbot A, Owens DK, Zolopa A. Cost-effectiveness of antiretroviral regimens in the World Health Organization's treatment guidelines: a South African analysis. AIDS 2011; 25:211-220.
20. Okwundu CI, Uthman OA, Okoromah CA. Antiretroviral preexposure prophylaxis (PrEP) for preventing HIV in high-risk individuals. Cochrane Database Syst Rev 2012; 7:CD007189.
21. Thigpen MC, Kebaabetswe PM, Paxton LA, Smith DK, Rose CE, Segolodi TM, et al. Antiretroviral preexposure prophylaxis for heterosexual HIV transmission in Botswana. N Engl J Med 2012; 367:423-434.
22. Van Damme L, Corneli A, Ahmed K, Agot K, Lombaard J, Kapiga S, et al. Preexposure prophylaxis for HIV infection among African women. N Engl J Med 2012; 367:411-422.
23. DeGruttola V, Smith DM, Little SJ, Miller V. Developing and evaluating comprehensive HIV infection control strategies: issues and challenges. Clin Infect Dis 2010; 50 (Suppl 3):S102 - S107.
24. van Sighem A, Vidondo B, Glass TR, Bucher HC, Vernazza P, Gebhardt M, et al. Resurgence of HIV infection among men who have sex with men in Switzerland: mathematical modelling study. PLoS One 2012; 7:e44819.
25. Jin F, Jansson J, Law M, Prestage GP, Zablotska I, Imrie JC, et al. Per-contact probability of HIV transmission in homosexual men in Sydney in the era of HAART. AIDS 2010; 24:907-913.
26. Smith K, Powers KA, Kashuba AD, Cohen MS. HIV-1 treatment as prevention: the good, the bad, and the challenges. Curr Opin HIV AIDS 2011; 6:315-325.
27. Brenner BG, Roger M, Stephens D, Moisi D, Hardy I, Weinberg J, et al. Transmission clustering drives the onward spread of the HIV epidemic among men who have sex with men in Quebec. J Infect Dis 2011; 204:1115-1119.
28. Hue S, Clewley JP, Cane PA, Pillay D. HIV-1 pol gene variation is sufficient for reconstruction of transmissions in the era of antiretroviral therapy. AIDS 2004; 18:719-728.
29. Brenner BG, Roger M, Routy JP, Moisi D, Ntemgwa M, Matte C, et al. High rates of forward transmission events after acute/early HIV-1 infection. J Infect Dis 2007; 195:951-959.
30. Pillay D, Fisher M. Primary HIV Infection, phylogenetics, and antiretroviral prevention. J Infect Dis 2007; 195:924-926.
31. Leigh Brown AJ, Lycett SJ, Weinert L, Hughes GJ, Fearnhill E, Dunn DT. Transmission network parameters estimated from HIV sequences for a nationwide epidemic. J Infect Dis 2011; 204:1463-1469.
32. Lam TT, Hon CC, Tang JW. Use of phylogenetics in the molecular epidemiology and evolutionary studies of viral infections. Crit Rev Clin Lab Sci 2010; 47:5-49.
33. Grenfell BT, Pybus OG, Gog JR, Wood JL, Daly JM, Mumford JA, et al. Unifying the epidemiological and evolutionary dynamics of pathogens. Science 2004; 303:327-332.
34. Pybus OG, Rambaut A. Evolutionary analysis of the dynamics of viral infectious disease. Nat Rev Genet 2009; 10:540-550.
35. Delva W, Wilson DP, Abu-Raddad L, Gorgens M, Wilson D, Hallett TB, et al. HIV treatment as prevention: principles of good HIV epidemiology modelling for public health decision-making in all modes of prevention and evaluation. PLoS Med 2012; 9:e1001239.
36. Delva W, Eaton JW, Meng F, Fraser C, White RG, Vickerman P, et al. HIV treatment as prevention: optimising the impact of expanded HIV treatment programmes. PLoS Med 2012; 9:e1001258.
37. Preston BD. Error-prone retrotransposition: rime of the ancient mutators. Proc Natl Acad Sci U S A 1996; 93:7427-7431.
38. Zhang M, Foley B, Schultz AK, Macke JP, Bulla I, Stanke M, et al. The role of recombination in the emergence of a complex and dynamic HIV epidemic. Retrovirology 2010; 7:25.
39. Korber B, Muldoon M, Theiler J, Gao F, Gupta R, Lapedes A, et al. Timing the ancestor of the HIV-1 pandemic strains. Science 2000; 288:1789-1796.
40. Onafuwa-Nuga A, Telesnitsky A. The remarkable frequency of human immunodeficiency virus type 1 genetic recombination. Microbiol Mol Biol Rev 2009; 73:451-480.
41. Preston BD, Dougherty JP. Mechanisms of retroviral mutation. Trends Microbiol 1996; 4:16-21.
42. Novitsky V, Wang R, Lagakos S, Essex M. HIV-1 subtype C phylodynamics in the global epidemic. Viruses 2010; 2:33-54.
43. Holmes EC, Grenfell BT. Discovering the phylodynamics of RNA viruses. PLoS Comput Biol 2009; 5:e1000505.
44. Clarke DK, Duarte EA, Moya A, Elena SF, Domingo E, Holland J. Genetic bottlenecks and population passages cause profound fitness differences in RNA viruses. J Virol 1993; 67:222-228.
45. Arien KK, Troyer RM, Gali Y, Colebunders RL, Arts EJ, Vanham G. Replicative fitness of historical and recent HIV-1 isolates suggests HIV-1 attenuation over time. AIDS 2005; 19:1555-1564.
46. Cohen MS, Shaw GM, McMichael AJ, Haynes BF. Acute HIV-1 Infection. N Engl J Med 2011; 364:1943-1954.
47. Lee HY, Giorgi EE, Keele BF, Gaschen B, Athreya GS, Salazar-Gonzalez JF, et al. Modeling sequence evolution in acute HIV-1 infection. J Theor Biol 2009; 261:341-360.
48. Salazar-Gonzalez JF, Bailes E, Pham KT, Salazar MG, Guffey MB, Keele BF, et al. Deciphering human immunodeficiency virus type 1 transmission and early envelope diversification by single-genome amplification and sequencing. J Virol 2008; 82:3952-3970.
49. Keele BF, Giorgi EE, Salazar-Gonzalez JF, Decker JM, Pham KT, Salazar MG, et al. Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc Natl Acad Sci USA 2008; 105:7552-7557.
50. Salazar-Gonzalez JF, Salazar MG, Keele BF, Learn GH, Giorgi EE, Li H, et al. Genetic identity, biological phenotype, and evolutionary pathways of transmitted/founder viruses in acute and early HIV-1 infection. J Exp Med 2009; 206:1273-1289.
51. Ferrari G, Korber B, Goonetilleke N, Liu MK, Turnbull EL, Salazar-Gonzalez JF, et al. Relationship between functional profile of HIV-1 specific CD8 T cells and epitope variability with the selection of escape mutants in acute HIV-1 infection. PLoS Pathog 2011; 7:e1001273.
52. Wood N, Bhattacharya T, Keele BF, Giorgi E, Liu M, Gaschen B, et al. HIV evolution in early infection: selection pressures, patterns of insertion and deletion, and the impact of APOBEC. PLoS Pathog 2009; 5:e1000414.
53. Kearney M, Maldarelli F, Shao W, Margolick JB, Daar ES, Mellors JW, et al. Human immunodeficiency virus type 1 population genetics and adaptation in newly infected individuals. J Virol 2009; 83:2715-2727.
54. Kong X, West JT, Zhang H, Shea DM, M'Soka TJ, Wood C. The human immunodeficiency virus type 1 envelope confers higher rates of replicative fitness to perinatally transmitted viruses than to nontransmitted viruses. J Virol 2008; 82:11609-11618.
55. Haaland RE, Hawkins PA, Salazar-Gonzalez J, Johnson A, Tichacek A, Karita E, et al. Inflammatory genital infections mitigate a severe genetic bottleneck in heterosexual transmission of subtype A and C HIV-1. PLoS Pathog 2009; 5:e1000274.
56. Ochsenbauer C, Edmonds TG, Ding H, Keele BF, Decker J, Salazar MG, et al. Generation of transmitted/founder HIV-1 infectious molecular clones and characterization of their replication capacity in CD4 T lymphocytes and monocyte-derived macrophages. J Virol 2012; 86:2715-2728.
57. Novitsky V, Ndung'u T, Wang R, Bussmann H, Chonco F, Makhema J, et al. Extended high viremics: a substantial fraction of individuals maintain high plasma viral RNA levels after acute HIV-1 subtype C infection. AIDS 2011; 25:1515-1522.
58. Bar KJ, Li H, Chamberland A, Tremblay C, Routy JP, Grayson T, et al. Wide variation in the multiplicity of HIV-1 infection among injection drug users. J Virol 2010; 84:6241-6247.
59. Abrahams MR, Anderson JA, Giorgi EE, Seoighe C, Mlisana K, Ping LH, et al. Quantitating the multiplicity of infection with human immunodeficiency virus type 1 subtype C reveals a nonpoisson distribution of transmitted variants. J Virol 2009; 83:3556-3567.
60. Gnanakaran S, Bhattacharya T, Daniels M, Keele BF, Hraber PT, Lapedes AS, et al. Recurrent signature patterns in HIV-1 B clade envelope glycoproteins associated with either early or chronic infections. PLoS Pathog 2011; 7:e1002209.
61. R T cells in acute HIV-1 infection inhibit transmitted/founder virus replication. J Virol 2012; 86:6835-6846.
62. Parrish NF, Wilen CB, Banks LB, Iyer SS, Pfaff JM, Salazar-Gonzalez JF, et al. Transmitted/founder and chronic subtype C HIV-1 use CD4 and CCR5 receptors with equal efficiency and are not inhibited by blocking the integrin alpha4beta7. PLoS Pathog 2012; 8:e1002686.
63. Pilcher CD, Tien HC, Eron JJ Jr, Vernazza PL, Leu SY, Stewart PW, et al. Brief but efficient: acute HIV infection and the sexual transmission of HIV. J Infect Dis 2004; 189:1785-1792.
64. Wawer MJ, Gray RH, Sewankambo NK, Serwadda D, Li X, Laeyendecker O, et al. Rates of HIV-1 transmission per coital act, by stage of HIV-1 infection, in Rakai, Uganda. J Infect Dis 2005; 191:1403-1409.
65. Hecht FM, Hartogensis W, Bragg L, Bacchetti P, Atchison R, Grant R, et al. HIV RNA level in early infection is predicted by viral load in the transmission source. AIDS 2010; 24:941-945.
66. Hollingsworth TD, Laeyendecker O, Shirreff G, Donnelly CA, Serwadda D, Wawer MJ, et al. HIV-1 transmitting couples have similar viral load set-points in Rakai, Uganda. PLoS Pathog 2010; 6:e1000876.
67. Brenner BG, Routy JP, Petrella M, Moisi D, Oliveira M, Detorio M, et al. Persistence and fitness of multidrug-resistant human immunodeficiency virus type 1 acquired in primary infection. J Virol 2002; 76:1753-1761.
68. Hamlyn E, Jones V, Porter K, Fidler S. Antiretroviral treatment of primary HIV infection to reduce onward transmission. Curr Opin HIV AIDS 2010; 5:283-290.
69. Skar H, Hedskog C, Albert J. HIV-1 evolution in relation to molecular epidemiology and antiretroviral resistance. Ann N Y Acad Sci 2011; 1230:108-118.
70. Brenner BG, Turner D, Wainberg MA. HIV-1 drug resistance: can we overcome? Expert Opin Biol Ther 2002; 2:751-761.
71. Gray RR, Tatem AJ, Lamers S, Hou W, Laeyendecker O, Serwadda D, et al. Spatial phylodynamics of HIV-1 epidemic emergence in east Africa. AIDS 2009; 23:F9-F17.
72. Kantor R. Impact of HIV-1 pol diversity on drug resistance and its clinical implications. Curr Opin Infect Dis 2006; 19:594-606.
73. Paraskevis D, Nikolopoulos G, Tsiara C, Paraskeva D, Antoniadou A, Lazanas M, et al. HIV-1 outbreak among injecting drug users in Greece, 2011: a preliminary report. Euro Surveill 2011; 16:1-4.
74. Gonzalez-Alba JM, Holguin A, Garcia R, Garcia-Bujalance S, Alonso R, Suarez A, et al. Molecular surveillance of HIV-1 in Madrid, Spain: a phylogeographic analysis. J Virol 2011; 85:10755-10763.
75. Paraskevis D, Magiorkinis E, Magiorkinis G, Sypsa V, Paparizos V, Lazanas M, et al. Increasing prevalence of HIV-1 subtype A in Greece: estimating epidemic history and origin. J Infect Dis 2007; 196:1167-1176.
76. Paraschiv S, Otelea D, Batan I, Baicus C, Magiorkinis G, Paraskevis D. Molecular typing of the recently expanding subtype B HIV-1 epidemic in Romania: evidence for local spread among MSMs in Bucharest area. Infect Genet Evol 2012; 12:1052-1057.
77. Salemi M, Lamers SL, Huysentruyt LC, Galligan D, Gray RR, Morris A, et al. Distinct patterns of HIV-1 evolution within metastatic tissues in patients with non-Hodgkins lymphoma. PLoS One 2009; 4:e8153.
78. Pang W, Zhang C, Duo L, Zhou YH, Yao ZH, Liu FL, et al. Extensive and complex HIV-1 recombination between B', C and CRF01-AE among IDUs in south-east Asia. AIDS 2012; 26:1121-1129.
79. Kuiken C, Korber B, Shafer RW. HIV sequence databases. AIDS Rev 2003; 5:52-61.
80. Maljkovic Berry I, Athreya G, Kothari M, Daniels M, Bruno WJ, Korber B, et al. The evolutionary rate dynamically tracks changes in HIV-1 epidemics: application of a simple method for optimizing the evolutionary rate in phylogenetic trees with longitudinal data. Epidemics 2009; 1:230-239.
81. Stanojevic M, Alexiev I, Beshkov D, Gokengin D, Mezei M, Minarovits J, et al. HIV1 molecular epidemiology in the Balkans: a melting pot for high genetic diversity. AIDS Rev 2012; 14:28-36.
82. He X, Xing H, Ruan Y, Hong K, Cheng C, Hu Y, et al. A comprehensive mapping of HIV-1 genotypes in various risk groups and regions across china based on a nationwide molecular epidemiologic survey. PLoS One 2012; 7:e47289.
83. Neogi U, Bontell I, Shet A, De Costa A, Gupta S, Diwan V, et al. Molecular epidemiology of HIV-1 subtypes in India: origin and evolutionary history of the predominant subtype C. PLoS One 2012; 7:e39819.
84. Lawyer G, Schulter E, Kaiser R, Reuter S, Oette M, Lengauer T. Endogenous or exogenous spreading of HIV-1 in NordrheinWestfalen, Germany, investigated by phylodynamic analysis of the RESINA Study cohort. Med Microbiol Immunol 2012; 201:259-269.
85. Yerly S, Vora S, Rizzardi P, Chave JP, Vernazza PL, Flepp M, et al. Acute HIV infection: impact on the spread of HIV and transmission of drug resistance. AIDS 2001; 15:2287-2292.
86. von Wyl V, Kouyos RD, Yerly S, Boni J, Shah C, Burgisser P, et al. The role of migration and domestic transmission in the spread of HIV-1 non-B subtypes in Switzerland. J Infect Dis 2011; 204:1095-1103.
87. Chemtob D, Grossman Z. Epidemiology of adult and adolescent HIV infection in Israel: a country of immigration. Int J STD AIDS 2004; 15:691-696.
88. Yebra G, de Mulder M, Martin L, Rodriguez C, Labarga P, Viciana I, et al. Most HIV type 1 non-B infections in the Spanish cohort of antiretroviral treatment-naive HIV-infected patients (CoRIS) are due to recombinant viruses. J Clin Microbiol 2012; 50:407-413.
89. Leoz M, Chaix ML, Delaugerre C, Rivoisy C, Meyer L, Rouzioux C, et al. Circulation of multiple patterns of unique recombinant forms B/CRF02-AG in France: precursor signs of the emergence of an upcoming CRF B/02. AIDS 2011; 25:1371-1377.
90. Hughes GJ, Fearnhill E, Dunn D, Lycett SJ, Rambaut A, Leigh Brown AJ. Molecular phylodynamics of the heterosexual HIV epidemic in the United Kingdom. PLoS Pathog 2009; 5:e1000590.
91. Xiridou M, van Veen M, Prins M, Coutinho R. How patterns of migration can influence the heterosexual transmission of HIV in The Netherlands. Sex Transm Infect 2011; 87:289-291.
92. Xiridou M, van Veen M, Coutinho R, Prins M. Can migrants from high-endemic countries cause new HIV outbreaks among heterosexuals in low-endemic countries? AIDS 2010; 24:2081-2088.
93. Lewis F, Hughes GJ, Rambaut A, Pozniak A, Leigh Brown AJ. Episodic sexual transmission of HIV revealed by molecular phylodynamics. PLoS Med 2008; 5:e50.
94. Bezemer D, van Sighem A, Lukashov VV, van der Hoek L, Back N, Schuurman R, et al. Transmission networks of HIV-1 among men having sex with men in the Netherlands. AIDS 2010; 24:271-282.
95. Yerly S, Junier T, Gayet-Ageron A, Amari EB, von Wyl V, Gunthard HF, et al. The impact of transmission clusters on primary drug resistance in newly diagnosed HIV-1 infection. AIDS 2009; 23:1415-1423.
96. Levy I, Mor Z, Anis E, Maayan S, Leshem E, Pollack S, et al. Men who have sex with men, risk behavior, and HIV infection: integrative analysis of clinical, epidemiological, and laboratory databases. Clin Infect Dis 2011; 52:1363-1370.
97. Pao D, Fisher M, Hue S, Dean G, Murphy G, Cane PA, et al. Transmission of HIV-1 during primary infection: relationship to sexual risk and sexually transmitted infections. AIDS 2005; 19:85-90.
98. Hue S, Clewley JP, Cane PA, Pillay D. Investigation of HIV-1 transmission events by phylogenetic methods: requirement for scientific rigour. AIDS 2005; 19:449-450.
99. German D, Sifakis F, Maulsby C, Towe VL, Flynn CP, Latkin CA, et al. Persistently high prevalence and unrecognized HIV infection among men who have sex with men in Baltimore: the BESURE study. J Acquir Immune Defic Syndr 2011; 57:77-87.
100. Paraskevis D, Pybus O, Magiorkinis G, Hatzakis A, Wensing AM, van de Vijver DA, et al. Tracing the HIV-1 subtype B mobility in Europe: a phylogeographic approach. Retrovirology 2009; 6:49.
101. Audelin AM, Cowan SA, Obel N, Nielsen C, Jorgensen LB, Gerstoft J. Phylogenetics of the Danish HIV epidemic: the role of Very Late Presenters in sustaining the epidemic. J Acquir Immune Defic Syndr 2013; 62:102-108.
102. Bezemer D, de Wolf F, Boerlijst MC, van Sighem A, Hollingsworth TD, Prins M, et al. A resurgent HIV-1 epidemic among men who have sex with men in the era of potent antiretroviral therapy. AIDS 2008; 22:1071-1077.
103. Kouyos RD, von Wyl V, Yerly S, Boni J, Taffe P, Shah C, et al. Molecular epidemiology reveals long-term changes in HIV type 1 subtype B transmission in Switzerland. J Infect Dis 2010; 201:1488-1497.
104. Yerly S, von Wyl V, Ledergerber B, Boni J, Schupbach J, Burgisser P, et al. Transmission of HIV-1 drug resistance in Switzerland: a 10-year molecular epidemiology survey. AIDS 2007; 21:2223-2229.
105. Frange P, Meyer L, Deveau C, Tran L, Goujard C, Ghosn J, et al. Recent HIV-1 infection contributes to the viral diffusion over the French territory with a recent increasing frequency. PLoS One 2012; 7:e31695.
106. Dennis AM, Hue S, Hurt CB, Napravnik S, Sebastian J, Pillay D, et al. Phylogenetic insights into regional HIV transmission. AIDS 2012; 26:1813-1822.
107. Aldous JL, Pond SK, Poon A, Jain S, Qin H, Kahn JS, et al. Characterizing HIV transmission networks across the United States. Clin Infect Dis 2012; 55:1135-1143.
108. Ambrosioni J, Junier T, Delhumeau C, Calmy A, Hirschel B, Zdobnov E, et al. Impact of HAART on the molecular epidemiology of newly diagnosed HIV infections in Geneva, Switzerland. AIDS 2012; 26:2079-2086.
109. Dennis AM, Hue S, Hurt CB, Napravnik S, Sebastian J, Pillay D, et al. Phylogenetic insights into HIV transmission in North Carolina. AIDS 2012; 26:1813-1822.
110. Ragonnet-Cronin M, Ofner-Agostini M, Merks H, Pilon R, Rekart M, Archibald CP, et al. Longitudinal phylogenetic surveillance identifies distinct patterns of cluster dynamics. J Acquir Immune Defic Syndr 2010; 55:102-108.
111. Chalmet K, Staelens D, Blot S, Dinakis S, Pelgrom J, Plum J, et al. Epidemiological study of phylogenetic transmission clusters in a local HIV-1 epidemic reveals distinct differences between subtype B and non-B infections. BMC Infect Dis 2010; 10:262.
112. Volz EM, Koopman JS, Ward MJ, Brown AL, Frost SD. Simple epidemiological dynamics explain phylogenetic clustering of HIV from patients with recent infection. PLoS Comput Biol 2012; 8:e1002552.
113. Pilcher CD, Joaki G, Hoffman IF, Martinson FE, Mapanje C, Stewart PW, et al. Amplified transmission of HIV-1: comparison of HIV-1 concentrations in semen and blood during acute and chronic infection. AIDS 2007; 21:1723-1730.
114. Redd AD, Collinson-Streng AN, Chatziandreou N, Mullis CE, Laeyendecker O, Martens C, et al. Previously transmitted HIV-1 strains are preferentially selected during subsequent sexual transmissions. J Infect Dis 2012; 206:1433-1442.
115. Sifakis F, Flynn CP, Metsch L, LaLota M, Murrill C, Koblin BA, et al. HIV prevalence, unrecognized infection, and HIV testing among men who have sex with men: five U.S. cities, June 2004-April 2005. MMWR Morb Mortal Wkly Rep 2005; 54:597-601.
116. Hernandez HL, Prejean J, Doshani M, Linley L, Ziebell R, Branson BM, et al. Previous HIV testing among adults and adolescents newly diagnosed with HIV infection: National HIV Surveillance System, 18 Jurisdictions, United States, 2006-2009. MMWR Morb Mortal Wkly Rep 2012; 61:441-445.
117. Marks G, Crepaz N, Janssen RS. Estimating sexual transmission of HIV from persons aware and unaware that they are infected with the virus in the USA. AIDS 2006; 20:1447-1450.
118. Lauby JL, Millett GA, LaPollo AB, Bond L, Murrill CS, Marks G. Sexual risk behaviors of HIV-positive, HIV-negative, and serostatus-unknown Black men who have sex with men and women. Arch Sex Behav 2008; 37:708-719.
119. Dawson JM, Fitzpatrick RM, Reeves G, Boulton M, McLean J, Hart GJ, et al. Awareness of sexual partners' HIV status as an influence upon high-risk sexual behaviour among gay men. AIDS 1994; 8:837-841.
120. Lavoie E, Alary M, Remis RS, Otis J, Vincelette J, Turmel B, et al. Determinants of HIV seroconversion among men who have sex with men living in a low HIV incidence population in the era of highly active antiretroviral therapies. Sex Transm Dis 2008; 35:25-29.
121. Cohen MS, Fidler S. HIV prevention 2010: where are we now and where are we going? Curr Opin HIV AIDS 2010; 5:265-268.
122. Powers KA, Ghani AC, Miller WC, Hoffman IF, Pettifor AE, Kamanga G, et al. The role of acute and early HIV infection in the spread of HIV and implications for transmission prevention strategies in Lilongwe, Malawi: a modelling study. Lancet 2011; 378:256-268.
123. Fisher M, Pao D, Brown AE, Sudarshi D, Gill ON, Cane P, et al. Determinants of HIV-1 transmission in men who have sex with men: a combined clinical, epidemiological and phylo-genetic approach. AIDS 2010; 24:1739-1747.
124. Jacquez JA, Koopman JS, Simon CP, Longini IM Jr. Role of the primary infection in epidemics of HIV infection in gay cohorts. J Acquir Immune Defic Syndr 1994; 7:1169-1184.
125. Kim JH, Riolo RL, Koopman JS. HIV transmission by stage of infection and pattern of sexual partnerships. Epidemiology 2010; 21:676-684.
126. Miller WC, Rosenberg NE, Rutstein SE, Powers KA. Role of acute and early HIV infection in the sexual transmission of HIV. Curr Opin HIV AIDS 2010; 5:277-282.
127. Pilcher CD, Christopoulos KA, Golden M. Public health rationale for rapid nucleic acid or p24 antigen tests for HIV. J Infect Dis 2010; 201 (Suppl 1):S7-S15.
128. Poon AF, McGovern RA, Mo T, Knapp DJ, Brenner B, Routy JP, et al. Dates of HIV infection can be estimated for seroprevalent patients by coalescent analysis of serial next-generation sequencing data. AIDS 2011; 25:2019-2026.
129. Kouyos RD, von Wyl V, Yerly S, Boni J, Rieder P, Joos B, et al. Ambiguous nucleotide calls from population-based sequencing of HIV-1 are a marker for viral diversity and the age of infection. Clin Infect Dis 2011; 52:532-539.
130. Rosenberg NE, Kamanga G, Phiri S, Nsona D, Pettifor A, Rutstein SE, et al. Detection of acute HIV infection: a field evaluation of the determine(R) HIV-1/2 Ag/Ab combo test. J Infect Dis 2012; 205:528-534.
131. Branson BM, Stekler JD. Detection of acute HIV infection: we can't close the window. J Infect Dis 2012; 205:521-524.
132. Giorgi EE, Funkhouser B, Athreya G, Perelson AS, Korber BT, Bhattacharya T. Estimating time since infection in early homogeneous HIV-1 samples using a poisson model. BMC Bioinfor-matics 2010; 11:532.
133. Maldarelli F, Shao W, Dewar R, Rehman T, Kearney M, Rehm C, et al. New bioinformatic algorithm to identify recent HIV-1 infection. Antiviral Ther 2010; 15:A97.
134. Yang J, Xia X, He X, Yang S, Ruan Y, Zhao Q, et al. A new pattern-based method for identifying recent HIV-1 infections from the viral env sequence. Sci China Life Sci 2012; 55:328-335.
135. Cousins MM, Ou SS, Wawer MJ, Munshaw S, Swan D, Magaret CA, et al. Comparison of a high-resolution melting assay to next-generation sequencing for analysis of HIV diversity. J Clin Microbiol 2012; 50:3054-3059.
136. Rieder P, Joos B, von Wyl V, Kuster H, Grube C, Leemann C, et al. HIV-1 transmission after cessation of early antiretroviral therapy among men having sex with men. AIDS 2010; 24:1177-1183.
137. Volz E, Frost SD, Rothenberg R, Meyers LA. Epidemiological bridging by injection drug use drives an early HIV epidemic. Epidemics 2010; 2:155-164.
138. Tagliamonte M, Naderi HR, Tornesello ML, Farid R, Buonaguro FM, Buonaguro L. HIV type 1 subtype A epidemic in injecting drug user (IDU) communities in Iran. AIDS Res Hum Retroviruses 2007; 23:1569-1574.
139. Balode D, Skar H, Mild M, Kolupajeva T, Ferdats A, Rozentale B, et al. Phylogenetic analysis of the Latvian HIV-1 epidemic. AIDS Res Hum Retroviruses 2012; 28:928-932.
140. Perez-Losada M, Jobes DV, Sinangil F, Crandall KA, Arenas M, Posada D, et al. Phylodynamics of HIV-1 from a phase III AIDS vaccine trial in Bangkok, Thailand. PLoS One 2011; 6:e16902.
141. Chen JH, Wong KH, Chan KC, To SW, Chen Z, Yam WC. Phylodynamics of HIV-1 subtype B among the men-having-sex-with-men (MSM) population in Hong Kong. PLoS One 2011; 6:e25286.
142. Kao CF, Chang SY, Hsia KT, Chang FY, Yang CH, Liu HR, et al. Surveillance of HIV type 1 recent infection and molecular epidemiology among different risk behaviors between 2007 and 2009 after the HIV type1 CRF07-BC outbreak in Taiwan. AIDS Res Hum Retroviruses 2011; 27:745-749.
143. Lemstra M, Rogers M, Thompson A, Moraros J, Buckingham R. Risk indicators associated with injection drug use in the Aboriginal population. AIDS Care 2012.
144. Martin LJ, Houston S, Yasui Y, Wild TC, Saunders LD. All-cause and HIV-related mortality rates among HIV-infected patients after initiating highly active antiretroviral therapy: the impact of Aboriginal ethnicity and injection drug use. Can J Public Health 2011; 102:90-96.
145. Chen JH, Wong KH, Li P, Chan KC, Lee MP, Lam HY, et al. Molecular epidemiological study of HIV-1 CRF01-AE transmission in Hong Kong. J Acquir Immune Defic Syndr 2009; 51:530-535.
146. Pilon R, Leonard L, Kim J, Vallee D, De Rubeis E, Jolly AM, et al. Transmission patterns of HIV and hepatitis C virus among networks of people who inject drugs. PLoS One 2011; 6:e22245.
147. Ciccozzi M, Lai A, Ebranati E, Gabanelli E, Galli M, Mugosa B, et al. Phylogeographic reconstruction of HIV type 1B in Montenegro and the Balkan Region. AIDS Res Hum Retroviruses 2012.
148. Bernini F, Ebranati E, De Maddalena C, Shkjezi R, Milazzo L, Lo Presti A, et al. Within-host dynamics of the hepatitis C virus quasispecies population in HIV-1/HCV coinfected patients. PLoS One 2011; 6:e16551.
149. Masharsky AE, Dukhovlinova EN, Verevochkin SV, Toussova OV, Skochilov RV, Anderson JA, et al. A substantial transmission bottleneck among newly and recently HIV-1-infected injection drug users in St Petersburg, Russia. J Infect Dis 2010; 201:1697-1702.
150. Yerly S, Rickenbach M, Popescu M, Taffe P, Craig C, Perrin L. Drug resistance mutations in HIV-1-infected subjects during protease inhibitor-containing highly active antiretroviral therapy with nelfinavir or indinavir. Antivir Ther 2001; 6:185-189.
151. Hilton BA, Thompson R, Moore-Dempsey L, Janzen RG. Harm reduction theories and strategies for control of human immunodeficiency virus: a review of the literature. J Adv Nurs 2001; 33:357-370.
152. Duri K, Gumbo F, Kristiansen K, Mapingure M, Munjoma M, Chirenje M, et al. Phylogenetic analysis of human immunodeficiency virus type1subtypeCenv gp120 sequences among four drug-naive families following subsequent heterosexual and vertical transmissions. AIDS Res Hum Retroviruses 2012; 28:885-893.
153. Novitsky V, Wang R, Margolin L, Baca J, Rossenkhan R, Moyo S, et al. Transmission of single and multiple viral variants in primary HIV-1 subtype C infection. PLoS One 2011; 6:e16714.
154. Novitsky V, Wang R, Bussmann H, Lockman S, Baum M, Shapiro R, et al. HIV-1 subtype C-infected individuals maintaining high viral load as potential targets for the 'test-and-treat' approach to reduce HIV transmission. PLoS One 2010; 5:e10148.
155. Koopman JS, Jacquez JA, Welch GW, Simon CP, Foxman B, Pollock SM, et al. The role of early HIV infection in the spread of HIV through populations. J Acquir Immune Defic Syndr Hum Retrovirol 1997; 14:249-258.
156. Hollingsworth TD, Anderson RM, Fraser C. HIV-1 transmission, by stage of infection. J Infect Dis 2008; 198:687-693.
157. Trask SA, Derdeyn CA, Fideli U, Chen Y, Meleth S, Kasolo F, et al. Molecular epidemiology of human immunodeficiency virus type 1 transmission in a heterosexual cohort of discordant couples in Zambia. J Virol 2002; 76:397-405.
158. Gray RH, Wawer MJ. Probability of heterosexual HIV-1 transmission per coital act in sub-Saharan Africa. J Infect Dis 2012; 205:351-352.
159. Eshleman SH, Hudelson SE, Redd AD, Wang L, Debes R, Chen YQ, et al. Analysis of genetic linkage of HIV from couples enrolled in the HIV Prevention Trials Network 052 trial. J Infect Dis 2011; 204:1918-1926.
160. Campbell MS, Mullins JI, Hughes JP, Celum C, Wong KG, Raugi DN, et al. Viral linkage in HIV-1 seroconverters and their partners in an HIV-1 prevention clinical trial. PLoS One 2011; 6:e16986.
161. Jain V, Liegler T, Vittinghoff E, Hartogensis W, Bacchetti P, Poole L, et al. Transmitted drug resistance in persons with acute/early HIV-1 in San Francisco, 2002-2009. PLoS One 2010; 5:e15510.
162. Brenner BG, Roger M, Moisi DD, Oliveira M, Hardy I, Turgel R, et al. Transmission networks of drug resistance acquired in primary/early stage HIV infection. AIDS 2008; 22:2509-2515.
163. Hue S, Gifford RJ, Dunn D, Fernhill E, Pillay D. Demonstration of sustained drug-resistant human immunodeficiency virus type 1 lineages circulating among treatment-naive individuals. J Virol 2009; 83:2645-2654.
164. Vercauteren J, Wensing AM, van de Vijver DA, Albert J, Balotta C, Hamouda O, et al. Transmission of drug-resistant HIV-1 is stabilizing in Europe. J Infect Dis 2009; 200:1503-1508.
165. Wittkop L, Gunthard HF, de Wolf F, Dunn D, Cozzi-Lepri A, de Luca A, et al. Effect of transmitted drug resistance on virological and immunological response to initial combination antiretroviral therapy for HIV (EuroCoord-CHAIN joint project): a European multicohort study. Lancet Infect Dis 2011; 11:363-371.
166. Brenner B, Turner D, Oliveira M, Moisi D, Detorio M, Carobene M, et al. A V106M mutation in HIV-1 clade C viruses exposed to efavirenz confers cross-resistance to nonnucleoside reverse transcriptase inhibitors. Aids 2003; 17:F1-F5.
167. Grossman Z, Istomin V, Averbuch D, Lorber M, Risenberg K, Levi I, et al. Genetic variation at NNRTI resistance-associated positions in patients infected with HIV-1 subtype C. AIDS 2004; 18:909-915.
168. Charpentier C, Gody JC, Tisserand P, Matta M, Pere H, Fournier J, et al. Surveillance of antiretroviral drug resistance mutations in untreated young children living in the Central African Republic. Antivir Ther 2011; 16:1347-1350.
169. Tshabalala M, Manasa J, Zijenah LS, Rusakaniko S, Kadzirange G, Mucheche M, et al. Surveillance of transmitted antiretroviral drug resistance among HIV-1 infected women attending antenatal clinics in Chitungwiza, Zimbabwe. PLoS One 2011; 6:e21241.
170. Brenner BG, Coutsinos D. The K65R mutation in HIV-1 reverse transcriptase: genetic barriers, resistance profile and clinical implications. HIV Ther 2009; 3:583-594.
171. Brenner BG, Oliveira M, Doualla-Bell F, Moisi DD, Ntemgwa M, Frankel F, et al. HIV-1 subtype C viruses rapidly develop K65R resistance to tenofovir in cell culture. AIDS 2006; 20:F9-F13.
172. Castor D, Low A, Evering T, Karmon S, Davis B, Figueroa A, et al. Transmitted drug resistance and phylogenetic relationships among acute and early HIV-1 infected individuals in New York City. J Acquir Immune Defic Syndr 2012.
173. Castro E, Khonkarly M, Ciuffreda D, Burgisser P, Cavassini M, Yerly S, et al. HIV-1 drug resistance transmission networks in southwest Switzerland. AIDS Res Hum Retroviruses 2010; 26:1233-1238.
174. Bennett DE, Camacho RJ, Otelea D, Kuritzkes DR, Fleury H, Kiuchi M, et al. Drug resistance mutations for surveillance of transmitted HIV-1 drug-resistance: 2009 update. PLoS One 2009; 4:e4724.
175. van de Vijver DA, Wensing AM, Angarano G, Asjo B, Balotta C, Boeri E, et al. The calculated genetic barrier for antire-troviral drug resistance substitutions is largely similar for different HIV-1 subtypes. J Acquir Immune Defic Syndr 2006; 41:352-360.
176. Grgic I, Lepej SZ, Lunar MM, Poljak M, Vince A, Vrakela IB, et al. The prevalence of transmitted drug resistance in newly diagnosed HIV-infected individuals in Croatia: the role of transmission clusters of men who have sex with men carrying the T215S surveillance drug resistance mutation. AIDS Res Hum Retroviruses 2012; [Epub ahead of print].
177. Buskin SE, Ellis GM, Pepper GG, Frenkel LM, Pergam SA, Gottlieb GS, et al. Transmission cluster of multiclass highly drug-resistant HIV-1 among 9 men who have sex with men in Seattle/King County, WA, 2005-2007. J Acquir Immune Defic Syndr 2008; 49:205-211.
178. Stolte IG, de Wit JB, Kolader ME, Fennema HS, Coutinho RA, Dukers NH. Low HIV-testing rates among younger high-risk homosexual men in Amsterdam. Sex Transm Infect 2007; 83:387-391.
179. Brenner B, Moodie E, Otis J, Ohnona F, Wainberg MA, Rousseau R, et al. Phylogenetic analysis of the SPOT cohort reveals risk determinants implicated in the spread of the Montreal Male-Sex-Male (MSM) epidemic. Can J Infect Dis Med Microbiol 2012; 23:79.
180. Le Vu S, Velter A, Meyer L, Peytavin G, Guinard J, Pillonel J, et al. Biomarker-based HIV incidence in a community sample of men who have sex with men in Paris, France. PLoS One 2012; 7:e39872.
181. Alam SJ, Romero-Severson E, Kim JH, Emond G, Koopman JS. Dynamic sex roles among men who have sex with men and transmissions from primary HIV infection. Epidemiology 2010; 21:669-675.
182. Bezemer D, de Wolf F, Boerlijst MC, van Sighem A, Hollings-worth TD, Fraser C. 27 years of the HIV epidemic amongst men having sex with men in the Netherlands: an in depth mathematical model-based analysis. Epidemics 2010; 2:66-79.
183. Chen M, Rhodes PH, Hall IH, Kilmarx PH, Branson BM, Valleroy LA. Prevalence of undiagnosed HIV infection among persons aged >/=13 years: National HIV Surveillance System, United States, 2005-2008. MMWR Surveill Summ 2012; 61:57-64.
184. Oster AM, Wiegand RE, Sionean C, Miles IJ, Thomas PE, Melendez-Morales L, et al. Understanding disparities in HIV infection between black and white MSM in the United States. AIDS 2011; 25:1103-1112.
185. Ayala G, Bingham T, Kim J, Wheeler DP, Millett GA. Modeling the impact of social discrimination and financial hardship on the sexual risk of HIV among Latino and Black men who have sex with men. Am J Public Health 2012; 102 (Suppl 2):S242 - S249.
186. Aldous JL, Pond SK, Poon A, Jain S, Qin H, Kahn JS, et al. Characterizing HIV transmission networks across the United States. Clin Infect Dis 2012.
187. Oster AM, Pieniazek D, Zhang X, Switzer WM, Ziebell RA, Mena LA, et al. Demographic but not geographic insularity in HIV transmission among young black MSM. AIDS 2011; 25:2157-2165.