Timing and source of subtype-C HIV-1 superinfection in the newly infected partner of Zambian couples with disparate viruses

Retrovirology

Volumn 9, Issue , 2012, Pages

  Kraft, Colleen S ^a   Basu, Debby ^a   Hawkins, Paulina A ^a   Hraber, Peter T ^b   Chomba, Elwyn ^c   Mulenga, Joseph ^c   Kilembe, William ^c   Khu, Naw H ^d   Derdeyn, Cynthia A ^a   Allen, Susan A ^c,d,e   Manigart, Olivier ^d   Hunter, Eric ^a  

^a EMORY UNIVERSITY   (United States)

^b LOS ALAMOS NATIONAL LABORATORY   (United States)

^c ZEHRP   (Zambia)

^d EMORY UNIVERSITY   (United States)

^e RZHRG   (Rwanda)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN GP 41; GP41 PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1;

ADULT; AMINO ACID SEQUENCE; ARTICLE; CLINICAL ARTICLE; COHORT ANALYSIS; ENVELOPE GENE; ETHNIC GROUP; FEMALE; GENE AMPLIFICATION; GENE SEQUENCE; GENETIC RECOMBINATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN RELATION; INCIDENCE; MALE; NONHUMAN; PHYLOGENY; SEROCONVERSION; SUPERINFECTION; VIREMIA; VIRUS GENOME; ZAMBIAN; CLASSIFICATION; DNA SEQUENCE; FAMILY SIZE; GENETICS; GENOTYPE; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; ISOLATION AND PURIFICATION; MIXED INFECTION; MOLECULAR EPIDEMIOLOGY; MOLECULAR GENETICS; TIME; VIROLOGY; ZAMBIA;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ADULT; COINFECTION; FAMILY CHARACTERISTICS; GENOTYPE; HIV ENVELOPE PROTEIN GP41; HIV INFECTIONS; HIV-1; HUMANS; INCIDENCE; MALE; MOLECULAR EPIDEMIOLOGY; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA; TIME FACTORS; ZAMBIA;

EID: 84858411581     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-9-22     Document Type: Article

References (60)

1. Chohan BH, Piantadosi A, Overbaugh J. HIV-1 Superinfection and its Implications for Vaccine Design. Curr HIV Res 2010, 8:596-601. 10.2174/157016210794088218, 21054252.
2. Allen TM, Altfeld M. HIV-1 superinfection. J Allergy Clin Immunol 2003, 112:829-835. 10.1016/j.jaci.2003.08.037, 14610465.
3. van der Kuyl AC, Cornelissen M. Identifying HIV-1 dual infections. Retrovirology 2007, 4:67. 10.1186/1742-4690-4-67, 2045676, 17892568.
4. Jost S, Bernard MC, Kaiser L, Yerly S, Hirschel B, Samri A, Autran B, Goh LE, Perrin L. A patient with HIV-1 superinfection. N Engl J Med 2002, 347:731-736. 10.1056/NEJMoa020263, 12213944.
5. Chohan B, Lavreys L, Rainwater SM, Overbaugh J. Evidence for frequent reinfection with human immunodeficiency virus type 1 of a different subtype. J Virol 2005, 79:10701-10708. 10.1128/JVI.79.16.10701-10708.2005, 1182664, 16051862.
6. Gottlieb GS, Nickle DC, Jensen MA, Wong KG, Kaslow RA, Shepherd JC, Margolick JB, Mullins JI. HIV type 1 superinfection with a dual-tropic virus and rapid progression to AIDS: a case report. Clin Infect Dis 2007, 45:501-509. 10.1086/520024, 17638203.
7. Hu DJ, Subbarao S, Vanichseni S, Mock PA, Ramos A, Nguyen L, Chaowanachan T, Griensven F, Choopanya K, Mastro TD, Tappero JW. Frequency of HIV-1 dual subtype infections, including intersubtype superinfections, among injection drug users in Bangkok, Thailand. AIDS 2005, 19:303-308.
8. Manigart O, Courgnaud V, Sanou O, Valea D, Nagot N, Meda N, Delaporte E, Peeters M, Van de Perre P. HIV-1 superinfections in a cohort of commercial sex workers in Burkina Faso as assessed by an autologous heteroduplex mobility procedure. AIDS 2004, 18:1645-1651. 10.1097/01.aids.0000131333.30548.db, 15280775.
9. McCutchan FE, Hoelscher M, Tovanabutra S, Piyasirisilp S, Sanders-Buell E, Ramos G, Jagodzinski L, Polonis V, Maboko L, Mmbando D, 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, 79:11693-11704. 10.1128/JVI.79.18.11693-11704.2005, 1212589, 16140747.
10. Ramos A, Hu DJ, Nguyen L, Phan KO, Vanichseni S, Promadej N, Choopanya K, Callahan M, Young NL, McNicholl J, et al. Intersubtype human immunodeficiency virus type 1 superinfection following seroconversion to primary infection in two injection drug users. J Virol 2002, 76:7444-7452. 10.1128/JVI.76.15.7444-7452.2002, 136380, 12097556.
11. van der Kuyl AC, Kozaczynska K, van den Burg R, Zorgdrager F, Back N, Jurriaans S, Berkhout B, Reiss P, Cornelissen M. Triple HIV-1 infection. N Engl J Med 2005, 352:2557-2559. 10.1056/NEJM200506163522420, 15958817.
12. Yerly S, Jost S, Monnat M, Telenti A, Cavassini M, Chave JP, Kaiser L, Burgisser P, Perrin L. HIV-1 co/super-infection in intravenous drug users. AIDS 2004, 18:1413-1421. 10.1097/01.aids.0000131330.28762.0c, 15199317.
13. Plantier JC, Lemee V, Dorval I, Gueudin M, Braun J, Hutin P, Ruffault A, Simon F. HIV-1 group M superinfection in an HIV-1 group O-infected patient. AIDS 2004, 18:2444-2446.
14. Altfeld M, Allen TM, Yu XG, Johnston MN, Agrawal D, Korber BT, Montefiori DC, O'Connor DH, Davis BT, Lee PK, et al. HIV-1 superinfection despite broad CD8+ T-cell responses containing replication of the primary virus. Nature 2002, 420:434-439. 10.1038/nature01200, 12459786.
15. Gottlieb GS, Nickle DC, Jensen MA, Wong KG, Grobler J, Li F, Liu SL, Rademeyer C, Learn GH, Karim SS, et al. Dual HIV-1 infection associated with rapid disease progression. Lancet 2004, 363:619-622. 10.1016/S0140-6736(04)15596-7, 14987889.
16. Koelsch KK, Smith DM, Little SJ, Ignacio CC, Macaranas TR, Brown AJ, Petropoulos CJ, Richman DD, Wong JK. Clade B HIV-1 superinfection with wild-type virus after primary infection with drug-resistant clade B virus. AIDS 2003, 17:F11-F16. 10.1097/00002030-200305020-00001, 12700477.
17. Smith DM, Wong JK, Hightower GK, Ignacio CC, Koelsch KK, Daar ES, Richman DD, Little SJ. Incidence of HIV superinfection following primary infection. Jama 2004, 292:1177-1178. 10.1001/jama.292.10.1177, 15353529.
18. Chakraborty B, Valer L, De Mendoza C, Soriano V, Quinones-Mateu ME. Failure to detect human immunodeficiency virus type 1 superinfection in 28 HIV-seroconcordant individuals with high risk of reexposure to the virus. AIDS Res Hum Retroviruses 2004, 20:1026-1031. 10.1089/aid.2004.20.1026, 15585092.
19. Gonzales MJ, Delwart E, Rhee SY, Tsui R, Zolopa AR, Taylor J, Shafer RW. Lack of detectable human immunodeficiency virus type 1 superinfection during 1072 person-years of observation. J Infect Dis 2003, 188:397-405. 10.1086/376534, 2547470, 12870121.
20. Tsui R, Herring BL, Barbour JD, Grant RM, Bacchetti P, Kral A, Edlin BR, Delwart EL. Human immunodeficiency virus type 1 superinfection was not detected following 215 years of injection drug user exposure. J Virol 2004, 78:94-103. 10.1128/JVI.78.1.94-103.2004, 303392, 14671091.
21. Rachinger A, Manyenga P, Burger JA, de Ven TLPDV, Stolte IG, Prins M, van't Wout AB, Schuitemaker H. Low incidence of HIV-1 superinfection even after episodes of unsafe sexual behavior of homosexual Men in the Amsterdam cohort studies on HIV infection and AIDS. J Infect Dis 2011, 203:1621-1628. 10.1093/infdis/jir164, 21592992.
22. Rachinger A, van de Ven TD, Burger JA, Schuitemaker H, Schuitemaker H, van't Wout AB. Evaluation of pre-screening methods for the identification of HIV-1 superinfection. J Virol Methods 2010, 165:311-317. 10.1016/j.jviromet.2010.02.016, 20178816.
23. Willberg CB, McConnell JJ, Eriksson EM, Bragg LA, York VA, Liegler TJ, Hecht FM, Grant RM, Nixon DF. Immunity to HIV-1 is influenced by continued natural exposure to exogenous virus. PLoS Pathog 2008, 4:e1000185. 10.1371/journal.ppat.1000185, 2562513, 18949024.
24. Blish CA, Dogan OC, Derby NR, Nguyen MA, Chohan B, Richardson BA, Overbaugh J. Human immunodeficiency virus type 1 superinfection occurs despite relatively robust neutralizing antibody responses. J Virol 2008, 82:12094-12103. 10.1128/JVI.01730-08, 2593335, 18842728.
25. Bragg L, McConnell J, Liegler T, Bacchetti P, Spotts G, Hecht F, Grant R. HIV-1 suoerinfection surveillence in an acute infection cohort using pol sequences from resistance genotyping: 1996-200. 2010, California: In Conference on Retoviruses and Opportunistic Infections; San Francisco.
26. Piantadosi A, Chohan B, Chohan V, McClelland RS, Overbaugh J. Chronic HIV-1 infection frequently fails to protect against superinfection. PLoS Pathog 2007, 3:e177. 10.1371/journal.ppat.0030177, 2077901, 18020705.
27. Smith DM, Strain MC, Frost SD, Pillai SK, Wong JK, Wrin T, Liu Y, Petropolous CJ, Daar ES, Little SJ, Richman DD. Lack of neutralizing antibody response to HIV-1 predisposes to superinfection. Virology 2006, 355:1-5. 10.1016/j.virol.2006.08.009, 16962152.
28. Blick G, Kagan RM, Coakley E, Petropoulos C, Maroldo L, Greiger-Zanlungo P, Gretz S, Garton T. The probable source of both the primary multidrug-resistant (MDR) HIV-1 strain found in a patient with rapid progression to AIDS and a second recombinant MDR strain found in a chronically HIV-1-infected patient. J Infect Dis 2007, 195:1250-1259. 10.1086/512240, 17396993.
29. Chakraborty B, Kiser P, Rangel HR, Weber J, Mirza M, Marotta ML, Asaad R, Rodriguez B, Valdez H, Lederman MM, Quinones-Mateu ME. Can HIV-1 superinfection compromise antiretroviral therapy?. AIDS 2004, 18:132-134.
30. Smith DM, Wong JK, Hightower GK, Ignacio CC, Koelsch KK, Petropoulos CJ, Richman DD, Little SJ. HIV drug resistance acquired through superinfection. AIDS 2005, 19:1251-1256. 10.1097/01.aids.0000180095.12276.ac, 16052079.
31. Grobler J, Gray CM, Rademeyer C, Seoighe C, Ramjee G, Karim SA, Morris L, Williamson C. 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, 190:1355-1359. 10.1086/423940, 15346349.
32. Sagar M, Lavreys L, Baeten JM, Richardson BA, Mandaliya K, Chohan BH, Kreiss JK, Overbaugh J. Infection with multiple human immunodeficiency virus type 1 variants is associated with faster disease progression. J Virol 2003, 77:12921-12926. 10.1128/JVI.77.23.12921-12926.2003, 262567, 14610215.
33. Taylor BS, Sobieszczyk ME, McCutchan FE, Hammer SM. The challenge of HIV-1 subtype diversity. N Engl J Med 2008, 358:1590-1602. 10.1056/NEJMra0706737, 2614444, 18403767.
34. Gross KL, Porco TC, Grant RM. HIV-1 superinfection and viral diversity. AIDS 2004, 18:1513-1520. 10.1097/01.aids.0000131361.75328.47, 15238769.
35. Taylor JE, Korber BT. HIV-1 intra-subtype superinfection rates: estimates using a structured coalescent with recombination. Infect Genet Evol 2005, 5:85-95.
36. Streeck H, Li B, Poon AFY, Schneidewind A, Gladden AD, Power KA, Daskalakis D, Bazner S, Zuniga R, Brander C, et al. Immune-driven recombination and loss of control after HIV superinfection. J Exp Med 2008, 205:1789-1796. 10.1084/jem.20080281, 2525594, 18625749.
37. Allen S, Meinzen-Derr J, Kautzman M, Zulu I, Trask S, Fideli U, Musonda R, Kasolo F, Gao F, Haworth A. Sexual behavior of HIV discordant couples after HIV counseling and testing. AIDS 2003, 17:733-740. 10.1097/00002030-200303280-00012, 12646797.
38. Allen S, Serufilira A, Bogaerts J, Van de Perre P, Nsengumuremyi F, Lindan C, Carael M, Wolf W, Coates T, Hulley S. Confidential HIV testing and condom promotion in Africa. Impact on HIV and gonorrhea rates. JAMA 1992, 268:3338-3343. 10.1001/jama.1992.03490230068030, 1453526.
39. Fideli US, Allen SA, Musonda R, Trask S, Hahn BH, Weiss H, Mulenga J, Kasolo F, Vermund SH, Aldrovandi GM. Virologic and immunologic determinants of heterosexual transmission of human immunodeficiency virus type 1 in Africa. AIDS Res Hum Retroviruses 2001, 17:901-910. 10.1089/088922201750290023, 2748905, 11461676.
40. Dunkle KL, Stephenson R, Karita E, Chomba E, Kayitenkore K, Vwalika C, Greenberg L, Allen S. New heterosexually transmitted HIV infections in married or cohabiting couples in urban Zambia and Rwanda: an analysis of survey and clinical data. Lancet 2008, 371:2183-2191. 10.1016/S0140-6736(08)60953-8, 18586173.
41. Trask SA, Derdeyn CA, Fideli U, Chen Y, Meleth S, Kasolo F, Musonda R, Hunter E, Gao F, Allen S, Hahn BH. Molecular epidemiology of human immunodeficiency virus type 1 transmission in a heterosexual cohort of discordant couples in Zambia. J Virol 2002, 76:397-405. 10.1128/JVI.76.1.397-405.2002, 135722, 11739704.
42. Haaland RE, Hawkins PA, Salazar-Gonzalez J, Johnson A, Tichacek A, Karita E, Manigart O, Mulenga J, Keele BF, Shaw GM, 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. 10.1371/journal.ppat.1000274, 2621345, 19165325.
43. Salazar-Gonzalez JF, Bailes E, Pham KT, Salazar MG, Guffey MB, Keele BF, Derdeyn CA, Farmer P, Hunter E, Allen S, 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. 10.1128/JVI.02660-07, 2293010, 18256145.
44. Piantadosi A, Ngayo MO, Chohan B, Overbaugh J. Examination of a second region of the HIV type 1 genome reveals additional cases of superinfection. AIDS Res Hum Retroviruses 2008, 24:1221. 10.1089/aid.2008.0100, 2743231,2743231, 18729772.
45. Derdeyn CA, Decker JM, Bibollet-Ruche F, Mokili JL, Muldoon M, Denham SA, Heil ML, Kasolo F, Musonda R, Hahn BH, et al. Envelope-constrained neutralization-sensitive HIV-1 after heterosexual transmission. Science 2004, 303:2019-2022. 10.1126/science.1093137, 15044802.
46. Keele BF, Giorgi EE, Salazar-Gonzalez JF, Decker JM, Pham KT, Salazar MG, Sun C, Grayson T, Wang S, Li H, 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. 10.1073/pnas.0802203105, 2387184, 18490657.
47. Blish CA, Blay WM, Haigwood NL, Overbaugh J. Transmission of HIV-1 in the face of neutralizing antibodies. Curr HIV Res 2007, 5:578-587. 10.2174/157016207782418461, 18045114.
48. Redd AD, Collinson-Streng A, Martens C, Ricklefs S, Mullis CE, Manucci J, Tobian AAR, Selig EJ, Laeyendecker O, Sewankambo N, et al. Identification of HIV superinfection in seroconcordant couples in Rakai, Uganda, by Use of next-generation deep sequencing. J Clin Microbiol 2011, 49:2859-2867. 10.1128/JCM.00804-11, 3147722, 21697329.
49. Roest RW, Maertzdorf J, Kant M, van der Meijden WI, Osterhaus ADME, Verjans GMGM. High incidence of genotypic variance between sequential herpes simplex virus type 2 isolates from HIV-1-seropositive patients with recurrent genital herpes. J Infect Dis 2006, 194:1115-1118. 10.1086/507683, 16991086.
50. Wawer MJ, Gray RH, Sewankambo NK, Serwadda D, Li X, Laeyendecker O, Kiwanuka N, Kigozi G, Kiddugavu M, Lutalo T, 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. 10.1086/429411, 15809897.
51. Merino A, Malhotra R, Morton M, Mulenga J, Allen S, Hunter E, Tang J, Kaslow RA. Impact of a functional KIR2DS4 allele on heterosexual HIV-1 transmission among discordant Zambian couples. J Infect Dis 2011, 203:487-495. 10.1093/infdis/jiq075, 3071217, 21216870.
52. Song W, He D, Brill I, Malhotra R, Mulenga J, Allen S, Hunter E, Tang J, Kaslow RA. Disparate associations of HLA class I markers with HIV-1 acquisition and control of viremia in an African population. PLoS One 2011, 6:e23469. 10.1371/journal.pone.0023469, 3157381, 21858133.
53. Tang J, Shao W, Yoo YJ, Brill I, Mulenga J, Allen S, Hunter E, Kaslow RA. Human leukocyte antigen class I genotypes in relation to heterosexual HIV type 1 transmission within discordant couples. J Immunol 2008, 181:2626-2635. 2570252, 18684953.
54. McKenna SL, Muyinda GK, Roth D, Mwali M, Ng'andu N, Myrick A, Luo C, Priddy FH, Hall VM, von Lieven AA, et al. Rapid HIV testing and counseling for voluntary testing centers in Africa. AIDS 1997, 11(Suppl 1):S103-S110.
55. Allen S, Karita E, Chomba E, Roth DL, Telfair J, Zulu I, Clark L, Kancheya N, Conkling M, Stephenson R, et al. Promotion of couples' voluntary counselling and testing for HIV through influential networks in two African capital cities. BMC Publ Health 2007, 7:349.
56. Kempf MC, Allen S, Zulu I, Kancheya N, Stephenson R, Brill I, Tichacek A, Haworth A, Chomba E. Enrollment and retention of HIV discordant couples in Lusaka, Zambia. J Acquir Immune Defic Syndr 2008, 47:116-125. 10.1097/QAI.0b013e31815d2f3f, 18030162.
57. Boeras DI, Luisi N, Karita E, McKinney S, Sharkey T, Keeling M, Chomba E, Kraft C, Wall K, Bizimana J, et al. Indeterminate and discrepant rapid HIV test results in couples' HIV testing and counselling centres in Africa. J Int AIDS Soc 2011, 14:18. 10.1186/1758-2652-14-18, 3086828, 21477317.
58. Allen SA, Chomba E, Karita E, Kilembe W, Inambao M, Streeb G. The contribution of HIV-discordant relationships to new HIV infections: a rebuttal. AIDS 2011, 25:1341-1343. 10.1097/QAD.0b013e32834835db, 21659799.
59. Delwart EL, Sheppard HW, Walker BD, Goudsmit J, Mullins JI. Human immunodeficiency virus type 1 evolution in vivo tracked by DNA heteroduplex mobility assays. J Virol 1994, 68:6672-6683. 237088, 8084001.
60. Clopper C, Pearson ES. The use of confidence or fiducial limits illustrated in the case of the binomial. Biometrika 1943, 26:403-413.