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RESEARCH ARTICLE

HIV-1 co-infection, superinfection and recombination

Megan C. Steain A , Bin Wang A , Dominic E. Dwyer A B and Nitin K. Saksena A C
+ Author Affiliations
- Author Affiliations

A Retroviral Genetics Laboratory, Center for Virus Research, Westmead Millennium Institute, Westmead, NSW 2145, Australia.

B Department of Virology, CIDMLS, ICPMR, Westmead Hospital, Westmead, NSW 2145, Australia.

C Corresponding author. Email: nitin_saksena@wmi.usyd.edu.au

Sexual Health 1(4) 239-250 https://doi.org/10.1071/SH04024
Submitted: 15 July 2004  Accepted: 1 November 2004   Published: 21 December 2004

Abstract

ABSTRACT. As the human immunodeficiency virus (HIV) pandemic progresses, an increasing number of recombinant viruses have been identified and in many geographical regions they are now the predominating strain. These recombinants are formed when an individual has acquired a co-infection or superinfection with more than one HIV-1 strain or subtype. Thus, dually infected individuals provide opportunities for studying HIV recombinants and viral interactions between infecting strains in vivo. The possible epidemiological, clinical and therapeutic implications of dual infections and recombination are many. Recombination may result in the emergence of more pathogenic and virulent HIV strains with altered fitness, tropism, and resistance to multiple drugs, and may hamper the development of subtype-based vaccines. This review is aimed at providing a more thorough understanding of dual infections (both co-infection and super-infection) and the possible consequences of the emergence of recombinant HIV-1 strains.

Additional keyword: subtypes.


References


[1] Domingo E,  Holland JJ. RNA virus mutations and fitness for survival. Annu Rev Microbiol 1997; 51 151–78.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[13] Dwyer DE,  Ge YC,  Wang B,  Bolton WV,  McCormack JG,  Cunningham AL, et al. First human immunodeficiency virus type 1 sequences in the V3 region, nef and vpr genes from Papua New Guinea. AIDS Res Hum Retroviruses 1997; 13(7): 625–7.
PubMed |

[14] Dwyer DE,  Herring BL,  Ge YC,  Bolton WV,  Ellis-Pegler RB,  Thomas M, et al. Human immunodeficiency virus type 1 subtypes B and C detected in New Zealand. AIDS Res Hum Retroviruses 1998; 14(12): 1105–8.
PubMed |

[15] Herring BL,  Ge YC,  Wang B,  Ratnamohan M,  Zheng F,  Cunningham AL, et al. Segregation of human immunodeficiency virus type 1 subtypes by risk factor in Australia. J Clin Microbiol 2003; 41(10): 4600–4.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[16] Peeters M,  Toure-Kane C,  Nkengasong JN. Genetic diversity of HIV in Africa: impact on diagnosis, treatment, vaccine development and trials. AIDS 2003; 17(18): 2547–60.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[17] Yamaguchi J,  Vallari AS,  Swanson P,  Bodelle P,  Kaptue L,  Ngansop C, et al. Evaluation of HIV type 1 group O isolates: identification of five phylogenetic clusters. AIDS Res Hum Retroviruses 2002; 18(4): 269–82.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[18] Yamaguchi J,  Bodelle P,  Kaptue L,  Zekeng L,  Gurtler LG,  Devare SG, et al. Near full-length genomes of 15 HIV type 1 group O isolates. AIDS Res Hum Retroviruses 2003; 19(11): 979–88.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[19] Dowling WE,  Kim B,  Mason CJ,  Wasunna KM,  Alam U,  Elson L, et al. Forty-one near full-length HIV-1 sequences from Kenya reveal an epidemic of subtype A and A-containing recombinants. AIDS 2002; 16(13): 1809–20.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[20] Temin HM. Sex and recombination in retroviruses. Trends Genet 1991; 7(3): 71–4.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[21] Yu H,  Jetzt AE,  Ron Y,  Preston BD,  Dougherty JP. The nature of human immunodeficiency virus type 1 strand transfers. J Biol Chem 1998; 273(43): 28384–91.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[22] Negroni M,  Buc H. Mechanisms of retroviral recombination. Annu Rev Genet 2001; 35 275–302.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[23] Xu H,  Boeke JD. High-frequency deletion between homologous sequences during retrotransposition of Ty elements in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 1987; 84(23): 8553–7.
PubMed |

[24] Hu WS,  Temin HM. Retroviral recombination and reverse transcription. Science 1990; 250(4985): 1227–33.
PubMed |

[25] Hsu TW,  Taylor JM. Single-stranded regions on unintegrated avian retrovirus DNA. J Virol 1982; 44(1): 47–53.
PubMed |

[26] Op de Coul E,  van der Schoot A,  Goudsmit J,  van den Burg R,  Janssens W,  Heyndrickx L, et al. Independent introduction of transmissible F/D recombinant HIV-1 from Africa into Belgium and The Netherlands. Virology 2000; 270(2): 267–77.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[27] Takehisa J,  Zekeng L,  Ido E,  Yamaguchi-Kabata Y,  Mboudjeka I,  Harada Y, et al. Human immunodeficiency virus type 1 intergroup (M/O) recombination in cameroon. J Virol 1999; 73(8): 6810–20.
PubMed |

[28] Gao F,  Bailes E,  Robertson DL,  Chen Y,  Rodenburg CM,  Michael SF, et al. Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature 1999; 397(6718): 436–41.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[29] Carr JK,  Torimiro JN,  Wolfe ND,  Eitel MN,  Kim B,  Sanders-Buell E, et al. The AG recombinant IbNG and novel strains of group M HIV-1 are common in Cameroon. Virology 2001; 286(1): 168–81.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[30] Montavon C,  Toure-Kane C,  Liegeois F,  Mpoudi E,  Bourgeois A,  Vergne L, et al. Most env and gag subtype A HIV-1 viruses circulating in West and West Central Africa are similar to the prototype AG recombinant virus IBNG. J Acquir Immune Defic Syndr 2000; 23(5): 363–74.
PubMed |

[31] Thomson MM,  Villahermosa ML,  Vazquez-de-Parga E,  Cuevas MT,  Delgado E,  Manjon N, et al. Widespread circulation of a B/F intersubtype recombinant form among HIV-1-infected individuals in Buenos Aires, Argentina. AIDS 2000; 14(7): 897–9.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[32] Tovanabutra S,  Beyrer C,  Sakkhachornphop S,  Razak MH,  Ramos GL,  Vongchak T, et al. The changing molecular epidemiology of HIV type 1 among northern Thai drug users, 1999 to 2002. AIDS Res Hum Retroviruses 2004; 20(5): 465–75.
PubMed |

[33] Liitsola K,  Tashkinova I,  Laukkanen T,  Korovina G,  Smolskaja T,  Momot O, et al. HIV-1 genetic subtype A/B recombinant strain causing an explosive epidemic in injecting drug users in Kaliningrad. AIDS 1998; 12(14): 1907–19.
PubMed |

[34] Dang Q,  Chen J,  Unutmaz D,  Coffin JM,  Pathak VK,  Powell D, et al. Nonrandom HIV-1 infection and double infection via direct and cell-mediated pathways. Proc Natl Acad Sci USA 2004; 101(2): 632–7.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[35] Ou CY,  Takebe Y,  Luo CC,  Kalish M,  Auwanit W,  Bandea C, et al. Wide distribution of two subtypes of HIV-1 in Thailand. AIDS Res Hum Retroviruses 1992; 8(8): 1471–2.
PubMed |

[36] McCutchan FE,  Hegerich PA,  Brennan TP,  Phanuphak P,  Singharaj P,  Jugsudee A, et al. Genetic variants of HIV-1 in Thailand. AIDS Res Hum Retroviruses 1992; 8(11): 1887–95.
PubMed |

[37] Carr JK,  Salminen MO,  Koch C,  Gotte D,  Artenstein AW,  Hegerich PA, et al. Full-length sequence and mosaic structure of a human immunodeficiency virus type 1 isolate from Thailand. J Virol 1996; 70(9): 5935–43.
PubMed |

[38] Anderson JP,  Rodrigo AG,  Learn GH,  Madan A,  Delahunty C,  Coon M, et al. Testing the hypothesis of a recombinant origin of human immunodeficiency virus type 1 subtype E. J Virol 2000; 74(22): 10752–65.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[39] Tovanabutra S,  Polonis V,  De Souza M,  Trichavaroj R,  Chanbancherd P,  Kim B, et al. First CRF01_AE/B recombinant of HIV-1 is found in Thailand. AIDS 2001; 15(8): 1063–5.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[40] Viputtijul K,  de Souza M,  Trichavaroj R,  Carr JK,  Tovanabutra S,  McCutchan FE, et al. Heterosexually acquired CRF01_AE/B recombinant HIV type 1 found in Thailand. AIDS Res Hum Retroviruses 2002; 18(16): 1235–7.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[41] Tovanabutra S,  Watanaveeradej V,  Viputtikul K,  De Souza M,  Razak MH,  Suriyanon V, et al. A new circulating recombinant form, CRF15_01B, reinforces the linkage between IDU and heterosexual epidemics in Thailand. AIDS Res Hum Retroviruses 2003; 19(7): 561–7.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[42] Andersson S,  Norrgren H,  Dias F,  Biberfeld G,  Albert J. Molecular characterization of human immunodeficiency virus (HIV)-1 and -2 in individuals from guinea-bissau with single or dual infections: predominance of a distinct HIV-1 subtype A/G recombinant in West Africa. Virology 1999; 262(2): 312–20.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[43] Carr JK,  Laukkanen T,  Salminen MO,  Albert J,  Alaeus A,  Kim B, et al. Characterization of subtype A HIV-1 from Africa by full genome sequencing. AIDS 1999; 13(14): 1819–26.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[44] Mboudjeka I,  Zekeng L,  Takehisa J,  Miura T,  Ido E,  Yamashita M, et al. HIV type 1 genetic variability in the northern part of Cameroon. AIDS Res Hum Retroviruses 1999; 15(11): 951–6.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[45] Mamadou S,  Vidal N,  Montavon C,  Ben A,  Djibo A,  Rabiou S, et al. Emergence of complex and diverse CRF02-AG/CRF06-cpx recombinant HIV type 1 strains in Niger, West Africa. AIDS Res Hum Retroviruses 2003; 19(1): 77–82.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[46] Janssens W,  Salminen MO,  Laukkanen T,  Heyndrickx L,  van der Auwera G,  Colebunders R, et al. Near full-length genome analysis of HIV type 1 CRF02.AG subtype C and CRF02.AG subtype G recombinants. AIDS Res Hum Retroviruses 2000; 16(12): 1183–9.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[47] Thomson MM,  Delgado E,  Herrero I,  Villahermosa ML,  Vazquez-de Parga E,  Cuevas MT, et al. Diversity of mosaic structures and common ancestry of human immunodeficiency virus type 1 BF intersubtype recombinant viruses from Argentina revealed by analysis of near full-length genome sequences. J Gen Virol 2002; 83(Pt 1): 107–19.
PubMed |

[48] Espinosa A,  Vignoles M,  Carrillo MG,  Sheppard H,  Donovan R,  Peralta LM, et al. Intersubtype BF recombinants of HIV-1 in a population of injecting drug users in Argentina. J Acquir Immune Defic Syndr 2004; 36(1): 630–6.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[49] Salminen MO. HIV inter-subtype recombination — consequences for the epidemic. AIDS Rev 2000; 2 178–89.


[50] Kunanusont C,  Foy HM,  Kreiss JK,  Rerks-Ngarm S,  Phanuphak P,  Raktham S, et al. HIV-1 subtypes and male-to-female transmission in Thailand. Lancet 1995; 345(8957): 1078–83.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[51] Soto-Ramirez LE,  Renjifo B,  McLane MF,  Marlink R,  O’Hara C,  Sutthent R, et al. HIV-1 Langerhans’ cell tropism associated with heterosexual transmission of HIV. Science 1996; 271(5253): 1291–3.
PubMed |

[52] Pope M,  Frankel SS,  Mascola JR,  Trkola A,  Isdell F, et al. Human immunodeficiency virus type 1 strains of subtypes B and E replicate in cutaneous dendritic cell–T-cell mixtures without displaying subtype-specific tropism. J Virol 1997; 71(10): 8001–7.
PubMed |

[53] French MA,  Herring BL,  Kaldor JM,  Sayer DC,  Furner V,  de Chaneet CC, et al. Intrafamilial transmission of HIV-1 infection from individuals with unrecognized HIV-1 infection. AIDS 2003; 17(13): 1977–81.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[54] van’t Wout AB,  Kootstra NA,  Mulder-Kampinga GA,  Albrecht-van Lent N,  Scherpbier HJ,  Veenstra J, et al. Macrophage-tropic variants initiate human immunodeficiency virus type 1 infection after sexual, parenteral, and vertical transmission. J Clin Invest 1994; 94(5): 2060–7.
PubMed |

[55] Zhu T,  Mo H,  Wang N,  Nam DS,  Cao Y,  Koup RA, et al. Genotypic and phenotypic characterization of HIV-1 patients with primary infection. Science 1993; 261(5125): 1179–81.
PubMed |

[56] O’Brien SJ,  Moore JP. The effect of genetic variation in chemokines and their receptors on HIV transmission and progression to AIDS. Immunol Rev 2000; 177 99–111.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[57] Luk KC,  Kaptue L,  Zekeng L,  Soriano V,  Gurtler L,  Devare SG, et al. Naturally occurring sequence polymorphisms within HIV type 1 group O protease. AIDS Res Hum Retroviruses 2001; 17(16): 1555–61.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[58] Descamps D,  Apetrei C,  Collin G,  Damond F,  Simon F,  Brun-Vezinet F. Naturally occurring decreased susceptibility of HIV-1 subtype G to protease inhibitors. AIDS 1998; 12(9): 1109–11.
PubMed |

[59] Maljkovic I,  Wilbe K,  Solver E,  Alaeus A,  Leitner T. Limited transmission of drug-resistant HIV type 1 in 100 Swedish newly detected and drug-naive patients infected with subtypes A, B, C, D, G, U, and CRF01_AE. AIDS Res Hum Retroviruses 2003; 19(11): 989–97.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[60] Becker-Pergola G,  Kataaha P,  Johnston-Dow L,  Fung S,  Jackson JB,  Eshleman SH. Analysis of HIV type 1 protease and reverse transcriptase in antiretroviral drug-naive Ugandan adults. AIDS Res Hum Retroviruses 2000; 16(8): 807–13.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[61] Moutouh L,  Corbeil J,  Richman DD. Recombination leads to the rapid emergence of HIV-1 dually resistant mutants under selective drug pressure. Proc Natl Acad Sci USA 1996; 93(12): 6106–11.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[62] Gunthard HF,  Leigh-Brown AJ,  D’Aquila RT,  Johnson VA,  Kuritzkes DR,  Richman DD, et al. Higher selection pressure from antiretroviral drugs in vivo results in increased evolutionary distance in HIV-1 pol. Virology 1999; 259(1): 154–65.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[63] Potter SJ,  Dwyer DE,  Saksena NK. Differential cellular distribution of HIV-1 drug resistance in vivo: evidence for infection of CD8+ T cells during HAART. Virology 2003; 305(2): 339–52.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[64] Potter SJ,  Lemey P,  Achaz G,  Chew CB,  Vandamme AM,  Dwyer DE, et al. HIV-1 compartmentalization in diverse leukocyte populations during antiretroviral therapy. J Leukoc Biol 2004; 76(3): 562–70.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[65] Levy DN,  Aldrovandi GM,  Kutsch O,  Shaw GM. Dynamics of HIV-1 recombination in its natural target cells. Proc Natl Acad Sci USA 2004; 101(12): 4204–9.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[66] Jagodzinski LL,  Cooley JD,  Weber M,  Michael NL. Performance characteristics of human immunodeficiency virus type 1 (HIV-1) genotyping systems in sequence-based analysis of subtypes other than HIV-1 subtype B. J Clin Microbiol 2003; 41(3): 998–1003.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[67] Chew CB,  Herring BL,  Zheng F,  Browne C,  Saksena NK,  Cunningham AL, et al. Comparison of three commercial assays for the quantification of HIV-1 RNA in plasma from individuals infected with different HIV-1 subtypes. J Clin Virol 1999; 14(2): 87–94.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[68] Gundlach BR,  Lewis MG,  Sopper S,  Schnell T,  Sodroski J,  Stahl-Hennig C, et al. Evidence for recombination of live, attenuated immunodeficiency virus vaccine with challenge virus to a more virulent strain. J Virol 2000; 74(8): 3537–42.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[69] Najera R,  Delgado E,  Perez-Alvarez L,  Thomson MM. Genetic recombination and its role in the development of the HIV-1 pandemic. AIDS 2002; 16((Suppl)): S3–16.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[70] Evans LA,  Moreau J,  Odehouri K,  Seto D,  Thomson-Honnebier G,  Legg H, et al. Simultaneous isolation of HIV-1 and HIV-2 from an AIDS patient. Lancet 1988; 332(8625): 1389–91.
Crossref | GoogleScholarGoogle Scholar |

[71] 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(9409): 619–22.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[72] Takehisa J,  Zekeng L,  Miura T,  Ido E,  Yamashita M,  Mboudjeka I, et al. Triple HIV-1 infection with group O and Group M of different clades in a single Cameroonian AIDS patient. J Acquir Immune Defic Syndr Hum Retrovirol 1997; 14(1): 81–2.
PubMed |

[73] Wang B,  Lal RB,  Dwyer DE,  Miranda-Saksena M,  Boadle R,  Cunningham AL, et al. Molecular and biological interactions between two HIV-1 strains from a coinfected patient reveal the first evidence in favor of viral synergism. Virology 2000; 274(1): 105–19.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[74] Takehisa J,  Zekeng L,  Ido E,  Mboudjeka I,  Moriyama H,  Miura T, et al. Various types of HIV mixed infections in Cameroon. Virology 1998; 245(1): 1–10.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[75] Janini LM,  Tanuri A,  Schechter M,  Peralta JM,  Vicente AC,  Dela Torre N, et al. Horizontal and vertical transmission of human immunodeficiency virus type 1 dual infections caused by viruses of subtypes B and C. J Infect Dis 1998; 177(1): 227–31.
PubMed |

[76] Otten RA,  Ellenberger DL,  Adams DR,  Fridlund CA,  Jackson E,  Pieniazek D, et al. Identification of a window period for susceptibility to dual infection with two distinct human immunodeficiency virus type 2 isolates in a Macaca nemestrina (pig-tailed macaque) model. J Infect Dis 1999; 180(3): 673–84.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[77] Fang G,  Weiser B,  Kuiken C,  Philpott SM,  Rowland-Jones S,  Plummer F, et al. Recombination following superinfection by HIV-1. AIDS 2004; 18(2): 153–9.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[78] 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(7): F11–6.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[79] 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(6914): 434–9.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[80] 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(10): 731–6.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[81] Ramos A,  Hu DJ,  Nguyen L,  Phan KO,  Vanichseni S,  Promadej N, et al. Intersubtype human immunodeficiency virus type 1 superinfection following seroconversion to primary infection in two injection drug users. J Virol 2002; 76(15): 7444–52.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[82] Wei Q,  Fultz PN. Extensive diversification of human immunodeficiency virus type 1 subtype B strains during dual infection of a chimpanzee that progressed to AIDS. J Virol 1998; 72(4): 3005–17.
PubMed |

[83] Fultz PN. HIV-1 superinfections: omens for vaccine efficacy? AIDS 2004; 18(1): 115–9.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[84] 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(1): 94–103.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[85] Gonzales MJ,  Delwart E,  Rhee SY,  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(3): 397–405.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[86] Weidle PJ,  Ganea CE,  Irwin KL,  Pieniazek D,  McGowan JP,  Olivo N, et al. Presence of human immunodeficiency virus (HIV) type 1, group M, non-B subtypes, Bronx, New York: a sentinel site for monitoring HIV genetic diversity in the United States. J Infect Dis 2000; 181(2): 470–5.
Crossref | GoogleScholarGoogle Scholar | PubMed |

[87] Brodine SK,  Mascola JR,  Weiss PJ,  Ito SI,  Porter KR,  Artenstein AW, et al. Detection of diverse HIV-1 genetic subtypes in the USA. Lancet 1995; 346(8984): 1198–9.
Crossref | GoogleScholarGoogle Scholar | PubMed |