1887

Abstract

Human immunodeficiency virus type 1 subtype C (HIV-1C) represents 30–65 % of HIV infections in southern Brazil, and isolated cases of HIV-1C infection have also been reported in Argentina, Uruguay, Paraguay and Venezuela. Phylogenetic studies have suggested that the Brazilian subtype C epidemic was initiated by the introduction of closely related strains. Nevertheless, because of sampling limitations, the point of entry and the timing of subtype C introduction into Brazil, as well as the origin of the founder lineage, remain controversial. The present study investigated the origin, spread and phylogeography of HIV-1C in South America. Phylogenetic analysis showed a well-supported monophyletic clade including all available strains from Brazil, Uruguay and Argentina. Only one lineage from Venezuela was unrelated to the epidemic involving the other three countries. Molecular clock and likelihood mapping analysis showed that HIV-1C introduction in Brazil dated back to the period 1960–1970, much earlier than previously thought, and was followed by a nearly simultaneous star-like outburst of viral lineages, indicating a subsequent rapid spread. Phylogeographic patterns suggested Paraná or Rio Grande do Sul as the possible entrance points of subtype C and an asymmetrical gene flow from Paraná to Sao Paulo, Santa Catarina and Rio Grande do Sul, as well as from Rio Grande do Sul to Sao Paulo fostered by the strong inter-connectivity between population centres in southern Brazil. The study illustrates how coupling phylogeography inference with geographical information system data is critical to understand the origin and dissemination of viral pathogens and potentially predict their future spread.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.028951-0
2011-07-01
2019-10-21
Loading full text...

Full text loading...

/deliver/fulltext/jgv/92/7/1698.html?itemId=/content/journal/jgv/10.1099/vir.0.028951-0&mimeType=html&fmt=ahah

References

  1. Anisimova M. , Gascuel O. . ( 2006; ). Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. . Syst Biol 55:, 539–552. [CrossRef].[PubMed].
    [Google Scholar]
  2. Bello G. , Passaes C. P. , Guimarães M. L. , Lorete R. S. , Matos Almeida S. E. , Medeiros R. M. , Alencastro P. R. , Morgado M. G. . ( 2008; ). Origin and evolutionary history of HIV-1 subtype C in Brazil. . AIDS 22:, 1993–2000. [CrossRef].[PubMed].
    [Google Scholar]
  3. Bello G. , Guimarães M. L. , Passaes C. P. , Matos Almeida S. E. , Veloso V. G. , Morgado M. G. . ( 2009; ). Evidences of recent decline in the expansion rate of the HIV type 1 subtype C and CRF31_BC epidemics in southern Brazil. . AIDS Res Hum Retroviruses 25:, 1065–1069. [CrossRef].[PubMed].
    [Google Scholar]
  4. Brazil ( 2008; ). Boletim Epidemiológico – AIDS e DST. , p. 64. Edited by da Saúde Ministério . . Brasília, Brazil:: Ministério da Saúde - Secretaria de Vigilância em Saúde - Programa Nacionald e DST e Aids;.
  5. Brazil ( 2010; ). Instituto Brasileiro de Geografia e Estatística: Ministério do Planejamento, Orçamento e Gestão. .
  6. Brígido L. F. , Nunes C. C. , Oliveira C. M. , Knoll R. K. , Ferreira J. L. , Freitas C. A. , Alves M. A. , Dias C. , Rodrigues R. . Research Capacity Program ( 2007; ). HIV type 1 subtype C and CB Pol recombinants prevail at the cities with the highest AIDS prevalence rate in Brazil. . AIDS Res Hum Retroviruses 23:, 1579–1586. [CrossRef].[PubMed].
    [Google Scholar]
  7. Carrion G. , Eyzaguirre L. , Montano S. M. , Laguna-Torres V. , Serra M. , Aguayo N. , Avila M. M. , Ruchansky D. , Pando M. A. et al. ( 2004; ). Documentation of subtype C HIV type 1 strains in Argentina, Paraguay, and Uruguay. . AIDS Res Hum Retroviruses 20:, 1022–1025. [CrossRef].[PubMed].
    [Google Scholar]
  8. Dachraoui R. , Depatureaux A. , Chakroun M. , Fodha I. , Letaief A. , Trabelsi A. , Simon F. , Plantier J. C. . ( 2008; ). Monitoring of HIV-1 resistance in Tunisia (North Africa) with a dried plasma spot strategy. . J Acquir Immune Defic Syndr 47:, 522–525. [CrossRef].[PubMed].
    [Google Scholar]
  9. de Almeida Neto C. , McFarland W. , Murphy E. L. , Chen S. , Nogueira F. A. , Mendrone A. Jr , Salles N. A. , Chamone D. A. , Sabino E. C. . ( 2007; ). Risk factors for human immunodeficiency virus infection among blood donors in Sao Paulo, Brazil, and their relevance to current donor deferral criteria. . Transfusion 47:, 608–614. [CrossRef].[PubMed].
    [Google Scholar]
  10. de Macedo Brigido L. F. . ( 2009; ). On the origin of South America HIV-1 C epidemic. . AIDS 23:, 543–544. [CrossRef].[PubMed].
    [Google Scholar]
  11. de Oliveira T. , Pillay D. , Gifford R. J. . UK Collaborative Group on HIV Drug Resistance ( 2010; ). The HIV-1 subtype C epidemic in South America is linked to the United Kingdom. . PLoS ONE 5:, e9311. [CrossRef].[PubMed].
    [Google Scholar]
  12. Dias C. F. , Nunes C. C. , Freitas I. O. , Lamego I. S. , Oliveira I. M. , Gilli S. , Rodrigues R. , Brigido L. F. . ( 2009; ). High prevalence and association of HIV-1 non-B subtype with specific sexual transmission risk among antiretroviral naïve patients in Porto Alegre, RS, Brazil. . Rev Inst Med Trop Sao Paulo 51:, 191–196.[PubMed].
    [Google Scholar]
  13. Drummond A. J. , Rambaut A. . ( 2007; ). beast: Bayesian evolutionary analysis by sampling trees. . BMC Evol Biol 7:, 214. [CrossRef].[PubMed].
    [Google Scholar]
  14. Felsenstein J. . ( 2006; ). Accuracy of coalescent likelihood estimates: do we need more sites, more sequences, or more loci?. Mol Biol Evol 23:, 691–700. [CrossRef].[PubMed].
    [Google Scholar]
  15. Ferreira J. L. , Thomaz M. , Rodrigues R. , Harrad D. , Oliveira C. M. , Oliveira C. A. , Batista J. P. , Ito T. S. , Brigido L. F. . ( 2008; ). Molecular characterisation of newly identified HIV-1 infections in Curitiba, Brazil: preponderance of clade C among males with recent infections. . Mem Inst Oswaldo Cruz 103:, 800–808. [CrossRef].[PubMed].
    [Google Scholar]
  16. Fonseca M. G. , Bastos F. I. . ( 2007; ). Twenty-five years of the AIDS epidemic in Brazil: principal epidemiological findings, 1980–2005. . Cad Saude Publica 23: Suppl 3 S333–S344. [CrossRef].[PubMed].
    [Google Scholar]
  17. Fontella R. , Soares M. A. , Schrago C. G. . ( 2008; ). On the origin of HIV-1 subtype C in South America. . AIDS 22:, 2001–2011. [CrossRef].[PubMed].
    [Google Scholar]
  18. Fontella R. , Soares M. A. , Schrago C. G. . ( 2009; ). The origin of South American HIV-1 subtype C: lack of evidence for a Mozambican ancestry. . AIDS 23:, 1926–1928. [CrossRef].[PubMed].
    [Google Scholar]
  19. Geretti A. M. . ( 2006; ). HIV-1 subtypes: epidemiology and significance for HIV management. . Curr Opin Infect Dis 19:, 1–7. [CrossRef].[PubMed].
    [Google Scholar]
  20. Gray R. R. , Tatem A. J. , Lamers S. , Hou W. , Laeyendecker O. , Serwadda D. , Sewankambo N. , Gray R. H. , Wawer M. et al. ( 2009; ). Spatial phylodynamics of HIV-1 epidemic emergence in east Africa. . AIDS 23:, F9–F17. [CrossRef].[PubMed].
    [Google Scholar]
  21. Guimarães M. L. , dos Santos Moreira A. , Loureiro R. , Galvão-Castro B. , Morgado M. G. . Brazilian Network for HIV Isolation and Characterization ( 2002; ). High frequency of recombinant genomes in HIV type 1 samples from Brazilian southeastern and southern regions. . AIDS Res Hum Retroviruses 18:, 1261–1269. [CrossRef].[PubMed].
    [Google Scholar]
  22. Guindon S. , Gascuel O. . ( 2003; ). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. . Syst Biol 52:, 696–704. [CrossRef].[PubMed].
    [Google Scholar]
  23. Hemelaar J. , Gouws E. , Ghys P. D. , Osmanov S. . ( 2006; ). Global and regional distribution of HIV-1 genetic subtypes and recombinants in 2004. . AIDS 20:, W13–W23. [CrossRef].[PubMed].
    [Google Scholar]
  24. Holmes E. C. . ( 2008; ). Evolutionary history and phylogeography of human viruses. . Annu Rev Microbiol 62:, 307–328. [CrossRef].[PubMed].
    [Google Scholar]
  25. Jones L. R. , Dilernia D. A. , Manrique J. M. , Moretti F. , Salomón H. , Gomez-Carrillo M. . ( 2009; ). In-depth analysis of the origins of HIV type 1 subtype C in South America. . AIDS Res Hum Retroviruses 25:, 951–959. [CrossRef].[PubMed].
    [Google Scholar]
  26. Korber B. , Muldoon M. , Theiler J. , Gao F. , Gupta R. , Lapedes A. , Hahn B. H. , Wolinsky S. , Bhattacharya T. . ( 2000; ). Timing the ancestor of the HIV-1 pandemic strains. . Science 288:, 1789–1796. [CrossRef].[PubMed].
    [Google Scholar]
  27. Locateli D. , Stoco P. H. , de Queiroz A. T. , Alcântara L. C. , Ferreira L. G. , Zanetti C. R. , Rodrigues R. , Grisard E. C. , Pinto A. R. . ( 2007; ). Molecular epidemiology of HIV-1 in Santa Catarina State confirms increases of subtype C in Southern Brazil. . J Med Virol 79:, 1455–1463. [CrossRef].[PubMed].
    [Google Scholar]
  28. Machado L. F. , Ishak M. O. , Vallinoto A. C. , Lemos J. A. , Azevedo V. N. , Moreira M. R. , Souza M. I. , Fernandes L. M. , Souza L. L. , Ishak R. . ( 2009; ). Molecular epidemiology of HIV type 1 in northern Brazil: identification of subtypes C and D and the introduction of CRF02_AG in the Amazon region of Brazil. . AIDS Res Hum Retroviruses 25:, 961–966. [CrossRef].[PubMed].
    [Google Scholar]
  29. Maddison D. R. , Maddison W. P. . ( 2008; ). MacClade, version 4.08. . Sunderland, MA:: Sinauer Associates;.
  30. Meloni S. T. , Kim B. , Sankalé J. L. , Hamel D. J. , Tovanabutra S. , Mboup S. , McCutchan F. E. , Kanki P. J. . ( 2004; ). Distinct human immunodeficiency virus type 1 subtype A virus circulating in West Africa: sub-subtype A3. . J Virol 78:, 12438–12445. [CrossRef].[PubMed].
    [Google Scholar]
  31. Nelson A. . ( 2008; ). Travel Time to Major Cities: a Global Map of Accessibility. Ispra, Italy:: Global Environment Monitoring Unit – Joint Research Center of the European Commission;.
    [Google Scholar]
  32. Osmanov S. , Heyward W. L. , Esparza J. . ( 1994; ). The World Health Organization Network for HIV Isolation and Characterization: summary of a pilot study. . AIDS Res Hum Retroviruses 10:, 1325–1326. [CrossRef].[PubMed].
    [Google Scholar]
  33. Osmanov S. , Pattou C. , Walker N. , Schwardländer B. , Esparza J. . WHO-UNAIDS Network for HIV Isolation and Characterization ( 2002; ). Estimated global distribution and regional spread of HIV-1 genetic subtypes in the year 2000. . J Acquir Immune Defic Syndr 29:, 184–190.[PubMed].[CrossRef]
    [Google Scholar]
  34. Peeters M. . ( 2000; ). Recombinant HIV sequences: their role in the global epidemic. . In HIV Sequence Compendium 2000, pp. I-39–I-54. Edited by Kuiken C. L. , Foley B. , Hahn B. , Korber B. , McCutchan F. , Marx P. A. , Mellors J. W. , Mullins J. I. , Sodroski J. , Wolinsky S. . Theoretical Biophysics Group . Los Alamos, NM:: Los Alamos National Laboratory;.
    [Google Scholar]
  35. Plantier J. C. , Leoz M. , Dickerson J. E. , De Oliveira F. , Cordonnier F. , Lemée V. , Damond F. , Robertson D. L. , Simon F. . ( 2009; ). A new human immunodeficiency virus derived from gorillas. . Nat Med 15:, 871–872. [CrossRef].[PubMed].
    [Google Scholar]
  36. Rangel H. R. , Garzaro D. , Gutiérrez C. R. , Vásquez L. , Guillen G. , Torres J. R. , Pujol F. H. . ( 2009; ). HIV diversity in Venezuela: predominance of HIV type 1 subtype B and genomic characterization of non-B variants. . AIDS Res Hum Retroviruses 25:, 347–350. [CrossRef].[PubMed].
    [Google Scholar]
  37. Reiche E. M. , Bonametti A. M. , Watanabe M. A. , Morimoto H. K. , Morimoto A. A. , Wiechmann S. L. , Breganó J. W. , Matsuo T. , Reiche F. V. . ( 2005; ). Socio-demographic and epidemiological characteristics associated with human immunodeficiency virus type 1 (HIV-1) infection in HIV-1-exposed but uninfected individuals, and in HIV-1-infected patients from a southern Brazilian population. . Rev Inst Med Trop Sao Paulo 47:, 239–246.[PubMed].[CrossRef]
    [Google Scholar]
  38. Rodrigues R. , Vazquez C. M. , Colares J. K. , Custodio R. M. , Bonásser Filho F. , Souza L. R. , Gianna M. C. , Marques C. C. , Brígido L. F. . ( 2005; ). Antiretroviral resistance mutations in human immunodeficiency virus type 1 infected patients enrolled in genotype testing at the Central Public Health Laboratory, São Paulo, Brazil: preliminary results. . Mem Inst Oswaldo Cruz 100:, 97–102. [CrossRef].[PubMed].
    [Google Scholar]
  39. Rodrigues R. , Manenti S. , Romao P. R. , de Paula Ferreira J. L. , Batista J. P. , Siqueira A. F. , de Macedo Brigido L. F. . ( 2010; ). Young pregnant women living with HIV/AIDS in Criciuma, Southern Brazil, are infected almost exclusively with HIV type 1 clade C. . AIDS Res Hum Retroviruses 26:, 351–357. [CrossRef].[PubMed].
    [Google Scholar]
  40. Salemi M. , Strimmer K. , Hall W. W. , Duffy M. , Delaporte E. , Mboup S. , Peeters M. , Vandamme A. M. . ( 2001; ). Dating the common ancestor of SIVcpz and HIV-1 group M and the origin of HIV-1 subtypes using a new method to uncover clock-like molecular evolution. . FASEB J 15:, 276–278.[PubMed].
    [Google Scholar]
  41. Salemi M. , Lamers S. L. , Yu S. , de Oliveira T. , Fitch W. M. , McGrath M. S. . ( 2005; a). Phylodynamic analysis of human immunodeficiency virus type 1 in distinct brain compartments provides a model for the neuropathogenesis of AIDS. . J Virol 79:, 11343–11352. [CrossRef].[PubMed].
    [Google Scholar]
  42. Salemi M. , de Oliveira T. , Soares M. A. , Pybus O. , Dumans A. T. , Vandamme A. M. , Tanuri A. , Cassol S. , Fitch W. M. . ( 2005; b). Different epidemic potentials of the HIV-1B and C subtypes. . J Mol Evol 60:, 598–605. [CrossRef].[PubMed].
    [Google Scholar]
  43. Salemi M. , Goodenow M. M. , Montieri S. , de Oliveira T. , Santoro M. M. , Beshkov D. , Alexiev I. , Elenkov I. , Elenkov I. et al. ( 2008; ). The HIV type 1 epidemic in Bulgaria involves multiple subtypes and is sustained by continuous viral inflow from West and East European countries. . AIDS Res Hum Retroviruses 24:, 771–779. [CrossRef].[PubMed].
    [Google Scholar]
  44. Santos A. F. , Schrago C. G. , Martinez A. M. , Mendoza-Sassi R. , Silveira J. , Sousa T. M. , Lengruber R. B. , Soares E. A. , Sprinz E. , Soares M. A. . ( 2007; ). Epidemiologic and evolutionary trends of HIV-1 CRF31_BC-related strains in southern Brazil. . J Acquir Immune Defic Syndr 45:, 328–333.[PubMed].
    [Google Scholar]
  45. Schmidt H. A. , Strimmer K. , Vingron M. , von Haeseler A. . ( 2002; ). tree-puzzle: maximum likelihood phylogenetic analysis using quartets and parallel computing. . Bioinformatics 18:, 502–504. [CrossRef].[PubMed].
    [Google Scholar]
  46. Sharp P. M. , Hahn B. H. . ( 2008; ). AIDS: prehistory of HIV-1. . Nature 455:, 605–606. [CrossRef].[PubMed].
    [Google Scholar]
  47. Slatkin M. . ( 1989; ). Detecting small amounts of gene flow from phylogenies of alleles. . Genetics 121:, 609–612.[PubMed].
    [Google Scholar]
  48. Soares E. A. , Martínez A. M. , Souza T. M. , Santos A. F. , Da Hora V. , Silveira J. , Bastos F. I. , Tanuri A. , Soares M. A. . ( 2005; ). HIV-1 subtype C dissemination in southern Brazil. . AIDS 19: Suppl. 4 S81–S86. [CrossRef].[PubMed].
    [Google Scholar]
  49. Stefani M. M. , Pereira G. A. , Lins J. A. , Alcantara K. C. , Silveira A. A. , Viegas A. A. , Maya N. C. , Mussi A. H. . ( 2007; ). Molecular screening shows extensive HIV-1 genetic diversity in Central West Brazil. . J Clin Virol 39:, 205–209. [CrossRef].[PubMed].
    [Google Scholar]
  50. Strimmer K. , von Haeseler A. . ( 1997; ). Likelihood-mapping: a simple method to visualize phylogenetic content of a sequence alignment. . Proc Natl Acad Sci U S A 94:, 6815–6819. [CrossRef].[PubMed].
    [Google Scholar]
  51. Stuyver L. , Wyseur A. , Rombout A. , Louwagie J. , Scarcez T. , Verhofstede C. , Rimland D. , Schinazi R. F. , Rossau R. . ( 1997; ). Line probe assay for rapid detection of drug-selected mutations in the human immunodeficiency virus type 1 reverse transcriptase gene. . Antimicrob Agents Chemother 41:, 284–291.[PubMed].
    [Google Scholar]
  52. Suchard M. A. , Weiss R. E. , Sinsheimer J. S. . ( 2001; ). Bayesian selection of continuous-time Markov chain evolutionary models. . Mol Biol Evol 18:, 1001–1013.[PubMed].[CrossRef]
    [Google Scholar]
  53. Swofford D. L. , Sullivan J. . ( 2009; ). Phylogeny inference based on parsimony and other methods using paup . . In The Phylogenetic Handbook. A Practical Approach to Phylogenetic Analysis and Hypothesis Testing, , 2nd edn., pp. 267–312. Edited by Lemey P. , Salemi M. , Vandamme A. M. . . New York, NY:: Cambridge University Press;.[CrossRef]
    [Google Scholar]
  54. Szwarcwald C. L. , Souza Júnior P. R. B. . ( 2006; ). Estimativa da prevalência de HIV na população brasileira de 15 a 49 anos, 2004. . Boletim Epidemiológico AIDS e DST, , Ano III., pp. 11–15.
    [Google Scholar]
  55. Takebe Y. , Kusagawa S. , Motomura K. . ( 2004; ). Molecular epidemiology of HIV: tracking AIDS pandemic. . Pediatr Int 46:, 236–244. [CrossRef].[PubMed].
    [Google Scholar]
  56. Thompson J. D. , Higgins D. G. , Gibson T. J. . ( 1994; ). clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. . Nucleic Acids Res 22:, 4673–4680. [CrossRef].[PubMed].
    [Google Scholar]
  57. Thomson M. M. , Delgado E. , Herrero I. , Villahermosa M. L. , Vázquez-de Parga E. , Cuevas M. T. , Carmona R. , Medrano L. , Pérez-Alvarez L. et al. ( 2002; ). 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 83:, 107–119.[PubMed].
    [Google Scholar]
  58. UNAIDS/WHO ( 2007; ). AIDS Epidemic Update: December 2007, p. 60. Geneva, Switzerland:: United Nations Programme on HIV/AIDS & World Health Organization;.
    [Google Scholar]
  59. Vidal N. , Mulanga C. , Bazepeo S. E. , Lepira F. , Delaporte E. , Peeters M. . ( 2006; ). Identification and molecular characterization of subsubtype A4 in central Africa. . AIDS Res Hum Retroviruses 22:, 182–187. [CrossRef].[PubMed].
    [Google Scholar]
  60. Worobey M. , Gemmel M. , Teuwen D. E. , Haselkorn T. , Kunstman K. , Bunce M. , Muyembe J. J. , Kabongo J. M. , Kalengayi R. M. et al. ( 2008; ). Direct evidence of extensive diversity of HIV-1 in Kinshasa by 1960. . Nature 455:, 661–664. [CrossRef].[PubMed].
    [Google Scholar]
  61. Xia X. , Xie Z. . ( 2001; ). dambe: software package for data analysis in molecular biology and evolution. . J Hered 92:, 371–373. [CrossRef].[PubMed].
    [Google Scholar]
  62. Xia X. , Xie Z. , Salemi M. , Chen L. , Wang Y. . ( 2003; ). An index of substitution saturation and its application. . Mol Phylogenet Evol 26:, 1–7. [CrossRef].[PubMed].
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.028951-0
Loading
/content/journal/jgv/10.1099/vir.0.028951-0
Loading

Data & Media loading...

Supplements

Accession numbers of the HIV-1C sequences selected from GenBank and the Los Alamos HIV sequence database for phylogenetic analysis based on the p24, RT and gp41 genes [Excel file](76 KB)

EXCEL

Index of substitution rate ( ss) and critical index of substitution rate ( ss.c) of the p24, RT and gp41 sequence datasets used for ML and Bayesian analysis [Single PDF file](9240 KB)

PDF

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error