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Genetic diversity of human papillomavirus types 35, 45 and 58 in cervical cancer in Brazil

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Abstract

In Brazil, most studies of intra-type variants of human papillomavirus (HPV) have focused on HPV16 and HPV18, but other high-risk HPV types have not been studied. Here, we report the prevalence of lineages and variants of HPV35, HPV45 and HPV58 in cervical cancers from the Amazonian and Southeast Brazilian regions. The most frequent sublineages were A1 for HPV35, B2 for HPV45, and A2 for HPV58. The Southeast region had a higher frequency of the B2 sublineage of HPV45, and for HPV35, the genetic and nucleotide sequence diversity were higher in the Southeast region, suggesting that regional factors are influencing the diversity and lineage prevalence.

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References

  1. Ferlay J, Soerjomataram I, Dikshit R et al (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136:E359–E386. doi:10.1002/ijc.29210

    Article  CAS  PubMed  Google Scholar 

  2. INCA-Instituto Nacional de Câncer José Alencar Gomes da Silva (2015) Coordenação de prevenção e vigilância. Estimativa 2016: Incidência de câncer no Brasil. Instituto Nacional de Câncer José Alencar Gomes da Silva, Rio de Janeiro, pp 1–126

    Google Scholar 

  3. Walboomers JMM, Jacobs MV, Manos MM et al (1999) Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J. Pathol. 189:12–19. doi:10.1002/(SICI)1096-9896(199909)189:1<12:AID-PATH431>3.0.CO;2-F

    Article  CAS  PubMed  Google Scholar 

  4. Muñoz N, Bosch FX, de Sanjose S  et al (2003) Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 348:518–527. doi:10.1056/NEJMoa021641

    Article  PubMed  Google Scholar 

  5. Joura EA, Giuliano AR, Iversen OE et al (2015) A 9-valent HPV vaccine against infection and intraepithelial neoplasia in women. N Engl J Med 372:711–723. doi:10.1056/NEJMoa1405044

    Article  CAS  PubMed  Google Scholar 

  6. Bernard HU, Burk RD, Chen Z et al (2010) Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology 401:70–79. doi:10.1016/j.virol.2010.02.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Burk RD, Harari A, Chen Z (2013) Human papillomavirus genome variants. Virology 445:232–243. doi:10.1016/j.virol.2013.07.018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Berumen J, Ordoñez RM, Lazcano E et al (2001) Asian-American variants of Human Papillomavirus 16 and risk for cervical cancer: a case–control study. J Natl Cancer Inst 93:1325–1330

    Article  CAS  PubMed  Google Scholar 

  9. Sichero L, Ferreira S, Trottier H et al (2007) High grade cervical lesions are caused preferentially by non-European variants of HPVs 16 and 18. Int J Cancer 120:1763–1768. doi:10.1002/ijc.22481

    Article  CAS  PubMed  Google Scholar 

  10. Zuna RE, Moore WE, Shanesmith RP et al (2009) Association of HPV16 E6 variants with diagnostic severity in cervical cytology samples of 354 women in a US population. Int J Cancer 125:2609–2613. doi:10.1002/ijc.24706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Cornet I, Gheit T, Iannacone MR et al (2013) HPV16 genetic variation and the development of cervical cancer worldwide. Br J Cancer 108:240–244. doi:10.1038/bjc.2012.508

    Article  CAS  PubMed  Google Scholar 

  12. Chen AA, Heideman DAM, Boon D et al (2014) Human papillomavirus 45 genetic variation and cervical cancer risk worldwide. J Virol 88:4514–4521. doi:10.1128/JVI.03534-13

    Article  PubMed  PubMed Central  Google Scholar 

  13. Chan PKS, Zhang C, Park J et al (2013) Geographical distribution and oncogenic risk association of human papillomavirus type 58 E6 and E7 sequence variations. Int J Cancer 132:2528–2536. doi:10.1002/ijc.27932

    Article  CAS  PubMed  Google Scholar 

  14. Junes-Gill K, Sichero L, Maciag PC et al (2008) Human papillomavirus type 16 variants in cervical cancer from an admixtured population in Brazil. J Med Virol 80:1639–1645. doi:10.1002/jmv.21238

    Article  CAS  PubMed  Google Scholar 

  15. Cerqueira DM, Raio T, Véras NM et al (2008) New variants of human papillomavirus type 18 identified in central Brazil. Virus Genes 37:282–287. doi:10.1007/s11262-008-0263-8

    Article  CAS  PubMed  Google Scholar 

  16. Cruz RM, Cerqueira MD, Cruz WB et al (2004) Prevalence of human papillomavirus type 16 variants in the Federal District, Central Brazil. Mem Inst Oswaldo Cruz 99:281–282. doi:10.1590/S0074-02762004000300007

    Article  PubMed  Google Scholar 

  17. Freitas LB, Chen Z, Muqui EF et al (2014) Human papillomavirus 16 non-European variants are preferentially associated with high-grade cervical lesions. PloS One 9:e10074. doi:10.1371/journal.pone.0100746

    Google Scholar 

  18. Vidal JPCB, Felix SF, Chaves CBP et al (2016) Genetic diversity of HPV16 and HPV18 in Brazilian patients with invasive cervical cancer. J Med Virol 88:1279–1287. doi:10.1002/jmv.24458

    Article  CAS  PubMed  Google Scholar 

  19. Alves-Silva J, da Silva Santos M, Guimarães PE et al (2000) The ancestry of Brazilian mtDNA lineages. Am J Hum Genet 67:444–461. doi:10.1086/303004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Cornet I, Gheit T, Franceschi S et al (2012) Human papillomavirus type 16 genetic variants: phylogeny and classification based on E6 and LCR. J Virol 86:6855–6861. doi:10.1128/JVI.00483-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Xi FL, Schiffman M, Koutsky LA et al (2014) Lineages of oncogenic Human Papillomavirus types other than type 16 and 18 and risk for cervical intraepithelial neoplasia. J Natl Cancer Inst 106:dju270. doi:10.1093/jnci/dju270

    Article  PubMed  PubMed Central  Google Scholar 

  22. Pérez S, Cid A, Iñarrea A et al (2014) Prevalence of HPV 16 and HPV 18 lineages in Galicia, Spain. PLoS One 9:e104678. doi:10.1371/journal.pone.0104678

    Article  PubMed  PubMed Central  Google Scholar 

  23. Fuessel Haws AL, He Q, Rady PL et al (2004) Nested PCR with the PGMY09/11 and GP5(+)/6(+) primer sets improves detection of HPV DNA in cervical samples. J Virol Methods 122:87–93. doi:10.1016/j.jviromet.2004.08.007

    Article  CAS  PubMed  Google Scholar 

  24. Almeida LM, Martins LF, Pontes V et al (2017) Human PapilomaVirus (HPV) genotype distribution among cervical cancer patients prior to Brazilian National HPV Immunization Program. J Environ Public Health 2017:1645074. doi:10.1155/2017/1645074

    Article  PubMed  PubMed Central  Google Scholar 

  25. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. doi:10.1093/bioinformatics/btp187

    Article  CAS  PubMed  Google Scholar 

  26. Tavaré S (1986) Some probabilistic and statistical aspects of the primary structure of nucleotide sequences. In: Miura RM (ed) Lectures on mathematics in the life sciences, vol 17. American Mathematical Society, Providence, pp 57–86

    Google Scholar 

  27. Lanave C, Preparata G, Saccone C, Serio G (1984) A new method for calculating evolutionary substitution rates. J Mol Evol 20:86–93

    Article  CAS  PubMed  Google Scholar 

  28. Guindon S, Dufayard JF, Lefort V et al (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyMV 3.0. Syst Biol 59:307–321

    Article  CAS  PubMed  Google Scholar 

  29. Bandelt HJ, Forster P, Röhl A (1999) Median-Joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  CAS  PubMed  Google Scholar 

  30. Excoffier L, Lischer H (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10:564–567. doi:10.1111/j.1755-0998.2010.02847.x

    Article  Google Scholar 

  31. Calleja-Macias IE, Villa LL, Prado JC et al (2005) Worldwide genomic diversity of the high-risk human papillomavirus types 31, 35, 52, and 58, four close relatives of human papillomavirus type 16. J Virol 79:13630–13640. doi:10.1128/JVI.79.21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Gauthier B, Coutlée F, Franco EL, Brassard P (2015) Human papillomavirus variants among Inuit women northern Quebec, Canada. Int J Circumpolar Health 74:1–7. doi:10.3402/ijch.v74.29482

    Article  Google Scholar 

  33. Calleja-Macias IE, Kalantari M, Huh J et al (2004) Genomic diversity of human papillomavirus-16, 18, 31, and 35 isolates in a Mexican population and relationship to European, African, and Native American variants. Virology 319:315–323. doi:10.1016/j.virol.2003.11.009

    Article  CAS  PubMed  Google Scholar 

  34. Schiffman M, Rodriguez AC, Chen Z et al (2010) A population-based prospective study of carcinogenic human papillomavirus (HPV) variant lineages, viral persistence, and cervical neoplasia. Cancer Res 70:3159–3169. doi:10.1158/0008-5472.CAN-09-4179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Marincevic-Zuniga Y, Gustavsson I, Gyllensten U (2012) Multiply-primed rolling circle amplification of human papillomavirus using sequence-specific primers. Virology 432:57–62. doi:10.1016/j.virol.2012.05.030

    Article  CAS  PubMed  Google Scholar 

  36. Li N, Franceschi S, Howell-Jones MR et al (2011) Human papillomavirus type distribution in 30,848 invasive cervical cancers worldwide: variationby geographical region, histological type and year of publication. Int J Cancer 128:927–935. doi:10.1002/ijc.25396

    Article  CAS  PubMed  Google Scholar 

  37. Chan PKS, Luk AC, Park JS et al (2011) Identification of Human Papillomavirus Type 58 lineages and the distribution worldwide. J Infect Dis 203:1565–1573. doi:10.1093/infdis/jir157

    Article  PubMed  Google Scholar 

  38. Lopera EA, Baena A, Florez V et al (2014) Unexpected inverse correlation between Native American ancestry and Asian American variants of HPV16 in admixed Colombian cervical cancer cases. Infect Genet Evol 28:339–348. doi:10.1016/j.meegid.2014.10.014

    Article  PubMed  Google Scholar 

  39. Manta FSN, Pereira R, Vianna R et al (2013) Revisiting the genetic ancestry of Brazilians using autosomal AIM-Indels. PloS One 8:e75145. doi:10.1371/journal.pone.0075145

    Article  CAS  Google Scholar 

  40. Resque R, Gusmão L, Geppert M et al (2016) Male lineages in Brazil: intercontinental admixture and stratification of the european background. PLoS One 11:e0152573. doi:10.1371/journal.pone.0152573

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We want to thank the physicians who collected the tumor biopsies. This work was supported by the National Institute for Cancer Control (INCT do Cancer: http://www.inct-cancer-control.com.br/); Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) Grants 573806/2008-0, 484005/2013-8 and 305873/2014-8; Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) Grant E26/170.026/2008; Ministry of Health – Brazil; and Pan-American Health Organization (PAHO).

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Author notes

  1. Miguel Ângelo Martins Moreira

    Present address: Genetics Program, Instituto Nacional de Câncer, Rio de Janeiro, Brazil

Authors and Affiliations

  1. Genetics Department, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

    Diogo Lisbôa Basto

  2. Genetics Program, Instituto Nacional de Câncer, Rio de Janeiro, Brazil

    Diogo Lisbôa Basto, João Paulo Vidal & Shayany Pinto Felix

  3. Department of Woman Health, Faculty of Medicine, Universidade Federal do Pará, Belém do Pará, Brazil

    Valéria Barbosa Pontes, Laine Celestino Pinto & Bruno Moreira Soares

  4. Population Research Department, Instituto Nacional de Câncer (INCA), Rio de Janeiro, Brazil

    Luis Felipe Martins, Flávia Miranda Correa & Liz Maria Almeida

  5. Department of Physiology and Pharmacology, Universidade Federal do Ceará, Fortaleza, Brazil

    Raquel Carvalho Montenegro

  6. Gynecologic Section and Molecular Carcinogenesis Program, Instituto Nacional de Câncer, Rio de Janeiro, Brazil

    Cláudia Bessa Pereira Chaves

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  1. Diogo Lisbôa Basto
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Corresponding author

Correspondence to Miguel Ângelo Martins Moreira.

Ethics declarations

Ethical approval

All procedures were approved by the Research Ethics Committees of the Instituto Nacional de Câncer (CAAE 53398416.0.0000.5274) and the Hospital Ophir Loyola (CAAE 03288212.0.1001.0018).

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All patients signed an informed consent form.

Animal rights

This article does not contain any studies with animals.

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The authors declare no conflict of interest.

Electronic supplementary material

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705_2017_3439_MOESM1_ESM.tif

Haplotype network for HPV35 generated by median joining analysis, based on samples of Rio de Janeiro and Pará, medium vectors are indicated by red dots, and the circles in gray (Pará) or black (Rio de Janeiro) are the haplotypes. The diameter of the black and grey circles are proportional to the number of samples sharing a same haplotype (see Table 2) (TIFF 178 kb)

705_2017_3439_MOESM2_ESM.tif

Haplotype network for HPV45 generated by median joining analysis, based on samples of Rio de Janeiro and Pará, medium vectors are indicated by red dots, and the circles in gray (Pará) or black (Rio de Janeiro) are the haplotypes. The diameter of the black and grey circles are proportional to the number of samples sharing a same haplotype (see Table 2) (TIFF 249 kb)

705_2017_3439_MOESM3_ESM.tif

Haplotype network for HPV58 generated by median joining analysis, based on samples of Rio de Janeiro and Pará, medium vectors are indicated by red dots, and the circles in gray (Pará) or black (Rio de Janeiro) are the haplotypes. The diameter of the black and grey circles are proportional to the number of samples sharing a same haplotype (see Table 2) (TIFF 211 kb)

Supplementary material 4 (DOC 29 kb)

Supplementary material 5 (XLS 110 kb)

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Basto, D.L., Vidal, J.P., Pontes, V.B. et al. Genetic diversity of human papillomavirus types 35, 45 and 58 in cervical cancer in Brazil. Arch Virol 162, 2855–2860 (2017). https://doi.org/10.1007/s00705-017-3439-5

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