Characterization of multiple human papillomavirus types in the human vagina following ovarian hormonal stimulation.

Humans Female Vagina / virology Papillomavirus Infections / virology Adult Phylogeny Papillomaviridae / genetics Ovulation Induction DNA, Viral / genetics Sequence Analysis, DNA Young Adult Metagenomics Genotype Human Papillomavirus Viruses
Alphapapillomavirus Gammapapillomavirus Ovarian hormonal stimulation Viral metagenomics

Journal

Virology journal
ISSN: 1743-422X
Titre abrégé: Virol J
Pays: England
ID NLM: 101231645

Informations de publication

Date de publication:
27 Sep 2024
Historique:
received: 15 07 2024
accepted: 17 09 2024
medline: 28 9 2024
pubmed: 28 9 2024
entrez: 28 9 2024
Statut: epublish

Résumé

The objective of study was to characterize HPV in vaginal samples from women being seen at the Center for Reproductive Medicine and Infertility at Weill Cornell Medicine before and following ovarian stimulation. A total of 29 women made samples available for analysis by viral metagenomics. Eighteen women were HPV-positive, six (33.3%) at their initial visit and 15 (83.3%) following hormone stimulation (p = 0.0059). Pairwise comparison of nucleotide sequences and phylogenetic analysis showed the classification sequences into two genera: Alphapapillomavirus and Gammapapillomavirus. Sequences were from 8 HPV types: HPV 51 (n = 2), HPV 68 (n = 1), HPV 83 (n = 9), HPV 84 (n = 2), HPV 121 (n = 6), HPV 175 (n = 1) and HPV 190 (n = 1). Additionally, C16b and C30 likely represent new types. In summary, multiple HPV types are present in the vagina of reproductive age women and are induced by hormone used to stimulate ovulation.

Identifiants

DOI: 10.1186/s12985-024-02507-7 PMID: 39334144
pubmed: 39334144
doi: 10.1186/s12985-024-02507-7
pii: 10.1186/s12985-024-02507-7
doi:

Substances chimiques

DNA, Viral 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

229

Subventions

Organisme : scholarship provided by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brasil
ID : CAPES
Organisme : scholarship provided by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brasil
ID : CAPES
Organisme : scholarship from HCFMUSP with funds donated by NUBANK under the #HCCOMVIDA scheme
ID : HCFMUSP

Informations de copyright

© 2024. The Author(s).

Références

Liu Z, Yang S, Wang Y, Shen Q, Yang Y, Deng X, Zhang W, Delwart E. Identification of a Novel Human Papillomavirus by Metagenomic Analysis of Vaginal Swab Samples from pregnant women. Virol J. 2016;13. https://doi.org/10.1186/s12985-016-0583-6 .
Kraberger S, Austin C, Farkas K, Desvignes T, Postlethwait JH, Fontenele RS, Schmidlin K, Bradley RW, Warzybok P, Van Doorslaer K, et al. Discovery of Novel Fish papillomaviruses: from the Antarctic to the commercial Fish Market. Virology. 2022;565:65–72. https://doi.org/10.1016/j.virol.2021.10.007 .
doi: 10.1016/j.virol.2021.10.007 pubmed: 34739918
Chen Z, Van Doorslaer K, DeSalle R, Wood CE, Kaplan JR, Wagner JD, Burk RD. Genomic diversity and Interspecies Host Infection of Α12 Macaca Fascicularis Papillomaviruses (MfPVs). Virology. 2009;393:304–10. https://doi.org/10.1016/j.virol.2009.07.012 .
doi: 10.1016/j.virol.2009.07.012 pubmed: 19716580
Van Doorslaer K, Chen Z, Bernard H-U, Chan PKS, DeSalle R, Dillner J, Forslund O, Haga T, McBride AA, Villa LL, et al. ICTV Virus Taxonomy Profile: Papillomaviridae. J Gen Virol. 2018;99:989–90. https://doi.org/10.1099/jgv.0.001105 .
doi: 10.1099/jgv.0.001105 pmcid: 6171710 pubmed: 29927370
Bergvall M, Melendy T, Archambault J. The E1 proteins. Virology. 2013;445:35–56. https://doi.org/10.1016/j.virol.2013.07.020 .
doi: 10.1016/j.virol.2013.07.020 pubmed: 24029589
McBride AA, The Papillomavirus E, Proteins. Virology. 2013;445:57–79. https://doi.org/10.1016/j.virol.2013.06.006 .
doi: 10.1016/j.virol.2013.06.006 pubmed: 23849793
Willemsen A, Bravo IG. Origin and evolution of Papillomavirus (Onco)genes and genomes. Phil Trans R Soc B. 2019;374. https://doi.org/10.1098/rstb.2018.0303 .
DiMaio D, Petti LM. The E5 proteins. Virology. 2013;445:99–114. https://doi.org/10.1016/j.virol.2013.05.006 .
doi: 10.1016/j.virol.2013.05.006 pubmed: 23731971
Doorbar J. The E4 protein; structure, function and patterns of expression. Virology. 2013;445:80–98. https://doi.org/10.1016/j.virol.2013.07.008 .
doi: 10.1016/j.virol.2013.07.008 pubmed: 24016539
Buck CB, Day PM, Trus BL. The Papillomavirus Major Capsid protein L1. Virology. 2013;445:169–74. https://doi.org/10.1016/j.virol.2013.05.038 .
doi: 10.1016/j.virol.2013.05.038 pubmed: 23800545
Wang JW, Roden RBS. L2, the minor capsid protein of Papillomavirus. Virology. 2013;445:175–86. https://doi.org/10.1016/j.virol.2013.04.017 .
doi: 10.1016/j.virol.2013.04.017 pubmed: 23689062
Bernard H-U. Regulatory Elements in the viral genome. Virology. 2013;445:197–204. https://doi.org/10.1016/j.virol.2013.04.035 .
doi: 10.1016/j.virol.2013.04.035 pubmed: 23725692
Bernard H-U, Burk RD, Chen Z, Van Doorslaer K, Hausen HZ, De Villiers E-M. Classification of Papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology. 2010;401:70–9. https://doi.org/10.1016/j.virol.2010.02.002 .
doi: 10.1016/j.virol.2010.02.002 pubmed: 20206957
Van Doorslaer K, Tan Q, Xirasagar S, Bandaru S, Gopalan V, Mohamoud Y, Huyen Y, McBride AA. The Papillomavirus Episteme: a Central Resource for Papillomavirus sequence data and analysis. Nucleic Acids Res. 2012;41:D571–8. https://doi.org/10.1093/nar/gks984 .
doi: 10.1093/nar/gks984 pmcid: 3531071 pubmed: 23093593
De Villiers E-M, Fauquet C, Broker TR, Bernard H-U, Zur Hausen H. Classification of Papillomaviruses. Virology. 2004;324:17–27. https://doi.org/10.1016/j.virol.2004.03.033 .
doi: 10.1016/j.virol.2004.03.033 pubmed: 15183049
De Villiers E-M. Cross-roads in the classification of Papillomaviruses. Virology. 2013;445:2–10. https://doi.org/10.1016/j.virol.2013.04.023 .
doi: 10.1016/j.virol.2013.04.023 pubmed: 23683837
Bzhalava D, Eklund C, Dillner J. International standardization and classification of human papillomavirus types. Virology. 2015;476:341–4. https://doi.org/10.1016/j.virol.2014.12.028 .
doi: 10.1016/j.virol.2014.12.028 pubmed: 25577151
Harari A, Chen Z, Burk RD. Human Papillomavirus Genomics: Past, Present and Future. In Current Problems in Dermatology; Ramírez-Fort, M.K., Khan, F., Rady, P.L., Tyring, S.K., Eds.; S. Karger AG, 2014; Vol. 45, pp. 1–18 ISBN 9783318025262.
Cubie HA. Diseases Associated with human papillomavirus infection. Virology. 2013;445:21–34. https://doi.org/10.1016/j.virol.2013.06.007 .
doi: 10.1016/j.virol.2013.06.007 pubmed: 23932731
Zhou Y, Shi X, Liu J, Zhang L. Correlation between human papillomavirus viral load and cervical lesions classification: a review of current research. Front Med (Lausanne). 2023;10:1111269. https://doi.org/10.3389/fmed.2023.1111269 .
doi: 10.3389/fmed.2023.1111269 pubmed: 36895724
Alhamlan FS, Alfageeh MB, Al Mushait MA, Al-Badawi IA, Al-Ahdal MN. Human Papillomavirus-Associated Cancers. Adv Exp Med Biol. 2021;1313:1–14. https://doi.org/10.1007/978-3-030-67452-6_1 .
doi: 10.1007/978-3-030-67452-6_1 pubmed: 34661888
Egawa N. Papillomaviruses and Cancer: commonalities and differences in HPV Carcinogenesis at different sites of the body. Int J Clin Oncol. 2023;28:956–64. https://doi.org/10.1007/s10147-023-02340-y .
doi: 10.1007/s10147-023-02340-y pmcid: 10390352 pubmed: 37199886
Global Cancer Burden Growing, amidst Mounting Need for Services Available online. https://www.who.int/news/item/01-02-2024-global-cancer-burden-growing--amidst-mounting-need-for-services (accessed on 10 February 2024).
Lewis RM, Laprise J-F, Gargano JW, Unger ER, Querec TD, Chesson HW, Brisson M, Markowitz LE. Estimated prevalence and incidence of Disease-Associated Human Papillomavirus types among 15- to 59-Year-Olds in the United States. Sex Trans Dis. 2021;48:273–7. https://doi.org/10.1097/OLQ.0000000000001356 .
doi: 10.1097/OLQ.0000000000001356
Suk R, Hong Y-R, Rajan SS, Xie Z, Zhu Y, Spencer JC. Assessment of US Preventive Services Task Force Guideline–Concordant Cervical Cancer Screening Rates and reasons for underscreening by Age, race and ethnicity, sexual orientation, rurality, and insurance, 2005 to 2019. JAMA Netw Open. 2022;5:e2143582. https://doi.org/10.1001/jamanetworkopen.2021.43582 .
doi: 10.1001/jamanetworkopen.2021.43582 pmcid: 8767443 pubmed: 35040970
Bouvard V, Baan R, Straif K, Grosse Y, Secretan B, Ghissassi FE, Benbrahim-Tallaa L, Guha N, Freeman C, Galichet L, et al. Rev Hum Carcinogens—Part B: Biol Agents Lancet Oncol. 2009;10:321–2. https://doi.org/10.1016/S1470-2045(09)70096-8 .
doi: 10.1016/S1470-2045(09)70096-8
Gheit T. Mucosal and cutaneous human papillomavirus infections and Cancer Biology. Front Oncol. 2019;9:355. https://doi.org/10.3389/fonc.2019.00355 .
doi: 10.3389/fonc.2019.00355 pmcid: 6517478 pubmed: 31134154
Viens LJ, Henley SJ, Watson M, Markowitz LE, Thomas CC, Thompson TD, Razzaghi H, Saraiya M. Human papillomavirus–Associated Cancers — United States, 2008–2012. MMWR Morb Mortal Wkly Rep. 2016;65:661–6. https://doi.org/10.15585/mmwr.mm6526a1 .
doi: 10.15585/mmwr.mm6526a1 pubmed: 27387669
Den Boon JA, Pyeon D, Wang SS, Horswill M, Schiffman M, Sherman M, Zuna RE, Wang Z, Hewitt SM, Pearson R et al. Molecular Transitions from Papillomavirus Infection to Cervical Precancer and Cancer: Role of Stromal Estrogen Receptor Signaling. Proc. Natl. Acad. Sci. U.S.A. 2015, 112, https://doi.org/10.1073/pnas.1509322112
Zhai Y, Bommer GT, Feng Y, Wiese AB, Fearon ER, Cho KR. Loss of Estrogen Receptor 1 enhances cervical Cancer Invasion. Am J Pathol. 2010;177:884–95. https://doi.org/10.2353/ajpath.2010.091166 .
doi: 10.2353/ajpath.2010.091166 pmcid: 2913367 pubmed: 20581058
Pagano MT, Ortona E, Dupuis ML. A role for estrogen receptor Alpha36 in Cancer Progression. Front Endocrinol. 2020;11:506. https://doi.org/10.3389/fendo.2020.00506 .
doi: 10.3389/fendo.2020.00506
Ranganathan P, Nadig N, Nambiar S. Non-canonical Estrogen Signaling in Endocrine Resistance. Front Endocrinol. 2019;10:708. https://doi.org/10.3389/fendo.2019.00708 .
doi: 10.3389/fendo.2019.00708
Li B, Zhang L, Zhao J, Tan G, Zhang W, Zhang N, Tian J, Qu P. The value of cytokine levels in triage and risk prediction for women with Persistent High-Risk Human Papilloma Virus infection of the Cervix. Infect Agents Cancer. 2019;14:16. https://doi.org/10.1186/s13027-019-0231-z .
doi: 10.1186/s13027-019-0231-z
Nguyen HH, Broker TR, Chow LT, Alvarez RD, Vu HL, Andrasi J, Brewer LR, Jin G, Mestecky J. Immune responses to human papillomavirus in genital tract of women with cervical Cancer. Gynecol Oncol. 2005;96:452–61. https://doi.org/10.1016/j.ygyno.2004.10.019 .
doi: 10.1016/j.ygyno.2004.10.019 pubmed: 15661235
Hammes L, Tekmal R, Naud P, Edelweiss M, Kirma N, Valente P, Syrjanen K, Cunhafilho J, Macrophages. Inflammation and risk of cervical intraepithelial neoplasia (CIN) progression—clinicopathological correlation. Gynecol Oncol. 2007;105:157–65. https://doi.org/10.1016/j.ygyno.2006.11.023 .
doi: 10.1016/j.ygyno.2006.11.023 pubmed: 17229459
Lagenaur LA, Hemmerling A, Chiu C, Miller S, Lee PP, Cohen CR, Parks TP. Connecting the dots: translating the vaginal Microbiome into a drug. J Infect Dis. 2021;223:S296–306. https://doi.org/10.1093/infdis/jiaa676 .
doi: 10.1093/infdis/jiaa676 pubmed: 33330916
Stevanović S, Pasetto A, Helman SR, Gartner JJ, Prickett TD, Howie B, Robins HS, Robbins PF, Klebanoff CA, Rosenberg SA, et al. Landscape of Immunogenic Tumor Antigens in successful immunotherapy of Virally Induced Epithelial Cancer. Science. 2017;356:200–5. https://doi.org/10.1126/science.aak9510 .
doi: 10.1126/science.aak9510 pmcid: 6295311 pubmed: 28408606
Wang J, Chitsaz F, Derbyshire MK, Gonzales NR, Gwadz M, Lu S, Marchler GH, Song JS, Thanki N, Yamashita RA, et al. The conserved domain database in 2023. Nucleic Acids Res. 2023;51:D384–8. https://doi.org/10.1093/nar/gkac1096 .
doi: 10.1093/nar/gkac1096 pubmed: 36477806
Okonechnikov K, Golosova O, Fursov M. The UGENE team Unipro UGENE: a unified Bioinformatics Toolkit. Bioinformatics. 2012;28:1166–7. https://doi.org/10.1093/bioinformatics/bts091 .
doi: 10.1093/bioinformatics/bts091 pubmed: 22368248
Trifinopoulos J, Nguyen L-T, von Haeseler A, Minh BQ, W-IQ-TREE. A fast online phylogenetic Tool for Maximum Likelihood Analysis. Nucleic Acids Res. 2016;44:W232–5. https://doi.org/10.1093/nar/gkw256 .
doi: 10.1093/nar/gkw256 pmcid: 4987875 pubmed: 27084950
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing platforms. Mol Biol Evol. 2018;35:1547–9. https://doi.org/10.1093/molbev/msy096 .
doi: 10.1093/molbev/msy096 pmcid: 5967553 pubmed: 29722887
Muhire BM, Varsani A, Martin DP, SDT. A virus classification Tool based on pairwise sequence alignment and identity calculation. PLoS ONE. 2014;9:e108277. https://doi.org/10.1371/journal.pone.0108277 .
doi: 10.1371/journal.pone.0108277 pmcid: 4178126 pubmed: 25259891
Edgar RC, MUSCLE. A multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics. 2004;5. https://doi.org/10.1186/1471-2105-5-113 .
Felsenstein J. Evolutionary trees from DNA sequences: a Maximum Likelihood Approach. J Mol Evol. 1981;17:368–76. https://doi.org/10.1007/BF01734359 .
doi: 10.1007/BF01734359 pubmed: 7288891
Tommasino M. The Biology of Beta Human papillomaviruses. Virus Res. 2017;231:128–38. https://doi.org/10.1016/j.virusres.2016.11.013 .
doi: 10.1016/j.virusres.2016.11.013 pubmed: 27856220
Ganti K, Broniarczyk J, Manoubi W, Massimi P, Mittal S, Pim D, Szalmas A, Thatte J, Thomas M, Tomaić V, et al. The human papillomavirus E6 PDZ binding motif: from life cycle to Malignancy. Viruses. 2015;7:3530–51. https://doi.org/10.3390/v7072785 .
doi: 10.3390/v7072785 pmcid: 4517114 pubmed: 26147797
Giarrè M, Caldeira S, Malanchi I, Ciccolini F, Leão MJ, Tommasino M. Induction of pRb degradation by the human papillomavirus type 16 E7 protein is essential to efficiently overcome p16INK4a-Imposed G1 cell cycle arrest. J Virol. 2001;75:4705–12. https://doi.org/10.1128/JVI.75.10.4705-4712.2001 .
doi: 10.1128/JVI.75.10.4705-4712.2001 pmcid: 114225 pubmed: 11312342
Harden ME, Munger K. Human papillomavirus Molecular Biology. Mutat Research/Reviews Mutat Res. 2017;772:3–12. https://doi.org/10.1016/j.mrrev.2016.07.002 .
doi: 10.1016/j.mrrev.2016.07.002
Van Doorslaer K. Evolution of the Papillomaviridae. Virology. 2013;445:11–20. https://doi.org/10.1016/j.virol.2013.05.012 .
doi: 10.1016/j.virol.2013.05.012 pubmed: 23769415
Kombe Kombe AJ, Li B, Zahid A, Mengist HM, Bounda G-A, Zhou Y, Jin T. Epidemiology and Burden of Human Papillomavirus and Related diseases, Molecular Pathogenesis, and vaccine evaluation. Front Public Health. 2021;8:552028. https://doi.org/10.3389/fpubh.2020.552028 .
doi: 10.3389/fpubh.2020.552028 pmcid: 7855977 pubmed: 33553082
Mittal R, Tsutsumi K, Pater A, Pater MM. Human papillomavirus type 16 expression in cervical keratinocytes: role of progesterone and glucocorticoid hormones. Gynecol Oncol. 1993;81:5–12.
Strehler E, Sterzik K, Malthaner D, Hoyer H, Nindl I, Schneider A. Influence of ovarian stimulation on the detection of human papillomavirus DNA in cervical scrapes obtained from patients undergoing assisted reproductive techniques. Fertil Steril. 1999;71:815–20.
doi: 10.1016/S0015-0282(99)00012-6 pubmed: 10231038
Zullo F, Fiano V, Gilio-Tos A, Leoncini S, Nesi G, Macri L, Preti M, Rolfo A, Benedetto C, Revelli A, De Marco L. Human papillomavirus infection in women undergoing in-vitro fertilization: effects on embryo development kinetics and live birth rate. Reproductive Biology Endocrinol. 2023;21:39–46.
doi: 10.1186/s12958-023-01091-9
Burchell AN, Winer RL, De Sanjosé S, Franco EL. Chapter 6: Epidemiology and Transmission Dynamics of Genital HPV Infection. Vaccine 2006, 24, S52–S61, https://doi.org/10.1016/j.vaccine.2006.05.031
Dickson EL, Vogel RI, Geller MA, Downs LS. Cervical cytology and multiple type HPV infection: a study of 8182 women ages 31–65. Gynecol Oncol. 2014;133:405–8. https://doi.org/10.1016/j.ygyno.2014.03.552 .
doi: 10.1016/j.ygyno.2014.03.552 pmcid: 4040336 pubmed: 24657488
Liu S, Li Y, Song Y, Wu X, Baloch Z, Xia X. The diversity of vaginal microbiome in women infected with single HPV and multiple genotype HPV infections in China. Front Cell Infect Microbiol. 2022;12:642074. https://doi.org/10.3389/fcimb.2022.642074 .
doi: 10.3389/fcimb.2022.642074 pmcid: 9806233 pubmed: 36601309
Hariri S, Unger ER, Sternberg M, Dunne EF, Swan D, Patel S, Markowitz LE. Prevalence of Genital Human Papillomavirus among females in the United States, the National Health and Nutrition Examination Survey, 2003–2006. J Infect Dis. 2011;204:566–73. https://doi.org/10.1093/infdis/jir341 .
doi: 10.1093/infdis/jir341 pubmed: 21791659
Meiring TL, Mbulawa ZZA, Lesosky M, Coetzee D, Williamson A-L. Alta diversidade de papilomavírus humanos alfa, beta e gama em amostras genitais de Homens Sul-Africanos Heterossexuais HIV negativos e HIV positivos. Pesquisa Sobre Papilomavírus. 2017;3:160–7. https://doi.org/10.1016/j.pvr.2017.05.001 .
doi: 10.1016/j.pvr.2017.05.001
Arroyo Mühr LS, Eklund C, Dillner J. Misclassifications in human papillomavirus databases. Virology. 2021;558:57–66. https://doi.org/10.1016/j.virol.2021.03.002 .
doi: 10.1016/j.virol.2021.03.002 pubmed: 33730650
Murahwa AT, Meiring TL, Mbulawa ZZA, Williamson A-L. Complete genome sequences of four Novel Human Gammapapillomavirus types, HPV-219, HPV-220, HPV-221, and HPV-222, isolated from Penile skin swabs from South African men. Genome Announc. 2018;6:e00584–18. https://doi.org/10.1128/genomeA.00584-18 .
doi: 10.1128/genomeA.00584-18 pmcid: 6013601 pubmed: 29930074
NISC Comparative Sequencing Program, Tirosh O, Conlan S, Deming C, Lee-Lin S-Q, Huang X, Su HC, Freeman AF, Segre JA, Kong HH. Expanded skin virome in DOCK8-Deficient patients. Nat Med. 2018;24:1815–21. https://doi.org/10.1038/s41591-018-0211-7 .
doi: 10.1038/s41591-018-0211-7
Van Doorslaer K. Revisiting Papillomavirus Taxonomy: a proposal for updating the current classification in line with evolutionary evidence. Viruses. 2022;14:2308. https://doi.org/10.3390/v14102308 .
doi: 10.3390/v14102308 pmcid: 9612317 pubmed: 36298863

Auteurs

Endrya do Socorro Foro Ramos (EDS)

Viral Diversity Laboratory, Institute of Biological Sciences, Federal University of Pará, Belem, Pará, Brazil.

Roseane da Silva Couto (R)

Viral Diversity Laboratory, Institute of Biological Sciences, Federal University of Pará, Belem, Pará, Brazil.

Tania Regina Tozetto-Mendoza (TR)

Medical Research Laboratory in Virology (LIM 52), Faculty of Medicine, University of São Paulo-Institute of Tropical Medicine de São Paulo, São Paulo, Brazil.

Pietro Bortoletto (P)

Boston IVF, Waltham, MA, USA.
Harvard Medical School, Boston, MA, USA.
Department of Obstetrics and Gynecology, Beth Israel Deaconess Medical Center, Boston, MA, USA.

Erick Matheus Garcia Barbosa (EMG)

Medical Research Laboratory in Virology (LIM 52), Faculty of Medicine, University of São Paulo-Institute of Tropical Medicine de São Paulo, São Paulo, Brazil.

Noely Evangelista Ferreira (NE)

Medical Research Laboratory in Virology (LIM 52), Faculty of Medicine, University of São Paulo-Institute of Tropical Medicine de São Paulo, São Paulo, Brazil.

Iara M Linhares (IM)

Department of Gynecology and Obstetrics, Faculty of Medicine, University of Sao Paulo, Sao Paulo, Brazil.

Steven D Spandorfer (SD)

Center for Reproductive Medicine and Infertility, Weill Cornell Medicine, New York, USA.

Antonio Charlys da Costa (AC)

Medical Research Laboratory in Virology (LIM 52), Faculty of Medicine, University of São Paulo-Institute of Tropical Medicine de São Paulo, São Paulo, Brazil. charlysbr@yahoo.com.br.

Elcio Leal (E)

Viral Diversity Laboratory, Institute of Biological Sciences, Federal University of Pará, Belem, Pará, Brazil. elcioleal@gmail.com.

Maria Cassia Mendes-Correa (MC)

Medical Research Laboratory in Virology (LIM 52), Faculty of Medicine, University of São Paulo-Institute of Tropical Medicine de São Paulo, São Paulo, Brazil. maria.cassia@hc.fm.usp.br.

Steven S Witkin (SS)

Medical Research Laboratory in Virology (LIM 52), Faculty of Medicine, University of São Paulo-Institute of Tropical Medicine de São Paulo, São Paulo, Brazil. switkin@med.cornell.edu.
Department of Obstetrics and Gynecology, Weill Cornell Medicine, New York, USA. switkin@med.cornell.edu.

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