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Viral metagenomics to track, explain and predict the transmission and spatiotemporal spread of Dengue and Chikungunya viruses in Brazil

Grant number: 17/00021-9
Support type:Scholarships in Brazil - Post-Doctorate
Effective date (Start): September 01, 2017
Effective date (End): August 31, 2021
Field of knowledge:Health Sciences - Medicine - Medical Clinics
Principal researcher:Ester Cerdeira Sabino
Grantee:Antonio Charlys da Costa
Home Institution: Faculdade de Medicina (FM). Universidade de São Paulo (USP). São Paulo , SP, Brazil
Associated research grant:18/14389-0 - Brazil-UK Centre for Arbovirus Discovery, Diagnosis, Genomics and Epidemiology (CADDE), AP.TEM

Abstract

Brazil is hyper-endemic for dengue, with over 10 million cases reported between 2000-2016. The transmission and dissemination of the four serotypes of dengue virus (DENV) is reported in the country through the mosquito vector (Aedes aegypti). Besides DENV, other two virus Chikungunya (CHIKV) and Zika (ZIKV) have already been introduced in Brazil and has caused severe epidemics, but the situation can be complicated even more as these have not yet started the period of rain. This project is a collaboration between researchers from the Institute of Tropical Medicine (IMT/USP), Oxford University (OU) and the Blood Systems Research Institute (BSRI) in an effort to reconstruct in detail the transmission dynamics of circulating viral strains in Brazil, using epidemiological data and the human host to better understand the pathogenesis of these viruses. The infrastructure already established by the Brazilian team has allowed the collection of individual blood samples from different cities in Brazil that will be included in the project and this project will be recruited other cities, which will allow the collection of isolates from current outbreaks of DENV, CHIKV and ZIKV. The aim of this study is to perform the viral metagenomics of samples collected in several Brazilian cities using next-generation sequencing to elucidate and predict the spatial dynamics and transmission of DENV, CHIKV and ZIKV in Brazil. At least 3000 from individuals that total nucleic acids are sequenced, the sequencing order of one or more viruses. The virus that through this approach are not completely sequenced will then be amplified and sequenced the missing parts. The obtained sequences are then subjected to mount "de novo" through a "pipeline" of BSRI for reconstruction of viral genomes, the consensus sequences generated will be submitted to genetic characterization focusing on the identification of transmission networks and viral spread. Then maximum likelihood and Bayesian phylogenetics will be reconstructed to determine the evolutionary relationships of the circulating strains in the national and global contexts. Best fitting nucleotide substitution, molecular clock, and coalescent models will be chosen using harmonic mean estimators, path sampling and stepping stone approaches. Rates of viral lineage movement among populations will be quantified using discrete phylogeographic approaches. Given the latitude and longitude coordinates of each isolate, we will also apply continuous diffusion models and summarize key epidemiological statistics such as dispersal velocity. Coalescent and birth-death skyline models will be used to estimate the rate of epidemic growth through time of different circulating lineages. Rates of synonymous and nonsynonymous changes will be quantified using renaissance counting and more recent algorithms for quantifying molecular adaptation being developed by the Oxford team. Viruses of dengue cases with the worst clinical outcomes will also be sequenced and analysed to see if there is any DENV sequence motif or mutational combination associated with severity. The association between disease severity and mutations will be tested using an association test that takes into account phylogenetic uncertainty. In summary, the study will combine genetic, ecological, clinical, and surveillance data to understand DENV, CHIKV and ZIKV epidemiology. Ultimately, the research proposed here aims to reduce the burden caused by important arbovirus outbreaks in Brazil, with potential benefits for both public health and vaccine development.

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Scientific publications (35)
(References retrieved automatically from Web of Science and SciELO through information on FAPESP grants and their corresponding numbers as mentioned in the publications by the authors)
LUCHS, ADRIANA; DA COSTA, ANTONIO CHARLYS; CILLI, AUDREY; VASCONCELOS KOMNINAKIS, SHIRLEY CAVALCANTE; COMPAGNOLI CARMONA, RITA DE CASSIA; BOEN, LAIS; MORILLO, SIMONE GUADAGNUCCI; SABINO, ESTER CERDEIRA; SAMPAIO TAVARES TIMENETSKY, MARIA DO CARMO. Spread of the emerging equine-like G3P[8] DS-1-like genetic backbone rotavirus strain in Brazil and identification of potential genetic variants. JOURNAL OF GENERAL VIROLOGY, v. 100, n. 1, p. 7-25, . (16/01735-2, 17/00021-9, 15/12944-9)
ARANHA WATANABE, ARIPUANA SAKURADA; LUCHS, ADRIANA; LEAL, ELCIO; DE PADUA MILAGRES, FLAVIO AUGUSTO; KOMNINAKIS, SHIRLEY VASCONCELOS; GILL, DANIELLE ELISE; BRITO SAYAO LOBATO, MARCIA CRISTINA ALVES; BRUSTULIN, RAFAEL; DAS CHAGAS, ROGERIO TOGISAKI; NEVES DOS SANTOS ABRAO, MARIA DE FATIMA; et al. Complete Genome Sequences of Six Human Bocavirus Strains from Patients with Acute Gastroenteritis in the North Region of Brazil. MICROBIOLOGY RESOURCE ANNOUNCEMENTS, v. 6, n. 17, . (15/12944-9, 16/01735-2, 17/00021-9)
ROSA, ULISSES ALVES; RIBEIRO, GEOVANI DE OLIVEIRA; VILLANOVA, FABIOLA; LUCHS, ADRIANA; DE PADUA MILAGRES, FLAVIO AUGUSTO; KOMNINAKIS, SHIRLEY VASCONCELOS; TAHMASEBI, ROOZBEH; BRITO SAYAO LOBATO, MARCIA CRISTINA ALVES; BRUSTULIN, RAFAEL; DAS CHAGAS, ROGERIO TOGISAKI; et al. First identification of mammalian orthoreovirus type 3 by gut virome analysis in diarrheic child in Brazil. SCIENTIFIC REPORTS, v. 9, . (15/12944-9, 17/00021-9, 16/01735-2)
RAMOS, ENDRYA DO SOCORRO FORO; RIBEIRO, GEOVANI DE OLIVEIRA; VILLANOVA, FABIOLA; MILAGRES, FLAVIO AUGUSTO DE PADUA; BRUSTULIN, RAFAEL; ARAUJO, EMERSON LUIZ LIMA; PANDEY, RAMENDRA PATI; RAJ, V. SAMUEL; DENG, XUTAO; DELWART, ERIC; et al. Composition of Eukaryotic Viruses and Bacteriophages in Individuals with Acute Gastroenteritis. Viruses-Basel, v. 13, n. 12, . (20/14786-0, 15/12944-9, 17/00021-9)
TINKER, RORY J.; DA COSTA, ANTONIO CHARLYS; TAHMASEBI, ROOZBEH; MILAGRES, FLAVIO AUGUSTO DE PADUA; DOS SANTOS MORAIS, VANESSA; PANDEY, RAMENDRA PATI; JOSE-ABREGO, ALEXIS; BRUSTULIN, RAFAEL; RODRIGUES TELES, MARIA DA APARECIDA; CUNHA, MARIANA SEQUETIN; et al. Norovirus strains in patients with acute gastroenteritis in rural and low-income urban areas in northern Brazil. ARCHIVES OF VIROLOGY, v. 166, n. 3, p. 905-913, . (17/00021-9, 15/12944-9, 16/01735-2, 19/21706-5)
RIBEIRO, GEOVANI DE OLIVEIRA; GILL, DANIELLE ELISE; ATHAIDE RIBEIRO, EDCELHA SOARES D.; COSTA MONTEIRO, FRED JULIO; MORAIS, VANESSA S.; MARCATTI, ROBERTA; REGO, MARLISSON OCTAVIO DA S.; ARAUJO, EMERSON LUIZ LIMA; WITKIN, STEVEN S.; VILLANOVA, FABIOLA; et al. Adaptive Evolution of New Variants of Dengue Virus Serotype 1 Genotype V Circulating in the Brazilian Amazon. Viruses-Basel, v. 13, n. 4, . (17/00021-9, 19/21706-5)
FORO RAMOS, ENDRYA DO SOCORRO; ROSA, ULISSES ALVES; RIBEIRO, GEOVANI DE OLIVEIRA; VILLANOVA, FABIOLA; DE PADUA MILAGRES, FLAVIO AUGUSTO; BRUSTULIN, RAFAEL; MORAIS, VANESSA DOS SANTOS; BERTANHE, MAYARA; MARCATTI, ROBERTA; ARAUJO, EMERSON LUIZ LIMA; et al. High Heterogeneity of Echoviruses in Brazilian Children with Acute Gastroenteritis. Viruses-Basel, v. 13, n. 4, . (19/21706-5, 17/00021-9, 15/12944-9)
DA ROCHA, LEONARDO CECILIO; ESTOFOLETE, CASSIA FERNANDA; GONCALVES DE AGUIAR MILHIM, BRUNO HENRIQUE; AUGUSTO, MARCOS TAYAR; ZINI, NATHALIA; DUTRA DA SILVA, GISLAINE CELESTINO; FERRAZ-JUNIOR, HELIO CORREA; SABADOTO BRIENZE, VANIA MARIA; LISO, ELISABETE; CUNHA, MARIANA SEQUETIN; et al. Enteric viruses circulating in undiagnosed central nervous system infections at tertiary hospital in Sao Jose do Rio Preto, Sao Paulo, Brazil. Journal of Medical Virology, v. 93, n. 6, . (13/21719-3, 16/15021-1, 17/00021-9, 15/12295-0)
TAHMASEBI, ROOZBEH; LUCHS, ADRIANA; TARDY, KAELAN; HEFFORD, PHILIP MICHAEL; TINKER, RORY J.; EILAMI, OWRANG; DE PADUA MILAGRES, FLAVIO AUGUSTO; BRUSTULIN, RAFAEL; RODRIGUES TELES, MARIA DA APARECIDA; MORAIS, VANESSA DOS SANTOS; et al. Viral gastroenteritis in Tocantins, Brazil: characterizing the diversity of human adenovirus F through next-generation sequencing and bioinformatics. JOURNAL OF GENERAL VIROLOGY, v. 101, n. 12, p. 1280-1288, . (19/21706-5, 17/00021-9)
VILLANOVA, FABIOLA; MARCATTI, ROBERTA; BERTANHE, MAYARA; MORAIS, VANESSA DOS SANTOS; DE PADUA MILAGRES, FLAVIO AUGUSTO; BRUSTULIN, RAFAEL; LIMA ARAUJO, EMERSON LUIZ; TAHMASEBI, ROOZBEH; WITKIN, STEVEN S.; DENG, XUTAO; et al. New Variants of Squash Mosaic Viruses Detected in Human Fecal Samples. MICROORGANISMS, v. 9, n. 7, . (17/00021-9, 19/21706-5)
LUCHS, ADRIANA; LEAL, ELCIO; KOMNINAKIS, SHIRLEY VASCONCELOS; DE PADUA MILAGRES, FLAVIO AUGUSTO; BRUSTULIN, RAFAEL; RODRIGUES TELES, MARIA DA APARECIDA; GILL, DANIELLE ELISE; DENG, XUTAO; DELWART, ERIC; SABINO, ESTER CERDEIRA; et al. Wuhan large pig roundworm virus identified in human feces in Brazil. VIRUS GENES, v. 54, n. 3, p. 470-473, . (16/01735-2, 17/00021-9, 15/12944-9)
FARIA, N. R.; KRAEMER, M. U. G.; HILL, S. C.; DE JESUS, J. GOES; AGUIAR, R. S.; IANI, F. C. M.; XAVIER, J.; QUICK, J.; DU PLESSIS, L.; DELLICOUR, S.; et al. Genomic and epidemiological monitoring of yellow fever virus transmission potential. Science, v. 361, n. 6405, p. 894+, . (16/01735-2, 17/00021-9)
DA COSTA, ANTONIO CHARLYS; LUCHS, ADRIANA; DE PADUA MILAGRES, FLAVIO AUGUSTO; KOMNINAKIS, SHIRLEY VASCONCELOS; GILL, DANIELLE ELISE; BRITO SAYAO LOBATO, MARCIA CRISTINA ALVES; BRUSTULIN, RAFAEL; DAS CHAGAS, ROGERIO TOGISAKI; NEVES DOS SANTOS ABRAO, MARIA DE FATIMA; DE DEUS ALVES SOARES, CASSIA VITORIA; et al. Near full length genome of a recombinant (E/D) cosavirus strain from a rural area in the central region of Brazil. SCIENTIFIC REPORTS, v. 8, . (16/01735-2, 17/00021-9, 15/12944-9)
FARIA, NUNO R.; DA COSTA, ANTONIO CHARLYS; LOURENCO, JOSE; LOUREIRO, PAULA; LOPES, MARIA ESTHER; RIBEIRO, ROBERTO; ALENCAR, CECILIA SALETE; KRAEMER, MORITZ U. G.; VILLABONA-ARENAS, CHRISTIAN J.; WU, CHIEH-HSI; et al. Genomic and epidemiological characterisation of a dengue virus outbreak among blood donors in Brazil. SCIENTIFIC REPORTS, v. 7, . (16/01735-2, 11/18955-1, 17/00021-9)
DA COSTA, ANTONIO CHARLYS; LEAL, ELCIO; GILL, DANIELLE; DE PADUA MILAGRES, FLAVIO AUGUSTO; KOMNINAKIS, SHIRLEY VASCONCELOS; BRUSTULIN, RAFAEL; RODRIGUES TELES, MARIA DA APARECIDA; BRITO SAYAO LOBATO, MARCIA CRISTINA ALVES; DAS CHAGAS, ROGERIO TOGISAKI; NEVES DOS SANTOS ABRAO, MARIA DE FATIMA; et al. Discovery of Cucumis melo endornavirus by deep sequencing of human stool samples in Brazil. VIRUS GENES, v. 55, n. 3, p. 332-338, . (16/01735-2, 17/00021-9, 15/12944-9)
DA COSTA, ANTONIO CHARLYS; THEZE, JULIEN; KOMNINAKIS, SHIRLEY CAVALCANTE VASCONCELOS; SANZ-DURO, RODRIGO LOPES; LEMOS FELINTO, MARTA REJANE; CORREA MOURA, LUCIA CRISTINA; DE OLIVEIRA BARROSO, IVONEIDE MOREIRA; CORREIA SANTOS, LUCINEIDE ELIZIARIO; DE LEMOS NUNES, MARDJANE ALVES; MOURA, ADRIANA AVILA; et al. Spread of Chikungunya Virus East/Central/South African Genotype in Northeast Brazil. Emerging Infectious Diseases, v. 23, n. 10, p. 1742-1744, . (16/01735-2, 17/00021-9, 12/03417-7)
FORO RAMOS, ENDRYA DO SOCORRO; ROSA, ULISSES ALVES; RIBEIRO, GEOVANI DE OLIVEIRA; VILLANOVA, FABIOLA; DE PADUA MILAGRES, FLAVIO AUGUSTO; BRUSTULIN, RAFAEL; MORAIS, VANESSA DOS SANTOS; LIMA ARAUJO, EMERSON LUIZ; PANDEY, RAMENDRA PATI; RAJ, V. SAMUEL; et al. Multiple clades of Husavirus in South America revealed by next generation sequencing. PLoS One, v. 16, n. 3, . (17/00021-9, 15/12944-9)
AUDREY CILLI; ADRIANA LUCHS; ELCIO LEAL; DANIELLE GILL; FLAVIO AUGUSTO DE PÁDUA MILAGRES; SHIRLEY VASCONCELOS KOMNINAKIS; RAFAEL BRUSTULIN; MARIA DA APARECIDA RODRIGUES TELES; MÁRCIA CRISTINA ALVES BRITO SAYÃO LOBATO; ROGÉRIO TOGISAKI DAS CHAGAS; et al. Human sapovirus GI.2 and GI.3 from children with acute gastroenteritis in northern Brazil. Memórias do Instituto Oswaldo Cruz, v. 114, . (17/00021-9, 15/12944-9, 16/01735-2)
LEAL, ELCIO; LUCHS, ADRIANA; DE PADUA MILAGRES, FLAVIO AUGUSTO; KOMNINAKIS, SHIRLEY VASCONCELOS; GILL, DANIELLE ELISE; BRITO SAYAO LOBATO, MARCIA CRISTINA ALVES; BRUSTULIN, RAFAEL; DAS CHAGAS, ROGERIO TOGISAKI; NEVES DOS SANTOS ABRAO, MARIA DE FATIMA; DE DEUS ALVES SOARES, CASSIA VITORIA; et al. Recombinant Strains of Human Parechovirus in Rural Areas in the North of Brazil. Viruses-Basel, v. 11, n. 6, . (15/12944-9, 17/00021-9, 16/01735-2)
RIBEIRO, GEOVANI DE OLIVEIRA; COSTA MONTEIRO, FRED JULIO; REGO, MARLISSON OCTAVIO DA S.; D'ATHAIDE RIBEIRO, EDCELHA SOARES; DE CASTRO, DANIELA FUNAYAMA; CASEIRO, MARCOS MONTANI; SOUZA MARINHO, ROBSON DOS SANTOS; KOMNINAKIS, SHIRLEY VASCONCELOS; WITKIN, STEVEN S.; DENG, XUTAO; et al. Detection of RNA-Dependent RNA Polymerase of Hubei Reo-Like Virus 7 by Next-Generation Sequencing in Aedes aegypti and Culex quinquefasciatus Mosquitoes from Brazil. Viruses-Basel, v. 11, n. 2, . (17/00021-9, 16/01735-2)
CUNHA, MARIANA SEQUETIN; DA COSTA, ANTONIO CHARLYS; COUTO DE AZEVEDO FERNANDES, NATALIA COELHO; GUERRA, JULIANA MARIOTTI; PEREIRA DOS SANTOS, FABIANA CRISTINA; NOGUEIRA, JULIANA SILVA; D'AGOSTINO, LEANDRO GUARIGLIA; KOMNINAKIS, SHIRLEY VASCONCELOS; WITKIN, STEVEN S.; RESSIO, RODRIGO ALBERGARIA; et al. Epizootics due to Yellow Fever Virus in Sao Paulo State, Brazil: viral dissemination to new areas (2016-2017). SCIENTIFIC REPORTS, v. 9, . (16/01735-2, 17/00021-9)
CUNHA, MARIANA SEQUETIN; FARIA, NUNO RODRIGUES; CALEIRO, GIOVANA SANTOS; CANDIDO, DARLAN SILVA; HILL, SARAH C.; CLARO, INGRA MORALES; DA COSTA, ANTONIO CHARLYS; NOGUEIRA, JULIANA SILVA; MAEDA, ADRIANA YURIKA; DA SILVA, FERNANDA GISELE; et al. Genomic evidence of yellow fever virus in Aedes scapularis, southeastern Brazil, 2016. Acta Tropica, v. 205, . (17/00021-9, 18/14389-0, 16/01735-2)
RIBEIRO, GEOVANI DE OLIVEIRA; DA COSTA, ANTONIO CHARLYS; GILL, DANIELLE ELISE; D'ATHAIDE RIBEIRO, EDCELHA SOARES; REGO, MARLISSON OCTAVIO DA S.; MONTEIRO, FRED JULIO COSTA; VILLANOVA, FABIOLA; NOGUEIRA, JULIANA SILVA; MAEDA, ADRIANA YURIKA; DE SOUZA, RENATO PEREIRA; et al. Guapiacu virus, a new insect-specific flavivirus isolated from two species of Aedes mosquitoes from Brazil. SCIENTIFIC REPORTS, v. 11, n. 1, . (19/21706-5, 16/01735-2, 13/21719-3, 12/23645-4, 17/00021-9)
ADRIANA LUCHS; LAIS SAMPAIO DE AZEVEDO; ELLEN VIANA DE SOUZA; ROBERTA SALZONE MEDEIROS; YASMIN FRANÇA VIANA PIRES DE SOUZA; DALANE LOUDAL FLORENTINO TEIXEIRA; THIAGO FRANCO DE OLIVEIRA CARNEIRO; GABRIELA MARIA FERNANDES DE ALENCAR; FERNANDA LÚCIA DE SOUSA LEITE MORAIS; DIANA DE FÁTIMA ALVES PINTO; et al. Coxsackievirus A6 strains causing an outbreak of hand-foot-and-mouth disease in Northeastern Brazil in 2018. Revista do Instituto de Medicina Tropical de São Paulo, v. 64, . (19/21706-5, 20/02469-0, 17/00021-9, 20/14786-0, 20/11182-6)
THAÍS DE MOURA COLETTI; CAMILA MALTA ROMANO; PAULO ROBERTO URBINATTI; RENILDO SOUZA TEIXEIRA; LEILA WEISS DE ALMEIDA PEDROSA; MARCELLO SCHIAVO NARDI; DELSIO NATAL; ANTÔNIO CHARLYS DA COSTA; JAQUELINE GOES DE JESUS; INGRA MORALES CLARO; et al. Characterization of insect-specific Culex flavivirus (Flaviviridae) nucleotide sequences in mosquitoes from urban parks in São Paulo, Brazil. Revista da Sociedade Brasileira de Medicina Tropical, v. 55, . (19/12000-1, 17/00021-9, 10/51230-8, 18/14389-0, 19/03859-9, 18/17176-8, 16/18204-0)
CASTRO, TALITA; SABALZA, MAITE; BARBER, CHERYL; ABRAMS, WILLIAM; DA COSTA, ANTONIO CHARLYS; DE PADUA MILAGRES, FLAVIO AUGUSTO; BRAZ-SILVA, PAULO HENRIQUE; MALAMUD, DANIEL; GALLOTTINI, MARINA. Rapid diagnosis of Zika virus through saliva and urine by Loop-mediated isothermal amplification (LAMP). JOURNAL OF ORAL MICROBIOLOGY, v. 10, n. 1, . (17/00021-9)
RIBEIRO, GEOVANI DE OLIVEIRA; LUCHS, ADRIANA; DE PADUA MILAGRES, FLAVIO AUGUSTO; KOMNINAKIS, SHIRLEY VASCONCELOS; GILL, DANIELLE ELISE; BRITO SAYAO LOBATO, MARCIA CRISTINA ALVES; BRUSTULIN, RAFAEL; DAS CHAGAS, ROGERIO TOGISAKI; NEVES DOS SANTOS ABRAO, MARIA DE FATIMA; DE DEUS ALVES SOARES, CASSIA VITORIA; et al. Detection and Characterization of Enterovirus B73 from a Child in Brazil. Viruses-Basel, v. 11, n. 1, . (15/12944-9, 17/00021-9, 16/01735-2)
DA COSTA, ANTONIO CHARLYS; LUCHS, ADRIANA; DE PADUA MILAGRES, FLAVIO AUGUSTO; KOMNINAKIS, SHIRLEY VASCONCELOS; GILL, DANIELLE ELISE; BRITO SAYAO LOBATO, MARCIA CRISTINA ALVES; BRUSTULIN, RAFAEL; DAS CHAGAS, ROGERIO TOGISAKI; NEVES DOS SANTOS ABRAO, MARIA DE FATIMA; DE DEUS ALVES SOARES, CASSIA VITORIA; et al. Recombination Located over 2A-2B Junction Ribosome Frameshifting Region of Saffold Cardiovirus. Viruses-Basel, v. 10, n. 10, . (15/12944-9, 16/01735-2, 17/00021-9)
FAHSBENDER, ELIZABETH; DA-COSTA, ANTONIO CHARLYS; GILL, DANIELLE ELISE; MILAGRES, FLAVIO AUGUSTO DE PADUA; BRUSTULIN, RAFAEL; MONTEIRO, FRED JULIO COSTA; REGO, MARLISSON OCTAVIO DA SILVA; RIBEIRO, EDCELHA SOARES D'ATHAIDE; SABINO, ESTER CERDEIRA; DELWART, ERIC. Plasma virome of 781 Brazilians with unexplained symptoms of arbovirus infection include a novel parvovirus and densovirus. PLoS One, v. 15, n. 3, . (17/00021-9, 16/01735-2)
CUNHA, MARIANA SEQUETIN; LUCHS, ADRIANA; DA COSTA, ANTONIO CHARLYS; RIBEIRO, GEOVANI DE OLIVEIRA; PEREIRA DOS SANTOS, FABIANA CRISTINA; NOGUEIRA, JULIANA SILVA; KOMNINAKIS, SHIRLEY VASCONCELOS; SOUZA MARINHO, ROBSON DOS SANTOS; WITKIN, STEVEN S.; VILLANOVA, FABIOLA; et al. Detection and characterization of Ilheus and Iguape virus genomes in historical mosquito samples from Southern Brazil. Acta Tropica, v. 205, . (17/00021-9, 16/01735-2)
FERNANDES, LICIA NATAL; COLETTI, THAIS DE MOURA; COSTA MONTEIRO, FRED JULIO; DA SILVA REGO, MARLISSON OCTAVIO; D'ATHAIDE RIBEIRO, EDCELHA SOARES; RIBEIRO, GEOVANI DE OLIVEIRA; SOUZA MARINHO, ROBSON DOS SANTOS; KOMNINAKIS, SHIRLEY VASCONCELOS; WITKIN, STEVEN S.; DENG, XUTAO; et al. A Novel Highly Divergent Strain of Cell Fusing Agent Virus (CFAV) in Mosquitoes from the Brazilian Amazon Region. Viruses-Basel, v. 10, n. 12, . (16/18204-0, 16/01735-2, 17/00021-9)
TAHMASEBI, ROOZBEH; DA COSTA, ANTONIO CHARLYS; TARDY, KAELAN; TINKER, RORY J.; DE PADUA MILAGRES, FLAVIO AUGUSTO; BRUSTULIN, RAFAEL; RODRIGUES TELES, MARIA DA APARECIDA; DAS CHAGAS, ROGERIO TOGISAKI; DE DEUS ALVES SOARES, CASSIA VITORIA; ARANHA WATANABE, ARIPUANA SAKURADA; et al. Genomic Analyses of Potential Novel Recombinant Human Adenovirus C in Brazil. Viruses-Basel, v. 12, n. 5, . (17/00021-9, 16/01735-2)
LUCHS, ADRIANA; TARDY, KAELAN; TAHMASEBI, ROOZBEH; MORILLO, SIMONE GUADAGNUCCI; MILAGRES, FLAVIO AUGUSTO DE PADUA; MORAIS, VANESSA DOS SANTOS; BRUSTULIN, RAFAEL; TELES, MARIA DA APARECIDA RODRIGUES; DE AZEVEDO, LAIS SAMPAIO; DE SOUZA, ELLEN VIANA; et al. Human astrovirus types 1, 4 and 5 circulating among children with acute gastroenteritis in a rural Brazilian state, 2010-2016. ARCHIVES OF VIROLOGY, v. 166, n. 11, . (19/21706-5, 15/12944-9, 17/00021-9, 20/11182-6, 20/02469-0, 16/01735-2)
RIBEIRO, GEOVANI DE OLIVEIRA; MORAIS, VANESSA S.; COSTA MONTEIRO, FRED JULIO; D'ATHAIDE RIBEIRO, EDCELHA SOARES; REGO, MARLISSON OCTAVIO DA S.; PICANCO SOUTO, RAIMUNDO NONATO; VILLANOVA, FABIOLA; TAHMASEBI, ROOZBEH; HEFFORD, PHILIP MICHAEL; DENG, XUTAO; et al. Aedes aegyptifrom Amazon Basin Harbor High Diversity of Novel Viral Species. Viruses-Basel, v. 12, n. 8, . (16/01735-2, 19/21706-5, 17/00021-9)
MARCELLE SILVA-SALES; ELCIO LEAL; FLAVIO AUGUSTO DE PÁDUA MILAGRES; RAFAEL BRUSTULIN; VANESSA DOS SANTOS MORAIS; ROBERTA MARCATTI; EMERSON LUIZ LIMA ARAÚJO; STEVEN S. WITKIN; XUTAO DENG; ESTER CERDEIRA SABINO; et al. Genomic constellation of human Rotavirus A strains identified in Northern Brazil: a 6-year follow-up (2010-2016). Revista do Instituto de Medicina Tropical de São Paulo, v. 62, . (17/00021-9, 19/21706-5, 15/12944-9)

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