Zika virus in the Americas: Early epidemiological and genetic findings

Zika virus genomes from Brazil The Zika virus outbreak is a major cause for concern in Brazil, where it has been linked with increased reports of otherwise rare birth defects and neuropathology. In a phylogenetic analysis, Faria et al. infer a single introduction of Zika to the Americas and estimated the introduction date to be about May to December 2013—some 12 months earlier than the virus was reported. This timing correlates with major events in the Brazilian cultural calendar associated with increased traveler numbers from areas where Zika virus has been circulating. A correlation was also observed between incidences of microcephaly and week 17 of pregnancy. Science, this issue p. 345 Virus sequencing indicates that Zika arrived in Brazil during the middle of 2013, coincident with a surge in air travelers. Brazil has experienced an unprecedented epidemic of Zika virus (ZIKV), with ~30,000 cases reported to date. ZIKV was first detected in Brazil in May 2015, and cases of microcephaly potentially associated with ZIKV infection were identified in November 2015. We performed next-generation sequencing to generate seven Brazilian ZIKV genomes sampled from four self-limited cases, one blood donor, one fatal adult case, and one newborn with microcephaly and congenital malformations. Results of phylogenetic and molecular clock analyses show a single introduction of ZIKV into the Americas, which we estimated to have occurred between May and December 2013, more than 12 months before the detection of ZIKV in Brazil. The estimated date of origin coincides with an increase in air passengers to Brazil from ZIKV-endemic areas, as well as with reported outbreaks in the Pacific Islands. ZIKV genomes from Brazil are phylogenetically interspersed with those from other South American and Caribbean countries. Mapping mutations onto existing structural models revealed the context of viral amino acid changes present in the outbreak lineage; however, no shared amino acid changes were found among the three currently available virus genomes from microcephaly cases. Municipality-level incidence data indicate that reports of suspected microcephaly in Brazil best correlate with ZIKV incidence around week 17 of pregnancy, although this correlation does not demonstrate causation. Our genetic description and analysis of ZIKV isolates in Brazil provide a baseline for future studies of the evolution and molecular epidemiology of this emerging virus in the Americas.

Giovanini Evelim Coelho | Simon I. Hay | Leandro Abade | Oliver G. Pybus | Iray Maria Rocco | Jane P. Messina | Luiz Carlos Junior Alcantara | Michael B. Bonsall | José Lourenço | Moritz U. G. Kraemer | Marta Giovanetti | Robert Tesh | Julien Thézé | Kamran Khan | Ilona Rissanen | S. Hay | M. Kraemer | K. Khan | O. Pybus | R. Tesh | M. Bonsall | J. Messina | P. F. Vasconcelos | N. Faria | I. Rissanen | T. Bowden | J. Cardoso | M. Nunes | C. D. de Lima | L. Alcântara | J. Thézé | Wanderson K. de Oliveira | M. Giovanetti | R. S. Azevedo | L. C. Martins | L. M. Casseb | S. Rodrigues | G. Coelho | J. Lourenço | Marisa Creatore | E. Delatorre | G. Bello | R. Souza | M. S. Cunha | S. Hill | I. M. Rocco | J. Nogueira | A. Maeda | F. G. Vasami | F. Macedo | A. Suzuki | A. C. Cruz | B. Nunes | D. B. Medeiros | D. S. G. Rodrigues | Alice Louize Nunes Queiroz | E. P. Silva | D. F. Henriques | E. S. Travassos da Rosa | C. S. de Oliveira | H. B. Vasconcelos | D. B. Simith | L. Abade | M. Lima | Rodrigo Santos de Oliveira | P. Lemos | L. Oliveira | S. P. da Silva | J. M. Vasconcelos | L. Franco | J. L. S. G. Vianez-Júnior | D. Mir | Wanderson Kleber de Oliveira | Edson Delatorre | Gonzalo Bello | Nuno Rodrigues Faria | Marcio R. T. Nunes | Thomas A. Bowden | Akemi Suzuki | Raimunda do Socorro da Silva Azevedo | Renato Souza | Mariana Sequetin Cunha | Sarah C. Hill | Juliana Silva Nogueira | Adriana Yurika Maeda | Fernanda Giseli da Silva Vasami | Fernando Luiz de Lima Macedo | Sueli Guerreiro Rodrigues | Ana Cecilia Ribeiro Cruz | Bruno Tardeli Nunes | Daniele Barbosa de Almeida Medeiros | Daniela Sueli Guerreiro Rodrigues | Eliana Vieira Pinto da Silva | Daniele Freitas Henriques | Elisabeth Salbe Travassos da Rosa | Consuelo Silva de Oliveira | Livia Caricio Martins | Helena Baldez Vasconcelos | Livia Medeiros Neves Casseb | Darlene de Brito Simith | Maricélia Maia de Lima | Poliana da Silva Lemos | Layanna Freitas de Oliveira | Clayton Pereira Silva de Lima | Sandro Patroca da Silva | Janaina Mota de Vasconcelos | Luciano Franco | Jedson Ferreira Cardoso | João Lídio da Silva Gonçalves Vianez-Júnior | Daiana Mir | Marisa Creatore | Pedro F. C. Vasconcelos | C. P. S. de Lima | P. Vasconcelos | E. Silva | F. L. L. Macedo | Eliana V. P. Silva | I. Rocco | Fernando L L Macedo

[1]  G. G. Stokes "J." , 1890, The New Yale Book of Quotations.

[2]  Catherine Linard,et al.  High-resolution gridded population datasets for Latin America and the Caribbean in 2010, 2015, and 2020 , 2015, Scientific Data.

[3]  Oumar Faye,et al.  Quantitative real-time PCR detection of Zika virus and evaluation with field-caught Mosquitoes , 2013, Virology Journal.

[4]  F. Barros,et al.  Microcephaly in Brazil: how to interpret reported numbers? , 2016, The Lancet.

[5]  K. Leder,et al.  Zika virus infection acquired during brief travel to Indonesia. , 2013, The American journal of tropical medicine and hygiene.

[6]  W. T. Hancock,et al.  Zika Virus, French Polynesia, South Pacific, 2013 , 2014, Emerging infectious diseases.

[7]  Forrest W. Crawford,et al.  Unifying the spatial epidemiology and molecular evolution of emerging epidemics , 2012, Proceedings of the National Academy of Sciences.

[8]  M. Suchard,et al.  Unifying Viral Genetics and Human Transportation Data to Predict the Global Transmission Dynamics of Human Influenza H3N2 , 2014, PLoS pathogens.

[9]  A. Ross Possible association between Zika virus infection and microcephaly , 2016 .

[10]  R. Lanciotti,et al.  Genetic and Serologic Properties of Zika Virus Associated with an Epidemic, Yap State, Micronesia, 2007 , 2008, Emerging infectious diseases.

[11]  M. Maia,et al.  Zika virus in Brazil and macular atrophy in a child with microcephaly , 2016, The Lancet.

[12]  A. L. Mosimann,et al.  First report of autochthonous transmission of Zika virus in Brazil , 2015, Memorias do Instituto Oswaldo Cruz.

[13]  《中华放射肿瘤学杂志》编辑部 Medline , 2001, Current Biology.

[14]  M. L. Barjas-Castro,et al.  First Complete Genome Sequence of Zika Virus (Flaviviridae, Flavivirus) from an Autochthonous Transmission in Brazil , 2016, Genome Announcements.

[15]  G. Dick,et al.  Zika virus. I. Isolations and serological specificity. , 1952, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[16]  M Hennessey,et al.  Zika Virus Spreads to New Areas — Region of the Americas, May 2015–January 2016 , 2016, American journal of transplantation : official journal of the American Society of Transplantation and the American Society of Transplant Surgeons.

[17]  J. Schmidt-Chanasit,et al.  Zika Virus Infection after Travel to Tahiti, December 2013 , 2014, Emerging infectious diseases.

[18]  Manolo Gouy,et al.  Remote access to ACNUC nucleotide and protein sequence databases at PBIL. , 2008, Biochimie.

[19]  R. Lanciotti,et al.  Notes from the Field: Evidence of Zika Virus Infection in Brain and Placental Tissues from Two Congenitally Infected Newborns and Two Fetal Losses--Brazil, 2015. , 2016, MMWR. Morbidity and mortality weekly report.

[20]  Emmanuel Fournier,et al.  Guillain-Barré Syndrome outbreak associated with Zika virus infection in French Polynesia: a case-control study , 2016, The Lancet.

[21]  S. Tavaré Some probabilistic and statistical problems in the analysis of DNA sequences , 1986 .

[22]  R. Charrel,et al.  Complete Coding Sequence of Zika Virus from a French Polynesia Outbreak in 2013 , 2014, Genome Announcements.

[23]  Andrew J. Tatem,et al.  Virus evolution and transmission in an ever more connected world , 2015, Proceedings of the Royal Society B: Biological Sciences.

[24]  James R. Knight,et al.  Genome sequencing in microfabricated high-density picolitre reactors , 2005, Nature.

[25]  Peng Jin,et al.  Zika Virus Infects Human Cortical Neural Progenitors and Attenuates Their Growth. , 2016, Cell stem cell.

[26]  D. Bryant,et al.  A Simple and Robust Statistical Test for Detecting the Presence of Recombination , 2006, Genetics.

[27]  Xavier Robert,et al.  Deciphering key features in protein structures with the new ENDscript server , 2014, Nucleic Acids Res..

[28]  Ramón Doallo,et al.  CircadiOmics: integrating circadian genomics, transcriptomics, proteomics and metabolomics , 2012, Nature Methods.

[29]  Marko Kolenc,et al.  Zika Virus Associated with Microcephaly. , 2016, The New England journal of medicine.

[30]  M. Suchard,et al.  Bayesian Phylogenetics with BEAUti and the BEAST 1.7 , 2012, Molecular biology and evolution.

[31]  S. Günther,et al.  Acute Zika Virus Infection after Travel to Malaysian Borneo, September 2014 , 2015, Emerging infectious diseases.

[32]  M. Reis,et al.  Accuracy of Dengue Reporting by National Surveillance System, Brazil , 2016, Emerging infectious diseases.

[33]  M. Suchard,et al.  Phylogeography of Dengue Virus Serotype 4, Brazil, 2010–2011 , 2012, Emerging infectious diseases.

[34]  D. Musso,et al.  Potential for Zika virus transmission through blood transfusion demonstrated during an outbreak in French Polynesia, November 2013 to February 2014. , 2014, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[35]  Stefan Fernandez,et al.  Zika Virus Infection, Philippines, 2012 , 2015, Emerging infectious diseases.

[36]  Robert B. Tesh,et al.  Genetic Characterization of Zika Virus Strains: Geographic Expansion of the Asian Lineage , 2012, PLoS neglected tropical diseases.

[37]  A. P. Adams,et al.  Genome-Scale Phylogenetic Analyses of Chikungunya Virus Reveal Independent Emergences of Recent Epidemics and Various Evolutionary Rates , 2010, Journal of Virology.

[38]  S. Hay,et al.  Emergence and potential for spread of Chikungunya virus in Brazil , 2015, BMC Medicine.

[39]  S. Ho,et al.  Relaxed Phylogenetics and Dating with Confidence , 2006, PLoS biology.

[40]  E. Lennette,et al.  Diagnostic Procedures for Viral, Rickettsial and Chlamydial Infections , 1989 .

[41]  R. Lanciotti,et al.  Zika virus outbreak on Yap Island, Federated States of Micronesia. , 2009, The New England journal of medicine.

[42]  Shane S. Sturrock,et al.  Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data , 2012, Bioinform..

[43]  O. O'Connor,et al.  Co-infection with Zika and Dengue Viruses in 2 Patients, New Caledonia, 2014 , 2015, Emerging infectious diseases.

[44]  J. Tognarelli,et al.  A report on the outbreak of Zika virus on Easter Island, South Pacific, 2014 , 2015, Archives of Virology.

[45]  M. Kaminski,et al.  STROBE Statement—Checklist of items that should be included in reports of cohort studies , 2016 .

[46]  Carlos G Schrago,et al.  Detection and sequencing of Zika virus from amniotic fluid of fetuses with microcephaly in Brazil: a case study. , 2016, The Lancet. Infectious diseases.

[47]  L. Schuler‐Faccini,et al.  Possible Association Between Zika Virus Infection and Microcephaly - Brazil, 2015. , 2016, MMWR. Morbidity and mortality weekly report.

[48]  M. Suchard,et al.  Air Travel Is Associated with Intracontinental Spread of Dengue Virus Serotypes 1–3 in Brazil , 2014, PLoS neglected tropical diseases.

[49]  J. Nataro,et al.  Zika Virus Infection. , 2017, Pediatric clinics of North America.

[50]  Amadou Alpha Sall,et al.  Zika Virus, French Polynesia, South Pacific, 2013 , 2014, Emerging Infectious Diseases.

[51]  S. Kutsuna,et al.  Two cases of Zika fever imported from French Polynesia to Japan, December 2013 to January 2014 [corrected]. , 2014, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[52]  C. Rice,et al.  Molecular biology of the flaviviruses. , 1987, Microbiological sciences.

[53]  Brian D. Foy,et al.  Probable Non–Vector-borne Transmission of Zika Virus, Colorado, USA , 2011, Emerging infectious diseases.

[54]  T. Wetter,et al.  Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. , 2004, Genome research.

[55]  D. Musso,et al.  Potential Sexual Transmission of Zika Virus , 2015, Emerging infectious diseases.

[56]  Trevor Bedford,et al.  Ebola Virus Epidemiology, Transmission, and Evolution during Seven Months in Sierra Leone , 2015, Cell.

[57]  A. Nisalak,et al.  Detection of Zika Virus Infection in Thailand, 2012–2014 , 2015, The American journal of tropical medicine and hygiene.

[58]  K. Pabbaraju,et al.  First case of Zika virus infection in a returning Canadian traveler. , 2014, The American journal of tropical medicine and hygiene.

[59]  J. Roehrig Antigenic structure of flavivirus proteins. , 2003, Advances in virus research.

[60]  F. Corpet Multiple sequence alignment with hierarchical clustering. , 1988, Nucleic acids research.

[61]  R. Duncan Public Health in the Americas , 2012 .

[62]  S. Ioos,et al.  Current Zika virus epidemiology and recent epidemics. , 2014, Medecine et maladies infectieuses.

[63]  M. Besnard,et al.  Evidence of perinatal transmission of Zika virus, French Polynesia, December 2013 and February 2014. , 2014, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[64]  M. Maia,et al.  Ophthalmological findings in infants with microcephaly and presumable intra-uterus Zika virus infection. , 2016, Arquivos brasileiros de oftalmologia.

[65]  D. Hoy,et al.  Concurrent outbreaks of dengue, chikungunya and Zika virus infections - an unprecedented epidemic wave of mosquito-borne viruses in the Pacific 2012-2014. , 2014, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[66]  Kazutaka Katoh,et al.  MAFFT: iterative refinement and additional methods. , 2014, Methods in molecular biology.

[67]  T. Pierson,et al.  Antibody-mediated neutralization of flaviviruses: a reductionist view. , 2011, Virology.

[68]  O. Gascuel,et al.  Estimating maximum likelihood phylogenies with PhyML. , 2009, Methods in molecular biology.

[69]  P. Moore,et al.  Imported Zika Virus Infection from the Cook Islands into Australia, 2014 , 2014, PLoS currents.

[70]  Microcephaly in Brazil potentially linked to the Zika virus epidemic 24 November 2015 , 2015 .

[71]  A. Lesk,et al.  The relation between the divergence of sequence and structure in proteins. , 1986, The EMBO journal.

[72]  H. L. Lee,et al.  Sensitivity of Aedes albopictus C6/36 cells line for the detection and infectivity titration of dengue virus. , 2005, Tropical biomedicine.

[73]  Marco A. R. Ferreira,et al.  Bayesian analysis of elapsed times in continuous‐time Markov chains , 2008 .

[74]  Stephanie J. Spielman,et al.  Time dependence of evolutionary metrics during the 2009 pandemic influenza virus outbreak , 2015, Virus evolution.