Duffy MR et al.2009. Zika virus outbreak on Yap Island, Federated States of Micronesia. N Engl J Med 360: 2536–2543.
World Health Organization , 2021. Available at: https://www.who.int/news-room/feature-stories/detail/the-history-of-zika-virus. Accessed October 27, 2021.
Pan-American Health Organization/World Health Organization , 2017. Available at: https://www.paho.org/en/documents/zika-epidemiological-report-haiti-1. Accessed October 27, 2021.
Beau De Rochars VEM et al.2015. Spectrum of outpatient illness in a school-based cohort in Haiti, with a focus on diarrheal pathogens. Am J Trop Med Hyg 92: 752–757.
Lednicky J et al., 2016. Zika virus outbreak in Haiti in 2014: molecular and clinical data. PLoS Negl Trop Dis 10: e0004687.
Ball JD et al.2019. Clinical and epidemiological patterns of Chikungunya virus infection and coincident arboviral disease in a school cohort in Haiti, 2014/2015. Clin Infect Dis 68: 919–926.
White SK , Mavian C , El Badry MA , Beau De Rochars VM , Paisie T , Telisma T , Salemi M , Lednicky JA , Morris JG , 2018. Detection and phylogenetic characterization of arbovirus dual-infections among persons during a Chikungunya fever outbreak, Haiti, 2014. PLoS Negl Trop Dis 12: e0006505.
Beau de Rochars VM et al., 2017. Isolation of coronavirus NL63 from blood from children in rural Haiti: phylogenetic similarities with recent isolates from Malaysia. Am J Trop Med Hyg 96: 144–147.
Lednicky J , Beau de Rochars VM , Elbadry M , Loeb J , Telisma T , Chavannes S , Anilis G , Cella E , Ciccozzi M , Okech B , Salemi M & Morris JG. 2016. Mayaro virus in child with acute febrile illness, Haiti, 2015. Emerg Infect Dis 22: 2000–2002.
Lanciotti RS et al.2008. Genetic and serologic properties of Zika virus associated with an epidemic, Yap State, Micronesia, 2007. Emerg Infect Dis 14: 1232–1239.
Lanciotti RS et al.2007. Chikungunya virus in US travelers returning from India, 2006. Emerg Infect Dis 13: 764–767.
Santiago GA et al.2013. Analytical and clinical performance of the CDC real time RT-PCR assay for detection and typing of dengue virus. PLoS Negl Trop Dis 7: e2311.
Rueda LM , 2004. Pictorial Keys for the Identification of Mosquitoes (Diptera: Culicidae) Associated with Dengue Virus Transmission. pp. 33–41.
White SK , Lednicky JA , Okech BA , Morris JG , Dunford JC , 2018. Spondweni virus in field-caught Culex quinquefasciatus mosquitoes, Haiti, 2016. Emerg Infect Dis 24: 1765–1767.
White SK , Mavian C , Salemi M , Morris JG , El Badry MA , Okech BA , Lednicky JA , Dunford JC , 2018. A new ‘American’ subgroup of African-lineage Chikungunya virus detected in and isolated from mosquitoes collected in Haiti, 2016. PLoS ONE 13: e0196857.
Crowder CD et al.2010. Extraction of total nucleic acids from ticks for the detection of bacterial and viral pathogens. J Med Entomol 47: 89–94.
Das B , 2012. Development and evaluation of a single-step multiplex PCR to differentiate the aquatic stages of morphologically similar Aedes (subgenus: Stegomyia) species. Trop Med Int Health 17: 235–243.
Smith JL , Fonseca DM , 2004. Rapid assays for identification of members of the Culex (Culex) pipiens complex, their hybrids, and other sibling species (Diptera: culicidae). Am J Trop Med Hyg 70: 339–345.
Sirot LK , Poulson RL , McKenna MC , Girnary H , Wolfner MF , Harrington LC , 2008. Identity and transfer of male reproductive gland proteins of the dengue vector mosquito, Aedes aegypti: potential tools for control of female feeding and reproduction. Insect Biochem Mol Biol 38: 176–189.
Salvemini M et al.2011. Genomic organization and splicing evolution of the doublesex gene, a Drosophila regulator of sexual differentiation, in the dengue and yellow fever mosquito Aedes aegypti. BMC Evol Biol 11: 41.
Katoh K , Standley DM , 2016. A simple method to control over-alignment in the MAFFT multiple sequence alignment program. Bioinformatics 32: 1933–1942.
Nguyen LT , Schmidt HA , von Haeseler A , Minh BQ , 2015. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32: 268–274.
Kalyaanamoorthy S , Minh BQ , Wong TKF , von Haeseler A , Jermiin LS , 2017. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14: 587–589.
Hoang DT , Chernomor O , von Haeseler A , Minh BQ , Vinh LS , 2018. UFBoot2: improving the Ultrafast Bootstrap Approximation. Mol Biol Evol 35: 518–522.
Schmidt HA , Strimmer K , Vingron M , von Haeseler A , 2002. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18: 502–504.
Strimmer K , von Haeseler A , 1997. Likelihood-mapping: a simple method to visualize phylogenetic content of a sequence alignment. Proc Natl Acad Sci USA 94: 6815–6819.
Rambaut A , Lam TT , Carvalho LM , Pybus OG , 2016. Exploring the temporal structure of heterochronous sequences using TempEst. Virus Evol 2: vew007.
Sagulenko P , Puller V , Neher RA , 2018. TreeTime: maximum-likelihood phylodynamic analysis. Virus Evol 4: vex042.
Grubaugh ND et al.2017. Genomic epidemiology reveals multiple introductions of Zika virus into the United States. Nature 546: 401.
Volz EM , Frost SDW , 2017. Scalable relaxed clock phylogenetic dating. Virus Evol 3: vex025.
Zambrana JV et al.2018. Seroprevalence, risk factor, and spatial analyses of Zika virus infection after the 2016 epidemic in Managua, Nicaragua. Proc Natl Acad Sci USA 115: 9294–9299.
Katzelnick LC et al.2021. Dengue and Zika virus infections in children elicit cross-reactive protective and enhancing antibodies that persist long term. Sci Transl Med 13: eabg9478.
Rodriguez-Barraquer I et al.2019. Impact of prexisting dengue immunity on Zika virus emergence in a dengue endemic region. Science 363: 607–610.
Xing H , Xu S , Jia F , Yang Y , Xu C , Qin C , Shi L , 2020. Zika NS2B is a crucial factor recruiting NS3 to the ER and activating its protease activity. Virus Res 275: 197793.
Evans JD , Seeger C , 2007. Differential effects of mutations in NS4B on West Nile virus replication and inhibition of interferon signaling. J Virol 81: 11809–11816.
Hill J et al., 2018. Structural insights into the inhibition of Zika virus NS2B-NS3 protease by a small-molecule inhibitor. Structure 26: 555–564.e3.
Liang Q et al., 2016. Zika virus NS4A and NS4B proteins deregulate Akt-mTOR signaling in human fetal neural stem cells to inhibit neurogenesis and induce autophagy. Cell Stem Cell 19: 663–671.
Boyer S , Calvez E , Chouin-Carneiro T , Diallo D , Failloux AB , 2018. An overview of mosquito vectors of Zika virus. Microbes Infect 20: 646–660.
Liu Y , 2017. Evolutionary enhancement of Zika virus infectivity in Aedes aegypti mosquitoes. Nature 545: 482–486.
Fernandes RS et al., 2019. Low vector competence in sylvatic mosquitoes limits Zika virus to initiate an enzootic cycle in South America. Sci Rep 9: 20151.
Valentine MJ , Murdock CC , Kelly PJ , 2019. Sylvatic cycles of arboviruses in non-human primates. BMC Parasite Vectors 12: 463.
Ciota AT , Bialosuknia SM , Ehrbar DJ & Kramer LD. 2017. Vertical transmission of Zika virus by Aedes aegypti and Ae. albopictus mosquitoes. Emerg Infect Dis 23: 880–882.
Smartt CT et al.2017. Evidence of Zika virus RNA fragments in Aedes albopictus (Diptera: Culicidae) field-collected eggs from Camaçari, Bahia, Brazil. J Med Entomol 2017.
Ferreira-de-Brito A et al., 2016. First detection of natural infection of Aedes aegypti with Zika virus in Brazil and throughout South America. Mem Inst Oswaldo Cruz 111: 655–658.
Mavian C et al.2017. Emergence of recombinant Mayaro strains from the Amazon basin. Sci Rep 7: 8718.
Lednicky JA et al.2019. Emergence of Madariaga virus as a cause of acute febrile illness in children, Haiti, 2015–2016. PLoS Negl Trop Dis 13: e0006972.
Blohm G et al.2019. Mayaro as a Caribbean traveler: evidence for multiple introductions and transmission of the virus into Haiti. Int J Infect Dis 87: 151–153.
Mavian C , Dulcey M , Munoz O , Salmei M , Vittor AY , Capua I , 2019. Islands as hotspots for emerging mosquito-borne viruses: a One-Health perspective. Viruses 11: 11.
Moreira-Soto A et al.2020. Rapid decline of Zika virus NS1 antigen-specific antibody responses, northeastern Brazil. Virus Genes 56: 632–637.
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Zika virus (ZIKV) infections occurred in epidemic form in the Americas in 2014–2016, with some of the earliest isolates in the region coming from Haiti. We isolated ZIKV from 20 children with acute undifferentiated febrile illness who were part of a cohort of children seen at a school clinic in the Gressier region of Haiti. The virus was also isolated from three pools of Aedes aegypti mosquitoes collected at the same location. On phylogenetic analysis, three distinct ZIKV clades were identified. Strains from all three clades were present in Haiti in 2014, making them among the earliest isolates identified in the Western Hemisphere. Strains from all three clades were also isolated in 2016, indicative of their persistence across the time period of the epidemic. Mosquito isolates were collected in 2016 and included representatives from two of the three clades; in one instance, ZIKV was isolated from a pool of male mosquitoes, suggestive of vertical transmission of the virus. The identification of multiple ZIKV clades in Haiti at the beginning of the epidemic suggests that Haiti served as a nidus for transmission within the Caribbean.
These authors contributed equally to this work.
Financial support: This work was funded in part by a grant from National Institute of Allergy and Infectious Diseases to J. G. M. (no. R01AI123657S).
Disclaimer: The opinions and assertions expressed herein are those of the author(s) and do not reflect the official policy or position of the Uniformed Services University of the Health Sciences or the Department of Defense.
Authors’ addresses: Md. Mahbubul Alam, Sarah K. White, Caroline J. Stephenson, Gabriela M. Blohm, Julia C. Loeb, and John A. Lednicky, Emerging Pathogens Institute, University of Florida, Gainesville, FL, and Department of Environmental and Global Health, College of Public Health and Health Professions, University of Florida, Gainesville, FL, E-mails: md.alam@epi.ufl.edu, sarahkellerwhite@gmail.com, c.stephenson@ufl.edu, gabriela.blohm@gmail.com, jloeb@phhp.ufl.edu, and jlednicky@phhp.ufl.edu. Carla Mavian and Marco Salemi, Emerging Pathogens Institute, University of Florida, Gainesville, FL, and Department of Pathology, Immunology, and Laboratory Medicine, College of Medicine, University of Florida, Gainesville, FL, E-mails: cmavian@ufl.edu and salemi@pathology.ufl.edu. Bernard A. Okech, Department of Preventive Medicine and Biostatistics at the F. Edward Hebert School of Medicine, Uniformed Services University, Bethesda, MD, E-mail: bernard.okech@usuhs.edu. Maha A. Elbadry, Proctor and Gamble, Cincinnati, OH, E-mail: elbadry.ma@pg.com. Rigan Louis, Emerging Pathogens Institute, University of Florida, Gainesville, FL, and State University of Haiti Faculty of Medicine and Pharmacy, Port-au-Prince, Haiti, E-mail: lrigan@gmail.com. Cyrus Saleem, Emerging Pathogens Institute, University of Florida, Gainesville, FL, E-mail: cyrus.saleem@epi.ufl.edu. Valery E. Madsen Beau de Rochars, Emerging Pathogens Institute, University of Florida, Gainesville, FL, and Department of Health Services Research, Management and Policy, College of Public Health and Health Professions, University of Florida, Gainesville, FL, E-mail: madsenbeau@phhp.ufl.edu. J. Glenn Morris, Jr., Emerging Pathogens Institute, University of Florida, Gainesville, FL, and Department of Medicine, College of Medicine, University of Florida, Gainesville, FL, E-mail: jgmorris@epi.ufl.edu.
Duffy MR et al.2009. Zika virus outbreak on Yap Island, Federated States of Micronesia. N Engl J Med 360: 2536–2543.
World Health Organization , 2021. Available at: https://www.who.int/news-room/feature-stories/detail/the-history-of-zika-virus. Accessed October 27, 2021.
Pan-American Health Organization/World Health Organization , 2017. Available at: https://www.paho.org/en/documents/zika-epidemiological-report-haiti-1. Accessed October 27, 2021.
Beau De Rochars VEM et al.2015. Spectrum of outpatient illness in a school-based cohort in Haiti, with a focus on diarrheal pathogens. Am J Trop Med Hyg 92: 752–757.
Lednicky J et al., 2016. Zika virus outbreak in Haiti in 2014: molecular and clinical data. PLoS Negl Trop Dis 10: e0004687.
Ball JD et al.2019. Clinical and epidemiological patterns of Chikungunya virus infection and coincident arboviral disease in a school cohort in Haiti, 2014/2015. Clin Infect Dis 68: 919–926.
White SK , Mavian C , El Badry MA , Beau De Rochars VM , Paisie T , Telisma T , Salemi M , Lednicky JA , Morris JG , 2018. Detection and phylogenetic characterization of arbovirus dual-infections among persons during a Chikungunya fever outbreak, Haiti, 2014. PLoS Negl Trop Dis 12: e0006505.
Beau de Rochars VM et al., 2017. Isolation of coronavirus NL63 from blood from children in rural Haiti: phylogenetic similarities with recent isolates from Malaysia. Am J Trop Med Hyg 96: 144–147.
Lednicky J , Beau de Rochars VM , Elbadry M , Loeb J , Telisma T , Chavannes S , Anilis G , Cella E , Ciccozzi M , Okech B , Salemi M & Morris JG. 2016. Mayaro virus in child with acute febrile illness, Haiti, 2015. Emerg Infect Dis 22: 2000–2002.
Lanciotti RS et al.2008. Genetic and serologic properties of Zika virus associated with an epidemic, Yap State, Micronesia, 2007. Emerg Infect Dis 14: 1232–1239.
Lanciotti RS et al.2007. Chikungunya virus in US travelers returning from India, 2006. Emerg Infect Dis 13: 764–767.
Santiago GA et al.2013. Analytical and clinical performance of the CDC real time RT-PCR assay for detection and typing of dengue virus. PLoS Negl Trop Dis 7: e2311.
Rueda LM , 2004. Pictorial Keys for the Identification of Mosquitoes (Diptera: Culicidae) Associated with Dengue Virus Transmission. pp. 33–41.
White SK , Lednicky JA , Okech BA , Morris JG , Dunford JC , 2018. Spondweni virus in field-caught Culex quinquefasciatus mosquitoes, Haiti, 2016. Emerg Infect Dis 24: 1765–1767.
White SK , Mavian C , Salemi M , Morris JG , El Badry MA , Okech BA , Lednicky JA , Dunford JC , 2018. A new ‘American’ subgroup of African-lineage Chikungunya virus detected in and isolated from mosquitoes collected in Haiti, 2016. PLoS ONE 13: e0196857.
Crowder CD et al.2010. Extraction of total nucleic acids from ticks for the detection of bacterial and viral pathogens. J Med Entomol 47: 89–94.
Das B , 2012. Development and evaluation of a single-step multiplex PCR to differentiate the aquatic stages of morphologically similar Aedes (subgenus: Stegomyia) species. Trop Med Int Health 17: 235–243.
Smith JL , Fonseca DM , 2004. Rapid assays for identification of members of the Culex (Culex) pipiens complex, their hybrids, and other sibling species (Diptera: culicidae). Am J Trop Med Hyg 70: 339–345.
Sirot LK , Poulson RL , McKenna MC , Girnary H , Wolfner MF , Harrington LC , 2008. Identity and transfer of male reproductive gland proteins of the dengue vector mosquito, Aedes aegypti: potential tools for control of female feeding and reproduction. Insect Biochem Mol Biol 38: 176–189.
Salvemini M et al.2011. Genomic organization and splicing evolution of the doublesex gene, a Drosophila regulator of sexual differentiation, in the dengue and yellow fever mosquito Aedes aegypti. BMC Evol Biol 11: 41.
Katoh K , Standley DM , 2016. A simple method to control over-alignment in the MAFFT multiple sequence alignment program. Bioinformatics 32: 1933–1942.
Nguyen LT , Schmidt HA , von Haeseler A , Minh BQ , 2015. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32: 268–274.
Kalyaanamoorthy S , Minh BQ , Wong TKF , von Haeseler A , Jermiin LS , 2017. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14: 587–589.
Hoang DT , Chernomor O , von Haeseler A , Minh BQ , Vinh LS , 2018. UFBoot2: improving the Ultrafast Bootstrap Approximation. Mol Biol Evol 35: 518–522.
Schmidt HA , Strimmer K , Vingron M , von Haeseler A , 2002. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18: 502–504.
Strimmer K , von Haeseler A , 1997. Likelihood-mapping: a simple method to visualize phylogenetic content of a sequence alignment. Proc Natl Acad Sci USA 94: 6815–6819.
Rambaut A , Lam TT , Carvalho LM , Pybus OG , 2016. Exploring the temporal structure of heterochronous sequences using TempEst. Virus Evol 2: vew007.
Sagulenko P , Puller V , Neher RA , 2018. TreeTime: maximum-likelihood phylodynamic analysis. Virus Evol 4: vex042.
Grubaugh ND et al.2017. Genomic epidemiology reveals multiple introductions of Zika virus into the United States. Nature 546: 401.
Volz EM , Frost SDW , 2017. Scalable relaxed clock phylogenetic dating. Virus Evol 3: vex025.
Zambrana JV et al.2018. Seroprevalence, risk factor, and spatial analyses of Zika virus infection after the 2016 epidemic in Managua, Nicaragua. Proc Natl Acad Sci USA 115: 9294–9299.
Katzelnick LC et al.2021. Dengue and Zika virus infections in children elicit cross-reactive protective and enhancing antibodies that persist long term. Sci Transl Med 13: eabg9478.
Rodriguez-Barraquer I et al.2019. Impact of prexisting dengue immunity on Zika virus emergence in a dengue endemic region. Science 363: 607–610.
Xing H , Xu S , Jia F , Yang Y , Xu C , Qin C , Shi L , 2020. Zika NS2B is a crucial factor recruiting NS3 to the ER and activating its protease activity. Virus Res 275: 197793.
Evans JD , Seeger C , 2007. Differential effects of mutations in NS4B on West Nile virus replication and inhibition of interferon signaling. J Virol 81: 11809–11816.
Hill J et al., 2018. Structural insights into the inhibition of Zika virus NS2B-NS3 protease by a small-molecule inhibitor. Structure 26: 555–564.e3.
Liang Q et al., 2016. Zika virus NS4A and NS4B proteins deregulate Akt-mTOR signaling in human fetal neural stem cells to inhibit neurogenesis and induce autophagy. Cell Stem Cell 19: 663–671.
Boyer S , Calvez E , Chouin-Carneiro T , Diallo D , Failloux AB , 2018. An overview of mosquito vectors of Zika virus. Microbes Infect 20: 646–660.
Liu Y , 2017. Evolutionary enhancement of Zika virus infectivity in Aedes aegypti mosquitoes. Nature 545: 482–486.
Fernandes RS et al., 2019. Low vector competence in sylvatic mosquitoes limits Zika virus to initiate an enzootic cycle in South America. Sci Rep 9: 20151.
Valentine MJ , Murdock CC , Kelly PJ , 2019. Sylvatic cycles of arboviruses in non-human primates. BMC Parasite Vectors 12: 463.
Ciota AT , Bialosuknia SM , Ehrbar DJ & Kramer LD. 2017. Vertical transmission of Zika virus by Aedes aegypti and Ae. albopictus mosquitoes. Emerg Infect Dis 23: 880–882.
Smartt CT et al.2017. Evidence of Zika virus RNA fragments in Aedes albopictus (Diptera: Culicidae) field-collected eggs from Camaçari, Bahia, Brazil. J Med Entomol 2017.
Ferreira-de-Brito A et al., 2016. First detection of natural infection of Aedes aegypti with Zika virus in Brazil and throughout South America. Mem Inst Oswaldo Cruz 111: 655–658.
Mavian C et al.2017. Emergence of recombinant Mayaro strains from the Amazon basin. Sci Rep 7: 8718.
Lednicky JA et al.2019. Emergence of Madariaga virus as a cause of acute febrile illness in children, Haiti, 2015–2016. PLoS Negl Trop Dis 13: e0006972.
Blohm G et al.2019. Mayaro as a Caribbean traveler: evidence for multiple introductions and transmission of the virus into Haiti. Int J Infect Dis 87: 151–153.
Mavian C , Dulcey M , Munoz O , Salmei M , Vittor AY , Capua I , 2019. Islands as hotspots for emerging mosquito-borne viruses: a One-Health perspective. Viruses 11: 11.
Moreira-Soto A et al.2020. Rapid decline of Zika virus NS1 antigen-specific antibody responses, northeastern Brazil. Virus Genes 56: 632–637.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 8207 | 2889 | 680 |
Full Text Views | 304 | 31 | 1 |
PDF Downloads | 205 | 33 | 0 |