Chikungunya Virus Asian Lineage Infection in the Amazon Region Is Maintained by Asiatic and Caribbean-Introduced Variants

The simultaneous transmission of two lineages of the chikungunya virus (CHIKV) was discovered after the pathogen’s initial arrival in Brazil. In Oiapoque (Amapá state, north Brazil), the Asian lineage (CHIKV-Asian) was discovered, while in Bahia state, the East-Central-South-African lineage (CHIKV-ECSA) was discovered (northeast Brazil). Since then, the CHIKV-Asian lineage has been restricted to the Amazon region (mostly in the state of Amapá), whereas the ECSA lineage has expanded across the country. Despite the fact that the Asian lineage was already present in the Amazon region, the ECSA lineage brought from the northeast caused a large outbreak in the Amazonian state of Roraima (north Brazil) in 2017. Here, CHIKV spread in the Amazon region was studied by a Zika–Dengue–Chikungunya PCR assay in 824 serum samples collected between 2013 and 2016 from individuals with symptoms of viral infection in the Amapá state. We found 11 samples positive for CHIKV-Asian, and, from these samples, we were able to retrieve 10 full-length viral genomes. A comprehensive phylogenetic study revealed that nine CHIKV sequences came from a local transmission cluster related to Caribbean strains, whereas one sequence was related to sequences from the Philippines. These findings imply that CHIKV spread in different ways in Roraima and Amapá, despite the fact that both states had similar climatic circumstances and mosquito vector frequencies.

[1]  S. Weaver,et al.  Lineage Divergence and Vector-Specific Adaptation Have Driven Chikungunya Virus onto Multiple Adaptive Landscapes , 2021, mBio.

[2]  E. Holmes,et al.  Epidemiologic History and Genetic Diversity Origins of Chikungunya and Dengue Viruses, Paraguay , 2021, Emerging infectious diseases.

[3]  E. Delwart,et al.  Adaptive Evolution of New Variants of Dengue Virus Serotype 1 Genotype V Circulating in the Brazilian Amazon , 2021, Viruses.

[4]  T. de Oliveira,et al.  Chikungunya virus ECSA lineage reintroduction in the northeasternmost region of Brazil. , 2021, International journal of infectious diseases : IJID : official publication of the International Society for Infectious Diseases.

[5]  J. Araújo,et al.  Epidemiologic and clinical investigations during a chikungunya outbreak in Rio Grande do Norte State, Brazil , 2020, PloS one.

[6]  S. Sardi,et al.  Genomic surveillance of the Chikungunya Virus (CHIKV) in Northeast Brazil after the first outbreak in 2014 , 2020, Revista da Sociedade Brasileira de Medicina Tropical.

[7]  C. Gilbert,et al.  Genome sequencing reveals coinfection by multiple chikungunya virus genotypes in a recent outbreak in Brazil , 2019, PLoS neglected tropical diseases.

[8]  Ann Nowé,et al.  A computational method for the identification of Dengue, Zika and Chikungunya virus species and genotypes , 2019, PLoS neglected tropical diseases.

[9]  N. Loman,et al.  Genomic, epidemiological and digital surveillance of Chikungunya virus in the Brazilian Amazon , 2019, PLoS neglected tropical diseases.

[10]  R. Nogueira,et al.  Following in the Footsteps of the Chikungunya Virus in Brazil: The First Autochthonous Cases in Amapá in 2014 and Its Emergence in Rio de Janeiro during 2016 , 2018, Viruses.

[11]  L. Figueiredo,et al.  Enzyme-linked immunosorbent assay using recombinant envelope protein 2 antigen for diagnosis of Chikungunya virus , 2018, Virology Journal.

[12]  Sarah K White,et al.  A new "American" subgroup of African-lineage Chikungunya virus detected in and isolated from mosquitoes collected in Haiti, 2016 , 2018, PloS one.

[13]  D. Fremont,et al.  Mxra8 is a receptor for multiple arthritogenic alphaviruses , 2018, Nature.

[14]  D. Boccolini,et al.  Vector competence of Italian Aedes albopictus populations for the chikungunya virus (E1-226V) , 2018, PLoS neglected tropical diseases.

[15]  O. Smith,et al.  Maternal invasion history of Aedes aegypti and Aedes albopictus into the Isthmus of Panama: Implications for the control of emergent viral disease agents , 2018, PloS one.

[16]  P. Moore,et al.  New insights into chikungunya virus emergence and spread from Southeast Asia , 2018, Emerging Microbes & Infections.

[17]  Nuno R. Faria,et al.  Spread of Chikungunya Virus East/Central/South African Genotype in Northeast Brazil , 2017, Emerging infectious diseases.

[18]  J. Burgerhof,et al.  Long-term Chikungunya Sequelae in Curaçao: Burden, Determinants, and a Novel Classification Tool , 2017, The Journal of infectious diseases.

[19]  G. Palacios,et al.  First report of naturally infected Aedes aegypti with chikungunya virus genotype ECSA in the Americas , 2017, PLoS neglected tropical diseases.

[20]  I. Sam,et al.  The neutralizing role of IgM during early Chikungunya virus infection , 2017, PloS one.

[21]  C. Carrington,et al.  Understanding the evolution and spread of chikungunya virus in the Americas using complete genome sequences , 2017, Virus evolution.

[22]  R. Charrel,et al.  Epidemiology of Chikungunya Virus Outbreaks in Guadeloupe and Martinique, 2014: An Observational Study in Volunteer Blood Donors , 2017, PLoS neglected tropical diseases.

[23]  G. Vieilledent,et al.  Gold-rush in a forested El Dorado: deforestation leakages and the need for regional cooperation , 2017 .

[24]  J. E. Staples,et al.  Epidemiology of Chikungunya in the Americas , 2016, The Journal of infectious diseases.

[25]  A. Agarwal,et al.  Two novel epistatic mutations (E1:K211E and E2:V264A) in structural proteins of Chikungunya virus enhance fitness in Aedes aegypti. , 2016, Virology.

[26]  D. Lin,et al.  Comprehensive Genome Scale Phylogenetic Study Provides New Insights on the Global Expansion of Chikungunya Virus , 2016, Journal of Virology.

[27]  R. Nogueira,et al.  Phylogenetic analyses of chikungunya virus among travelers in Rio de Janeiro, Brazil, 2014-2015 , 2016, Memorias do Instituto Oswaldo Cruz.

[28]  A. Failloux,et al.  Insect-pathogen interactions: contribution of viral adaptation to the emergence of vector-borne diseases, the example of chikungunya. , 2015, Current opinion in insect science.

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

[30]  R. Lourenço-de-Oliveira,et al.  Updating the geographical distribution and frequency of Aedes albopictus in Brazil with remarks regarding its range in the Americas , 2014, Memorias do Instituto Oswaldo Cruz.

[31]  Anders Larsson,et al.  AliView: a fast and lightweight alignment viewer and editor for large datasets , 2014, Bioinform..

[32]  S. Weaver Arrival of Chikungunya Virus in the New World: Prospects for Spread and Impact on Public Health , 2014, PLoS neglected tropical diseases.

[33]  R. Césaire,et al.  Chikungunya outbreak in the Caribbean region, December 2013 to March 2014, and the significance for Europe. , 2014, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[34]  R. Lourenço-de-Oliveira,et al.  High Level of Vector Competence of Aedes aegypti and Aedes albopictus from Ten American Countries as a Crucial Factor in the Spread of Chikungunya Virus , 2014, Journal of Virology.

[35]  Jeffrey E. Lee,et al.  The Secret Life of Viral Entry Glycoproteins: Moonlighting in Immune Evasion , 2013, PLoS pathogens.

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

[37]  S. Weaver,et al.  Sequential Adaptive Mutations Enhance Efficient Vector Switching by Chikungunya Virus and Its Epidemic Emergence , 2011, PLoS pathogens.

[38]  O. Gascuel,et al.  New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. , 2010, Systematic biology.

[39]  D. Posada jModelTest: phylogenetic model averaging. , 2008, Molecular biology and evolution.

[40]  Rosalia M. Kalani,et al.  Seroprevalence of Chikungunya virus (CHIKV) infection on Lamu Island, Kenya, October 2004. , 2008, The American journal of tropical medicine and hygiene.

[41]  S. Higgs,et al.  A Single Mutation in Chikungunya Virus Affects Vector Specificity and Epidemic Potential , 2007, PLoS pathogens.

[42]  A. Rambaut,et al.  BEAST: Bayesian evolutionary analysis by sampling trees , 2007, BMC Evolutionary Biology.

[43]  J. Varni,et al.  Crossing the border for health care: access and primary care characteristics for young children of Latino farm workers along the US-Mexico border. , 2003, Ambulatory pediatrics : the official journal of the Ambulatory Pediatric Association.

[44]  K. Katoh,et al.  MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. , 2002, Nucleic acids research.

[45]  A. Brault,et al.  Re-emergence of Chikungunya and O'nyong-nyong viruses: evidence for distinct geographical lineages and distant evolutionary relationships. , 2000, The Journal of general virology.

[46]  B. Simizu,et al.  Structural proteins of Chikungunya virus , 1984, Journal of virology.

[47]  R. Ross The Newala epidemic: III. The virus: isolation, pathogenic properties and relationship to the epidemic , 1956, Journal of Hygiene.

[48]  M C ROBINSON,et al.  An epidemic of virus disease in Southern Province, Tanganyika Territory, in 1952-53. I. Clinical features. , 1955, Transactions of the Royal Society of Tropical Medicine and Hygiene.