{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,24]],"date-time":"2026-09-24T09:03:19Z","timestamp":1790240599347,"version":"4.1.0"},"reference-count":43,"publisher":"MDPI AG","issue":"19","license":[{"start":{"date-parts":[[2022,10,3]],"date-time":"2022-10-03T00:00:00Z","timestamp":1664755200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"National Council for Scientific and Technological Development (CNPQ)","award":["167330\/2018-7"],"award-info":[{"award-number":["167330\/2018-7"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJERPH"],"abstract":"<jats:p>Environmental changes are among the main factors that contribute to the emergence or re-emergence of viruses of public health importance. Here, we show the impact of environmental modifications on cases of infections by the dengue, chikungunya and Zika viruses in humans in the state of Tocantins, Brazil, between the years 2010 and 2019. We conducted a descriptive and principal component analysis (PCA) to explore the main trends in environmental modifications and in the cases of human infections caused by these arboviruses in Tocantins. Our analysis demonstrated that the occurrence of El Ni\u00f1o, deforestation in the Cerrado and maximum temperatures had correlations with the cases of infections by the Zika virus between 2014 and 2016. El Ni\u00f1o, followed by La Ni\u00f1a, a gradual increase in precipitation and the maximum temperature observed between 2015 and 2017 were shown to have contributed to the infections by the chikungunya virus. La Ni\u00f1a and precipitation were associated with infections by the dengue virus between 2010 and 2012 and El Ni\u00f1o contributed to the 2019 outbreak observed within the state. By PCA, deforestation, temperatures and El Ni\u00f1o were the most important variables related to cases of dengue in humans. We conclude from this analysis that environmental changes (deforestation and climate change) presented a strong influence on the human infections caused by the dengue, chikungunya and Zika viruses in Tocantins from 2010 to 2019.<\/jats:p>","DOI":"10.3390\/ijerph191912665","type":"journal-article","created":{"date-parts":[[2022,10,8]],"date-time":"2022-10-08T22:19:27Z","timestamp":1665267567000},"page":"12665","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":41,"title":["Environmental Changes and the Impact on the Human Infections by Dengue, Chikungunya and Zika Viruses in Northern Brazil, 2010\u20132019"],"prefix":"10.3390","volume":"19","author":[{"given":"Robson dos Santos Souza","family":"Marinho","sequence":"first","affiliation":[{"name":"Retrovirology Laboratory, Federal University of S\u00e3o Paulo, S\u00e3o Paulo 04039-032, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rodrigo Lopes Sanz","family":"Duro","sequence":"additional","affiliation":[{"name":"Retrovirology Laboratory, Federal University of S\u00e3o Paulo, S\u00e3o Paulo 04039-032, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"M\u00e2nlio Tasso de Oliveira","family":"Mota","sequence":"additional","affiliation":[{"name":"Retrovirology Laboratory, Federal University of S\u00e3o Paulo, S\u00e3o Paulo 04039-032, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9524-0629","authenticated-orcid":false,"given":"James","family":"Hunter","sequence":"additional","affiliation":[{"name":"Retrovirology Laboratory, Federal University of S\u00e3o Paulo, S\u00e3o Paulo 04039-032, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8395-7304","authenticated-orcid":false,"given":"Ricardo Sobhie","family":"Diaz","sequence":"additional","affiliation":[{"name":"Retrovirology Laboratory, Federal University of S\u00e3o Paulo, S\u00e3o Paulo 04039-032, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fernando Shinji","family":"Kawakubo","sequence":"additional","affiliation":[{"name":"Faculty of Philosophy, Letters and Human Sciences, University of S\u00e3o Paulo, S\u00e3o Paulo 05508-000, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shirley Vasconcelos","family":"Komninakis","sequence":"additional","affiliation":[{"name":"Retrovirology Laboratory, Federal University of S\u00e3o Paulo, S\u00e3o Paulo 04039-032, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,10,3]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"105165","DOI":"10.1016\/j.actatropica.2019.105165","article-title":"Impact of environmental changes on infectious diseases: Key findings from an international conference in Trieste, Italy in May 2017","volume":"213","author":"Brattig","year":"2021","journal-title":"Acta Trop."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"113020","DOI":"10.1016\/j.jenvman.2021.113020","article-title":"Deforestation drivers in the Brazilian Amazon: Assessing new spatial predictors","volume":"294","author":"Santos","year":"2021","journal-title":"J. Environ. Manag."},{"key":"ref_3","unstructured":"(2022, January 26). Forest Trends Organization. Available online: https:\/\/brazil.forest-trends.org\/."},{"key":"ref_4","unstructured":"(2022, January 26). Global Forest Watch. Available online: https:\/\/www.globalforestwatch.org\/."},{"key":"ref_5","unstructured":"CPTEC (2022, February 26). Centro de Previs\u00e3o de Tempo e Estudos Clim\u00e1ticos. Available online: https:\/\/www.cptec.inpe.br\/."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1515\/reveh-2017-0042","article-title":"Effects of climate change on the spread of zika virus: A public health threat","volume":"33","author":"Asad","year":"2018","journal-title":"Rev. Environ. Health"},{"key":"ref_7","unstructured":"NOAA (2022, January 30). National Oceanic and Atmospheric Administration, Available online: https:\/\/www.cpc.ncep.noaa.gov\/products\/precip\/CWlink\/MJO\/enso.shtml."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1481","DOI":"10.1016\/S0140-6736(03)14695-8","article-title":"El Ni\u00f1o and health","volume":"362","author":"Kovats","year":"2003","journal-title":"Lancet"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1186\/s13071-019-3515-7","article-title":"Risk factors associated with sustained circulation of six zoonotic arboviruses: A systematic review for selection of surveillance sites in non-endemic areas","volume":"12","author":"Esser","year":"2019","journal-title":"Parasit Vectors"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1089\/vbz.2016.1952","article-title":"Emergence of Human Arboviral Diseases in the Americas, 2000\u20132016","volume":"16","author":"Vasconcelos","year":"2016","journal-title":"Vector Borne Zoonotic Dis."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/978-981-10-8727-1_1","article-title":"Arboviruses: A Family on the Move","volume":"1062","author":"Young","year":"2018","journal-title":"Adv. Exp. Med. Biol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"e1","DOI":"10.1017\/erm.2018.6","article-title":"Arbovirus lifecycle in mosquito: Acquisition, propagation and transmission","volume":"21","author":"Wu","year":"2019","journal-title":"Expert. Rev. Mol. Med."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"9072","DOI":"10.1073\/pnas.1303395110","article-title":"Host and viral features of human dengue cases shape the population of infected and infectious Aedes aegypti mosquitoes","volume":"110","author":"Nguyen","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1590\/S0102-311X2001000700025","article-title":"Inadequate management of natural ecosystem in the Brazilian Amazon region results in the emergence and reemergence of arboviruses","volume":"17","author":"Vasconcelos","year":"2001","journal-title":"Cad. Saude Publica"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1590\/0037-8682-0133-2013","article-title":"Arboviral diseases in the Western Brazilian Amazon: A perspective and analysis from a tertiary health & research center in Manaus, State of Amazonas","volume":"48","author":"Bastos","year":"2015","journal-title":"Rev. Soc. Bras. Med. Trop."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"540","DOI":"10.1186\/s13071-020-04419-1","article-title":"No evidence for sylvatic cycles of chikungunya, dengue and Zika viruses in African green monkeys (Chlorocebus aethiops sabaeus) on St. Kitts, West Indies","volume":"13","author":"Valentine","year":"2020","journal-title":"Parasites Vectors"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Colt, S., Garcia-Casal, M.N., Pe\u00f1a-Rosas, J.P., Finkelstein, J.L., Rayco-Solon, P., Prinzo, Z.C.W., and Mehta, S. (2017). Transmission of Zika virus through breast milk and other breastfeeding-related bodily-fluids: A systematic review. PLoS Neglected Trop. Dis., 11.","DOI":"10.1371\/journal.pntd.0005528"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"e210020","DOI":"10.1590\/1980-549720210020","article-title":"Entry of dengue virus serotypes and their geographic distribution in Brazilian federative units: A systematic review","volume":"24","author":"Bezerra","year":"2021","journal-title":"Rev. Bras. Epidemiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1016\/j.ijid.2018.04.3661","article-title":"Outbreak of Zika Virus Infection an the Co-Circulation of Other Arboviruses in State of Tocantins, Brazil","volume":"73","author":"Milagres","year":"2018","journal-title":"Int. J. Infect. Dis."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"724","DOI":"10.1016\/j.jiph.2020.02.034","article-title":"Detection of coinfection with Chikungunya virus and Dengue virus serotype 2 in serum samples of patients in State of Tocantins, Brazil","volume":"13","author":"Marinho","year":"2020","journal-title":"J. Infect. Public Health"},{"key":"ref_21","unstructured":"IBGE (2022, January 30). Brazilian Institute of Geography and Statistics, Available online: https:\/\/cidades.ibge.gov.br\/brasil\/to\/panorama."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Lorenz, C., Azevedo, T.S., Virginio, F., Aguiar, B., Chiaravalloti-Neto, F., and Suesdek, L. (2017). Impact of environmental factors on neglected emerging arboviral diseases. PLoS Neglected Trop. Dis., 11.","DOI":"10.1371\/journal.pntd.0005959"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"536","DOI":"10.1126\/science.316.5824.536","article-title":"Carbon emissions. Improved Monitoring of Rainforests Helps Pierce Haze of Deforestation","volume":"316","author":"Kintisch","year":"2007","journal-title":"Science"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"111243","DOI":"10.1016\/j.jenvman.2020.111243","article-title":"Uncovering the spatial variability of recent deforestation drivers in the Brazilian Cerrado","volume":"275","author":"Trigueiro","year":"2020","journal-title":"J. Environ. Manag."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/j.ieri.2013.11.069","article-title":"Evaluation of the Progress of Intensive Agriculture in the Cerrado Piauiense\u2014Brazil","volume":"5","author":"Furtado","year":"2013","journal-title":"IERI Procedia"},{"key":"ref_26","unstructured":"Magrin, G.O., Marengo, J.A., Boulanger, J.P., Buckeridge, M.S., Castellanos, E.J., Poveda, G., Scarano, F.R., and Vicu\u00f1a, S. (2014). Central and south America. Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part B: Regional Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge University Press. Available online: https:\/\/www.ipcc.ch\/site\/assets\/uploads\/2018\/02\/WGIIAR5-Chap27_FINAL.pdf."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"538","DOI":"10.1080\/1747423X.2016.1182221","article-title":"Land cover and land use changes in a Brazilian Cerrado landscape: Drivers, processes, and patterns","volume":"11","author":"Garcia","year":"2016","journal-title":"J. Land Use Sci."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"044029","DOI":"10.1088\/1748-9326\/aafb85","article-title":"Pathways for recent Cerrado soybean expansion: Extending the soy moratorium and implementing integrated crop livestock systems with soybeans","volume":"14","author":"Nepstad","year":"2019","journal-title":"Environ. Res. Lett."},{"key":"ref_29","unstructured":"(2022, February 02). Chain Reaction Research. Available online: https:\/\/chainreactionresearch.com\/wp-content\/uploads\/2019\/04\/CRR_Tocantins-Report-Portuguese.pdf."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Chaves, L.F., Cohen, J., Pascual, M., and Wilson, M.L. (2008). Social Exclusion Modifies Climate and Deforestation Impacts on a Vector-Borne Disease. PLoS Neglected Trop. Dis., 2.","DOI":"10.1371\/journal.pntd.0000176"},{"key":"ref_31","first-page":"1","article-title":"Formation Mechanism for 2015\/16 Super El Ni\u00f1o","volume":"7","author":"Chen","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"2276","DOI":"10.1038\/s41598-017-01479-9","article-title":"Inter-basin sources for two-year predictability of the multi-year La Ni\u00f1a event in 2010\u20132012","volume":"7","author":"Luo","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1465","DOI":"10.1126\/science.330.6010.1465","article-title":"Climate change. El Ni\u00f1o Lends More Confidence to Strong Global Warming","volume":"330","author":"Kerr","year":"2010","journal-title":"Science"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"687","DOI":"10.1126\/science.309.5735.687","article-title":"Climate change. El Ni\u00f1o or La Ni\u00f1a? The Past Hints at the Future","volume":"309","author":"Kerr","year":"2005","journal-title":"Science"},{"key":"ref_35","unstructured":"Environmental Science (2022, February 05). El Ni\u00f1o and La Ni\u00f1a: Their Impact on the Environment. Available online: https:\/\/www.environmentalscience.org\/el-nino-la-nina-impact-environment."},{"key":"ref_36","unstructured":"European Centre for Medium-Range Weather Forecasts (2022, February 05). The 2015\/2016 El Ni\u00f1o and Beyond. Available online: https:\/\/www.ecmwf.int\/en\/newsletter\/151\/meteorology\/2015-2016-el-nino-and-beyond."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1639","DOI":"10.1016\/j.scitotenv.2018.09.242","article-title":"Relation of El Ni\u00f1o and La Ni\u00f1a phenomena to precipitation, evapotranspiration and temperature in the Amazon basin","volume":"651","author":"Moura","year":"2018","journal-title":"Sci. Total Environ."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"5727","DOI":"10.1038\/s41598-018-24003-z","article-title":"ENSO-driven climate variability promotes periodic major outbreaks of dengue in Venezuela","volume":"8","author":"Tami","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Chretien, J.-P., Anyamba, A., Small, J., Britch, S., Sanchez, J.L., Halbach, A.C., Tucker, C., and Linthicum, K.J. (2015). Global Climate Anomalies and Potential Infectious Disease Risks: 2014\u20132015. PLoS Curr., 7.","DOI":"10.1371\/currents.outbreaks.95fbc4a8fb4695e049baabfc2fc8289f"},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Kalbus, A., Sampaio, V.D.S., Boenecke, J., and Reintjes, R. (2021). Exploring the influence of deforestation on dengue fever incidence in the Brazilian Amazonas state. PLoS ONE, 16.","DOI":"10.1371\/journal.pone.0242685"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"e209","DOI":"10.1016\/S2542-5196(20)30292-8","article-title":"Combined effects of hydrometeorological hazards and urbanisation on dengue risk in Brazil: A spatiotemporal modelling study","volume":"5","author":"Lowe","year":"2021","journal-title":"Lancet Planet. Health"},{"key":"ref_42","unstructured":"(2022, February 08). National Institute for Space Research. Available online: http:\/\/enos.cptec.inpe.br\/."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"e00123417","DOI":"10.1590\/0102-311x00123417","article-title":"Sazonalidade nas notifica\u00e7\u00f5es de dengue das capitais da Amaz\u00f4nia e os impactos do El Ni\u00f1o\/La Ni\u00f1a [Seasonality of dengue reporting in state capitals in the Brazilian Amazon and impacts of El Ni\u00f1o\/La Ni\u00f1a]","volume":"35","author":"Moraes","year":"2019","journal-title":"Cad. Saude Publica"}],"container-title":["International Journal of Environmental Research and Public Health"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1660-4601\/19\/19\/12665\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T00:46:06Z","timestamp":1760143566000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1660-4601\/19\/19\/12665"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,10,3]]},"references-count":43,"journal-issue":{"issue":"19","published-online":{"date-parts":[[2022,10]]}},"alternative-id":["ijerph191912665"],"URL":"https:\/\/doi.org\/10.3390\/ijerph191912665","relation":{},"ISSN":["1660-4601"],"issn-type":[{"value":"1660-4601","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,10,3]]}}}