https://doi.org/10.4081/gh.2021.997
Environmental influence on Triatoma vitticeps occurrence and Trypanosoma cruzi infection in the Atlantic Forest of south-eastern Brazil
Submitted: 10 March 2021
Accepted: 26 May 2021
Published: 28 October 2021
Accepted: 26 May 2021
Abstract Views: 1531
PDF: 442
Appendix: 114
HTML: 16
Appendix: 114
HTML: 16
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
Authors
Trypanosoma cruzi requires a triatomine insect vector for its life cycle, which can be complex in different enzootic scenarios, one of which is the unique transmission network in the Atlantic Forest of south-eastern Brazil. In EspÃrito Santo (ES) State, highly infected Triatoma vitticeps are frequently reported invading domiciles. However, triatomines were not found colonizing residences and mammals in the surrounding areas did not present T. cruzi infection. To date, the biotic and abiotic variables that modulate T. vitticeps occurrence and T. cruzi infection in ES State are still unknown. The aim of this study was to identify the environmental variables that modulate their occurrence. Local thematic maps were generated for two response variables: T. vitticeps occurrence and T. cruzi infection. The following explanatory variables were tested: climate (temperature, relative air humidity and rainfall), altitude elevation, mammalian species richness as well as soil and vegetation types. Spatiotemporal distribution patterns and correlation levels between response and explanatory variables were assessed through spatial statistics and map algebra modelling. The central and southern mesoregions presented higher T. vitticeps and T. cruzi distributions and can be considered transmission hotspots. The explanatory variables that can explain these phenomena were relative air humidity, average temperature, soil type, altitude elevation and mammalian species richness. Algebra map modelling demonstrated that central and southern mesoregions presented the environmental conditions needed for T. vitticeps occurrence and T. cruzi infection. The consideration of environmental variables is essential for understanding the T. cruzi transmission cycle. Cartographic and statistical methodologies used in parasitology have been demonstrated to be reliable and enlightening tools that should be incorporated routinely to expand the understanding of vector-borne parasite transmission.
Alene KA, Viney K, Moore HC, Wagaw M, Clements ACA, 2019. Spatial patterns of tuberculosis and HIV co-infection in Ethiopia. PLoS One 14:e0226127.
DOI: https://doi.org/10.1371/journal.pone.0226127
Asin S, Catalá S, 1995. Development of Trypanosoma cruzi in Triatoma infestans: influence of temperature and blood consumption. J Parasitol 81:1-7.
DOI: https://doi.org/10.2307/3283997
Barrozo RB, Manrique G, Lazzari CR, 2003. The role of water vapour in the orientation behaviour of the blood-sucking bug Triatoma infestans (Hemiptera, Reduviidae). J Insect Physiol 49:315-21.
DOI: https://doi.org/10.1016/S0022-1910(03)00005-2
Barrozo RB, Reisenman CE, Guerenstein P, Lazzari CR, Lorenzo MG, 2017. An inside look at the sensory biology of triatomines. J Insect Physiology 97:3-19.
DOI: https://doi.org/10.1016/j.jinsphys.2016.11.003
Bavia ME, Carneiro DDMT, Gurgel HDC, Madureira Filho C, Barbosa MGR, 2005. Remote sensing and geographic information systems and risk of American Visceral Leishmaniasis in Bahia, Brazil. Parassitologia 47:165-9.
Bovendorp RS, Villar N, de Abreu-Junior EF, Bello C, Regolin AL, Percequillo AR, Percequillo AR, Galetti M, 2017. Atlantic small-mammal: a dataset of communities of rodents and marsupials of the Atlanticforests of South America. Ecology 98:2226.
DOI: https://doi.org/10.1002/ecy.1893
Carbajal-de-la-Fuente AL, Provecho YM, Fernández MdelP, Cardinal MV, Lencina P, Spillmann C, Gürtler RE, 2017. The eco-epidemiology of Triatoma infestans in the temperate Monte Desert ecoregion of mid-western Argentina. Mem Inst Oswaldo Cruz 112:698-708.
DOI: https://doi.org/10.1590/0074-02760160519
Carmona-Galindo VD, MarÃn Recinos MF, Gámez Hidalgo SA, Recinos Paredes G, Posada Vaquerano EE, Romero Magaña AL, Ayala AKC, 2020. Morphological variability and ecological characterization of the Chagas disease vector Triatoma dimidiata (Hemiptera: Reduviidae) in El Salvador. Acta Trop 205:105392.
DOI: https://doi.org/10.1016/j.actatropica.2020.105392
Chen Y, 2013. New Approaches for Calculating Moran’s Index of Spatial Autocorrelation. PLoS One 8:e68336.
DOI: https://doi.org/10.1371/journal.pone.0068336
Dario MA, Rodrigues MS, Barros JH, Xavier SC, D’Andrea PS, Roque AL, Jansen AM, 2016. Ecological scenario and Trypanosoma cruzi DTU characterization of a fatal acute Chagas disease case transmitted orally (EspÃrito Santo state, Brazil). Parasit Vectors 9:477.
DOI: https://doi.org/10.1186/s13071-016-1754-4
Dario MA, Moratelli R, Schwabl P, Jansen AM, Llewellyn MS, 2017a. Small subunit ribosomal metabarcoding reveals extraordinary trypanosomatid diversity in Brazilian bats. PLoS Negl Trop Dis (7):e0005790.
DOI: https://doi.org/10.1371/journal.pntd.0005790
Dario MA, Lisboa CV, Costa LM, Moratelli R, Nascimento MP, Costa LP, Leite YLR, Llewellyn MS, Xavier SCdC, Roque ALR, Jansen AM, 2017b. High Trypanosoma spp. diversity is maintained by bats and triatomines in EspÃrito Santo state, Brazil. PLoS One 12:e0188412.
DOI: https://doi.org/10.1371/journal.pone.0188412
Dario MA, Andrade TES, Dos Santos CB, Fux B, Brandão AA, Falqueto A, 2018. Molecular characterization of Trypanosoma cruzi samples derived from Triatoma vitticeps and Panstrongylus geniculatus of the Atlantic rainforest, southeast Brazil. Parasite 25:59.
DOI: https://doi.org/10.1051/parasite/2018060
de Fuentes-Vicente JA, Cabrera-Bravo M, EnrÃque-Vara JN, Bucio-Torres MI, Gutiérrez-Cabrera AE, Vidal-López DG, MartÃnez-Ibarra JA, Salazar-Schettino PM, Córdoba-Aguilar A, 2017. A relationship between altitude, triatomine (Triatoma dimidiata) immune response and virulence of Trypanosoma cruzi, the casual agent of Chagas’ disease. Med Vet Entomol 31:63-71.
DOI: https://doi.org/10.1111/mve.12198
de Fuentes-Vicente JA, GutÃerrez-Cabrera AE, Flores-Villegas AL, Lowenberger C, Benelli G, Salazar-Schettino PM, Córdoba-Aguilar A, 2018. What makes an effective Chagas disease vector? Factors underlying Trypanosoma cruzi-triatomine interactions. Acta Trop 183:23-31.
DOI: https://doi.org/10.1016/j.actatropica.2018.04.008
Delignette-Muller ML, Dutang C, 2015. Fitdistrplus: an R package for fitting distributions. J Stat Softw 64:1-34.
DOI: https://doi.org/10.18637/jss.v064.i04
de Souza RdCM, Diotaiuti L, Lorenzo MG, Gorla DE, 2010. Analysis of the geographical distribution of Triatoma vitticeps (Stal, 1859) based on data of species occurrence in Minas Gerais, Brazil. Infect Genet Evol 10:720-6.
DOI: https://doi.org/10.1016/j.meegid.2010.05.007
de Souza RdC, Campolina-Silva GH, Bezerra CM, Diotaiuti L, Gorla DE, 2015. Does Triatoma brasiliensis occupy the same environmental niche space as Triatoma melanica?. Parasit Vectors 8:361.
DOI: https://doi.org/10.1186/s13071-015-0973-4
Dias JVL, Queiroz DRM, Martins HR, Gorla DE, Pires HHR, Diotaiuti L, 2016. Spatial distribution of triatomines in domiciles of an urban area of the Brazilian Southeast Region. Mem Inst Oswaldo Cruz 111:43-50.
DOI: https://doi.org/10.1590/0074-02760150352
Elliott P, Wartenberg D, 2004. Spatial epidemiology: current approaches and future challenges. Environ Health Perspect 112:998-1006.
DOI: https://doi.org/10.1289/ehp.6735
Espinoza Echeverria J, Rodriguez AN, Cortez MR, Diotaiuti LG, Gorla DE, 2017. Spatial and temporal distribution of house infestation by Triatoma infestans in the Toro Toro municipality, Potosi, Bolivia. Parasites Vectors 10:58.
DOI: https://doi.org/10.1186/s13071-017-1984-0
Fernández MdP, Gaspe MS, Sartor P, Gürtler RE, 2019. Human Trypanosoma cruzi infection is driven by eco-social interactions in rural communities of the Argentine Chaco. PLoS Negl Trop Dis 13:e0007430.
DOI: https://doi.org/10.1371/journal.pntd.0007430
Ferro e Silva AM, Sobral-Souza T, Vancine MH, Muylaert RL, de Abreu AP, Pelloso SM, Carvalho MDdB, Andrade Ld, Ribeiro MC, Toledo MJdO, 2018. Spatial prediction of risk areas for vector transmission of Trypanosoma cruzi in the State of Paraná, southern Brazil. PLoS Negl Trop Dis 12:e0006907.
DOI: https://doi.org/10.1371/journal.pntd.0006907
Grijalva MJ, Suarez-Davalos V, Villacis AG, Ocaña-Mayorga S, Dangles O, 2012. Ecological factors related to the widespread distribution of sylvatic Rhodnius ecuadoriensis populations in southern Ecuador. Parasit Vectors 5:17.
DOI: https://doi.org/10.1186/1756-3305-5-17
Gurgel-Gonçalves R, Cuba CA, 2009. Predicting the potential geographical distribution of Rhodnius neglectus (Hemiptera, Reduviidae) based on ecological niche modeling. J Med Entomol 46:952-60.
DOI: https://doi.org/10.1603/033.046.0430
Gurgel-Gonçalves R, Galvão C, Costa J, Peterson AT, 2012. Geographic distribution of Chagas disease vectors in Brazil based on ecological niche modeling. J Trop Med 2012:15.
DOI: https://doi.org/10.1155/2012/705326
Ibarra-Cerdeña CN, ZaldÃvar-Riverón A, Peterson AT, Sánchez-Cordero V, Ramsey JM, 2014. Phylogeny and niche conservatism in North and Central American triatomine bugs (Hemiptera: Reduviidae: Triatominae), vectors of Chagas’ disease. PLoS Negl Trop Dis 8:e3266.
DOI: https://doi.org/10.1371/journal.pntd.0003266
Instituto Brasileiro de Geografia e EstatÃstica, 1990. Divisão regional do Brasil em mesorregiões e microrregiões geográficas. Biblioteca IBGE 1:86-7.
Instituto Brasileiro de Geografia e EstatÃstica, 2016. Divisão Territorial Brasileira. Available from: https://www.ibge.gov.br/geociencias/organizacao-do-territorio/divisao-regional/23701-divisao-territorial brasileira.html?=&t=o-que-e
Instituto Brasileiro de Geografia e EstatÃstica, 2019. Ãrea territorial oficial - consulta por Unidade da Federação. Available from: https://www.ibge.gov.br/cidades-e-estados/es/.html?
Jansen AM, Xavier SCDC, Roque ALR, 2020. Landmarks of the knowledge and Trypanosoma cruzi biology in the wild environment. Front Cell Infect Microbiol 10:10.
DOI: https://doi.org/10.3389/fcimb.2020.00010
Kitron U, Clennon JA, Cecere MC, Gürtler RE, King CH, Prokopec GV, 2006. Upscale or downscale: applications of fine scale remotely sensed data to Chagas disease in Argentina and schistosomiasis in Kenya. Geospat Health 1:49-58.
DOI: https://doi.org/10.4081/gh.2006.280
Lamas IR, Pinto LPS, Fonseca M, Lima RPN, Lima RXd, 2006. O corredor central da Mata Atlântica. BrasÃlia: Ministério do Meio Ambiente, Conservação Internacional, SOS Mata Atlântica.
Leite GR, dos Santos CBl, Falqueto A, 2011. Influence of the landscape on dispersal of sylvatic triatomines to anthropic habitats in the Atlantic Forest. J Biogeogr 38:651-63.
DOI: https://doi.org/10.1111/j.1365-2699.2010.02442.x
Lent H, Wygodzinsky P, 1979. Triatominae. Bull Am Mus Nat Hist 163:496-7.
Lewin HA, Robinson GE, Kress WJ, Baker WJ, Coddington J, Crandall KA, Durbin R, Edward SV, Forest F, Gilbert FMTP, Goldstein MM, Grigoriev IV, Hackett KJ, Haussler D, Jarvis ED, Jonhson WE, Patrinos A, Richards S, Castilla-Rubio JC, van Sluys MA, Soltis PS, Xu X, Yang H, Zhang G, 2018. Earth biogenome project: sequencing life for the future of life. PNAS 115:4325-33.
DOI: https://doi.org/10.1073/pnas.1720115115
Lisboa CV, Dietz J, Baker AJ, Jansen AM, 2000. Trypanosoma cruzi infection in Leontopithecus rosalia at the Reserva Biológica de Poco das Antas, Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz 95:445-52.
DOI: https://doi.org/10.1590/S0074-02762000000400002
Lisboa CV, Mangia RH, Luz SL, Kluczkovski Jr A, Ferreira LF, Ribeiro CT, Fernandes O, Jansen AM, 2006. Stable infection of primates with Trypanosoma cruzi I and II. Parasitolology 133:603-11.
DOI: https://doi.org/10.1017/S0031182006000722
Luenam A, Puttanapong N, 2020. Modelling and analyzing spatial clusters of leptospirosis based on satellite-generated measurements of environmental factors in Thailand during 2013-2015. Geospat Health 15:856.
DOI: https://doi.org/10.4081/gh.2020.856
Machado Silva CL, Fonseca SC, Kawa H, Palmer DdOQ, 2017. Spatial distribution of leprosy in Brazil: a literature review. Rev Soc Bras Med Trop 50:439-49.
DOI: https://doi.org/10.1590/0037-8682-0170-2016
Mandal R, Kesari S, Kumar V, Das P, 2018. Trends in spatio-temporal dynamics of visceral leishmaniasis cases in a highlyendemic focus of Bihar, India: na investigation based on GIS tools. Parasit Vectors 11:220.
DOI: https://doi.org/10.1186/s13071-018-2707-x
Miranda LdFC, Pacheco RdS, Pimentel MIF, Salgueiro MdM, da Silva AF, de Mello CX, Barros JHdS, Valete-Rosalino CM, Madeira MdF, Xavier SCdC, Schubach AdO, 2019. Geospatial analysis of tegumentary leishmaniasis in Rio de Janeiro state, Brazil from 2000 to 2015: species typing and flow of travelers and migrants with leishmaniasis. PLoS Negl Trop Dis 13:e0007748.
DOI: https://doi.org/10.1371/journal.pntd.0007748
Monteiro RV, Baldez J, Dietz J, Baker A, Lisboa CV, Jansen AM, 2006. Clinical, biochemical, and electrocardiographic aspects of Trypanosoma cruzi infection in free-ranging golden lion tamarins (Leontopithecus rosalia). J Med Primatol 35:48-55.
DOI: https://doi.org/10.1111/j.1600-0684.2005.00139.x
Moran PAP, 1948. The interpretation of statistical maps. J. Royal Stat Soc Series B 37:243-51.
DOI: https://doi.org/10.1111/j.2517-6161.1948.tb00012.x
Núñez-González S, Gault C, Simancas-Racines D, 2019. Spatial analysis of dengue, cysticercosis and Chagas disease mortality in Ecuador, 2011-2016. Trans R Soc Trop Med Hyg 113:44-7.
DOI: https://doi.org/10.1093/trstmh/try106
Okunlola AO, Oyeyemi OT, 2019. Spatio-temporal analysis of association between incidence of malaria and environmental predictors of malaria transmission in Nigeria. Sci Rep 9:17500.
DOI: https://doi.org/10.1038/s41598-019-53814-x
Organização Pan-Americana de Saúde, 2012. Manual de capacitação na detecção de Trypanosoma cruzi para microscopistas de malária e laboratoristas da rede pública. Modulo III, 155-277 pp.
Osei FB, Stein A, 2017. Spatio-temporal analysis of smallarea intestinal parasites infections in Ghana. Sci Rep 7:12217.
DOI: https://doi.org/10.1038/s41598-017-12397-1
Ostfeld R, Keesing F, 2000. The function of biodiversity in the ecology of vector-borne zoonotic diseases. Can J Zool 78:2061-78.
DOI: https://doi.org/10.1139/z00-172
Parra-Henao G, Quirós-Gómez O, Jaramillo-O N, Cardona ÃS, 2016. Environmental determinants of the distribution of Chagas disease vector Triatoma diminuta in Colombia. AM J Trop Med Hyg 94:767-74.
DOI: https://doi.org/10.4269/ajtmh.15-0197
Pecl GT, Araújo MB, Bell JD, Blanchard J, Bonebrake TC, Chen IC, 2017. Biodiversity redistribution under climate change: Impacts on ecosystems and human well-being. Science 355:eaai9214.
DOI: https://doi.org/10.1126/science.aai9214
Pereira JM, Almeida PSD, Sousa AVD, Paula AMD, Machado RB, Gurgel-Gonçalves R, 2013. Climatic factors influencing triatomine occurrence in Central-West Brazil. Mem Inst Oswaldo Cruz 108:335-41.
DOI: https://doi.org/10.1590/S0074-02762013000300012
Pérez-Morales D, Hernández KDR, MartÃnez I, Agredano-Moreno LT, Jiménez-GarcÃa LF, Espinoza B, 2017. Ultrastructural and physiological changes induced by different stress conditions on the human parasite Trypanosoma cruzi. Cell Stress Chaperones 22:15-27.
DOI: https://doi.org/10.1007/s12192-016-0736-y
Ramsey JM, Ordoñez R, Cruz-Celis A, Alvear AL, Chavez V, Lopez R, Pintor JR, Gama F, Carrillo S, 2000. Distribution of domestic Triatominae and stratification of Chagas disease transmission in Oaxaca, Mexico. Med Vet Entomol 14:19-30.
DOI: https://doi.org/10.1046/j.1365-2915.2000.00214.x
Robertson C, Nelson TA, 2014. An overview of spatial analysis of emerging infectious diseases. Prof Geogr 66:579-588.
DOI: https://doi.org/10.1080/00330124.2014.907702
Rocha ATdF, Espindola GMd, Soares MRA, Rocha JdRdS, Costa CHN, 2018. Visceral leishmaniasis and vulnerability conditions in an endemic urban area of Northeastern Brazil. Trans R Soc Trop Med Hyg 112:317-25.
DOI: https://doi.org/10.1093/trstmh/try058
Roque ALR, Xavier SCC, Rocha MG, Duarte AC, D’Andrea PS, Jansen AM, 2008. Trypanosoma cruzi transmission cycle among wild and domestic mammals in three areas of orally transmitted Chagas disease outbreaks. Am J Trop Med Hyg 79:742-9.
DOI: https://doi.org/10.4269/ajtmh.2008.79.742
Salimi M, Jesri N, Javanbakht M, Farahani LZ, Shirzadi MR, Saghafipour A, 2018. Spatio-temporal distribution analysis of zoonotic cutaneous leishmaniasis in Qom Province, Iran. J Parasit Dis 42:570-6.
DOI: https://doi.org/10.1007/s12639-018-1036-5
Santos CB, Leite GR, Ferreira GEM, Ferreira AL, 2006. Infecção natural de Triatoma vitticeps (Stal, 1859) por flagelados semelhantes a Trypanosoma cruzi (Chagas, 1909) no estado do EspÃrito Santo. Rev Soc Bras Med Trop 39:89-91.
DOI: https://doi.org/10.1590/S0037-86822006000100019
Schmidt KA, Ostfeld RS, 2001. Biodiversity and the dilution effect in disease ecology. Ecology 82:609-19.
DOI: https://doi.org/10.1890/0012-9658(2001)082[0609:BATDEI]2.0.CO;2
Sessa PA, Pimentel RR, Ferreira AL, Falqueto A, 2002. Soroprevalência da doença de Chagas em crianças em idade escolar do Estado do EspÃrito Santo, Brasil, em 1999-2000. Cad Saúde Pública 18:1765-9.
DOI: https://doi.org/10.1590/S0102-311X2002000600031
Simpson JE, Hurtado PJ, Medlock J, Molaei G, Andreadis TG, Galvani AP, Diuk-Wasser MA, 2012. Vector host-feeding preferences drive transmission of multi-host pathogens: West Nile Virus as a model system. Proc Roy Soc B-Biol Sci 279:925-33.
DOI: https://doi.org/10.1098/rspb.2011.1282
SOS Matla Atlântica, 2019. Atlas dos remanescentes florestais da mata atlântica - perÃodo 2017-2018. São Paulo: Fundação SOS Mata Atlântica.
Suarez-Davalos V, Dangles O, Villacis AG, Grijalva MJ, 2010. Microdistribution of sylvatic triatomine populations in central-coastal Ecuador. J Med Entomol 47:80-8.
DOI: https://doi.org/10.1093/jmedent/47.1.80
Tamayo LD, Guhl F, Vallejo GA, RamÃrez JD, 2018. The effect of temperature increases on the development of Rhodnius prolixus and the course of Trypanosoma cruzi metacyclogenesis. PLoS Negl Trop Dis 12:e0006735.
DOI: https://doi.org/10.1371/journal.pntd.0006735
Tewara MA, Mbah-Fongkimeh PN, Dayimu A, Kang F, Xue F, 2018. Small-area spatial statistical analysis of malaria clusters and hotspots in Cameroon; 2000-2015. BMC Infect Dis 18:636.
DOI: https://doi.org/10.1186/s12879-018-3534-6
Vivaldini SM, Pinto FKA, Kohiyama IM, Almeida ECd, Mendes-Correa MC, Santos AF, Ribeiro RA, Pereira GFM, de Araújo WN, 2019. Exploratory spatial analysis of HBV cases in Brazil between 2005 and 2017. Rev Bras Epidemiol 22:E190007.supl.1.
DOI: https://doi.org/10.1590/1980-549720190007.supl.1
Wigglesworth V, Gillett J, 1934. The function of the antennae in Rhodnius prolixus (Hemiptera) and the mechanism of orientation to the host. J Exp Biol 11:120-39.
DOI: https://doi.org/10.1242/jeb.11.2.120
Xavier SCdC, Roque ALR, Lima VdS, Monteiro KJL, Otaviano JCR, Ferreira da Silva LFC, Jansen AM, 2012. Lower richness of small wild mammal species and Chagas disease risk. PLoS Negl Trop Dis 6:e1647.
DOI: https://doi.org/10.1371/journal.pntd.0001647
How to Cite
Dario, M. A., Maranhão, P. H. C. ., dos Santos, G. Q. ., Rocha, M. de M. ., Falqueto, A., da Silva, L. F. C. F. ., Jansen, A. M. ., & das Chagas Xavier, S. C. (2021). Environmental influence on <em>Triatoma vitticeps</em> occurrence and <em>Trypanosoma cruzi</em> infection in the Atlantic Forest of south-eastern Brazil. Geospatial Health, 16(2). https://doi.org/10.4081/gh.2021.997
PAGEPress has chosen to apply the Creative Commons Attribution NonCommercial 4.0 International License (CC BY-NC 4.0) to all manuscripts to be published.
List of Cited By :
