• View in gallery

    (A) Male specimens of Triatoma infestans; (B) head and thorax detail of T. infestans; (C) connexivum detail of T. infestans; and (D) specimen label. This figure appears in color at www.ajtmh.org.

  • 1.

    World Health Organization, 2020. Chagas Disease (American Trypanosomiasis). Geneva, Switzerland: WHO. Available at: http://www.who.int/chagas/en/. Accessed May 5, 2020.

    • Search Google Scholar
    • Export Citation
  • 2.

    Chagas C, 1909. Nova tripanozomiaze humana: estudos sobre a morfolojia e o ciclo evolutivo do Schizotrypanum cruzi n. gen., n. sp., ajente etiolojico de nova entidade morbida do homem. Mem Inst Oswaldo Cruz 1: 159218.

    • Search Google Scholar
    • Export Citation
  • 3.

    Galvão C, 2014. Vetores da doença de Chagas no Brasil. Curitiba, Brazil: Sociedade Brasileira de Zoologia.

  • 4.

    Dorn PL, Just AS, Dale C, Stevens L, Galvão C, Cordon RL, Monroy C, 2018. Description of Triatoma mopan sp. n. (Hemiptera, Reduviidae, Triatominae) from a cave in Belize. Zookeys 775: 6995.

    • Search Google Scholar
    • Export Citation
  • 5.

    Lima-Cordón RA, Monroy MC, Stevens L, Rodas A, Rodas GA, Dorni PL, Justi AS, 2019. Description of Triatoma huehuetenanguensis sp. n., a potential Chagas disease vector (Hemiptera, Reduviidae, Triatominae). Zookeys 820: 5170.

    • Search Google Scholar
    • Export Citation
  • 6.

    Nascimento JD 2019. Taxonomical over splitting in the Rhodnius prolixus (Insecta: Hemiptera: Reduviidae) clade: are R. taquarussuensis (da Rosa et al., 2017) and R. neglectus (Lent, 1954) the same species? PLoS One 14: 0211285.

    • Search Google Scholar
    • Export Citation
  • 7.

    Oliveira J, Ayala JM, Justi SA, Rosa JA, Galvão C, 2018. Description of a new species of Nesotriatoma Usinger, 1944 from Cuba and revalidation of synonymy between Nesotriatoma bruneri (Usinger, 1944) and N. flavida (Neiva, 1911) (Hemiptera, Reduviidae, Triatominae). J Vect Ecol 43: 148157.

    • Search Google Scholar
    • Export Citation
  • 8.

    Poinar G, 2019. A primitive triatomine bug, Paleotriatoma metaxytaxa gen. et sp. nov. (Hemiptera: Reduviidae: Triatominae), in mid-Cretaceous amber from northern Myanmar. Cretac Res 93: 9097.

    • Search Google Scholar
    • Export Citation
  • 9.

    Gorla D, Noireau F, 2017. Geographic distribution of Triatominae vectors in America. Telleria J, Tibayrenc M, eds. American Trypanosomiasis Chagas Disease. Amsterdam, The Netherlands: Elsevier, 197221.

    • Search Google Scholar
    • Export Citation
  • 10.

    Souza EDS, Von Atzingen NCB, Furtado MB, Oliveira JD, Nascimento JD, Vendrami DP, Gardim S, Rosa JA, 2016. Description of Rhodnius marabaensis sp. n. (Hemiptera, Reduviidade, Triatominae) from Pará State, Brazil. ZooKeys 621: 4562.

    • Search Google Scholar
    • Export Citation
  • 11.

    Dujardin JP, Schofield CJ, Tibayrenc M, 1998. Population structure of Andean Triatoma infestans: allozyme frequencies and their epidemiological relevance. Med Vet Entomol 12: 2029.

    • Search Google Scholar
    • Export Citation
  • 12.

    Schofield CJ, 1998. Biosystematics of the Triatominae. Service MW, ed. Biosystematics of Haematophagous Insects. Oxford, England: Claredon Press.

    • Search Google Scholar
    • Export Citation
  • 13.

    Pessoa GCD, Rosa ACL, Bedin C, Wilhelms T, Mello F, Coutinho HS, Fonseca EOL, Santos RF, Diotaiuti L, 2015. Susceptibility characterization of residual Brazilian populations of Triatoma infestans Klug, 1834 (Hemiptera: Reduviidae) to deltamethrin pyrethroid. Rev Soc Bras Med Trop 48: 157161.

    • Search Google Scholar
    • Export Citation
  • 14.

    Vinhaes MC, Dias JCP, 2000. Chagas disease in Brazil. Cad Saude Publica 16: 712.

  • 15.

    Dias JC, Silveira AC, Schofield CJ, 2002. The impact of Chagas disease control in Latin America: a review. Mem Inst Oswaldo Cruz 97: 603612.

  • 16.

    Lent H, Wygodzinsky P, 1979. Revision of the Triatominae (Hemiptera, Reduviidae), and their significance as vectors of Chagas’ disease. Bull Am Mus Nat Hist 163: 123520.

    • Search Google Scholar
    • Export Citation
  • 17.

    Borsatto KC, Azeredo-Oliveira MTV, Alevi KCC, 2019. CytoKey: identification key for the Chagas disease vectors of the largest Brazilian urban center, based on cytogenetics data. Am J Trop Med Hyg 101: 113115.

    • Search Google Scholar
    • Export Citation
  • 18.

    Borsatto KC, Azeredo-Oliveira MTV, Alevi KCC, 2018. Identification key for the Chagas disease vectors of five Brazilian states, based on cytogenetics data. Am J Trop Med Hyg 100: 303305.

    • Search Google Scholar
    • Export Citation
  • 19.

    Santos CB, Leite GR, Ferreira GEM, Ferreira AL, 2006. Infecção natural de Triatoma vitticeps (Stal, 1859) por flagelados morfologicamente semelhantes a Trypanosoma cruzi (Chagas, 1909) no Estado do Espírito Santo, Brasil. Rev Soc Bras Med Trop 39: 8991.

    • Search Google Scholar
    • Export Citation
  • 20.

    Santos UM, Pinto AFS, Almeida AZ, Zanganelli FL, Carrancho PV, Netto NA, 1969. Doença de Chagas no estado do Espírito Santo–III–Vetores do tripanosoma. Rev Soc Bras Med Trop 3: 5152.

    • Search Google Scholar
    • Export Citation
  • 21.

    Barros GC, Mayrink W, Abreu Salgado AA, Barros RCG, Sessa PA, 1975. Contribuição para o conhecimento da doença de Chagas autóctone no estado do Espírito Santo. Rev Soc Bras Med Trop 17: 319329.

    • Search Google Scholar
    • Export Citation
  • 22.

    Sessa PA, Pimentel RR, Ferreira AL, Falqueto A, 2002. Soroprevalência da doença de Chagas em crianças em idade escolar do Estado do Espírito Santo, Brasil, em 1999–2000. Cad Saúde Púb 18: 17651769.

    • Search Google Scholar
    • Export Citation
  • 23.

    Barros GC, Sessa PA, Barros RC, Matos EA, 1980. Inquérito sorológico sobre doença de Chagas no banco de sangue do hospital das Clínicas da Universidade Federal do Espírito Santo. Rev Pat Trop 9: 153156.

    • Search Google Scholar
    • Export Citation
  • 24.

    Madeira FF, Menezes ALR, Jesus AC, Moraes MHS, Oliveira J, Rosa JA, Camargo LMA, Meneguetti DLO, Berrnarde PS, 2020. First report of Rhodnius montenegrensis (Hemiptera, Reduviidae, Triatominae) in Amazonas, Brazil. Rev Soc Bras Med Trop 53: 20190436.

    • Search Google Scholar
    • Export Citation
  • 25.

    Ramos LJ, Souza JL, Souza CR, Oliveira J, Rosa JA, Camargo LMA, Cunha RM, Meneguetti DUO, 2018. First report of Triatoma sordida Stål, 1859 (Hemiptera, Reduviidae, Triatominae) in the State of Acre and Brazilian western Amazon. Rev Soc Bras Med Trop 51: 7779.

    • Search Google Scholar
    • Export Citation
  • 26.

    Ramos LJ, Castro GVS, Souza JL, Oliveira J, Rosa JA, Camargo LMA, Cunha RM, Meneguetti DUO, 2018. First report of Rhodnius neglectus (Hemiptera, Reduviidae, Triatominae) from the State of Acre, Brazil, and the Brazilian western Amazon region. Rev Soc Bras Med Trop 51: 212214.

    • Search Google Scholar
    • Export Citation
  • 27.

    Meneguetti DUO, Castro GVS, Souza JL, Oliveira J, Rosa JA, Camargo LMA, 2016. First report of Rhodnius stali (Hemiptera, Reduviidae, Triatominae) in the State of Acre and in the Brazilian Amazon. Rev Soc Bras Med Trop 49: 365368.

    • Search Google Scholar
    • Export Citation
  • 28.

    Meneguetti DUO, Tojal SD, Miranfda PRM, Rosa JA, Camargo LMA, 2015. First report of Rhodnius montenegrensis (Hemiptera, Reduviidae, Triatominae) in the State of Acre, Brazil. Rev Soc Bras Med Trop 48: 471473.

    • Search Google Scholar
    • Export Citation
  • 29.

    Castro MALR, Castro GVS, Souza JL, Souza CR, Ramos LJ, Oliveira J, Rosa JA, Camargo LMA, 2018. First report of Panstrongylus megistus (Hemiptera, Reduviidae, Triatominae) in the State of Acre and Rondônia, Amazon, Brazil. Acta Trop 182: 158160.

    • Search Google Scholar
    • Export Citation
  • 30.

    Oliveira AS, Ribeiro MAL, Castro GVS, Brilhante NA, Camargo LMA, Meneguetti DUO, 2019. Confirmation of the occurrence of Panstrongylus rufotuberculatus in the state of Acre, western Amazon. Rev Soc Bras Med Trop 52: e20180388.

    • Search Google Scholar
    • Export Citation
  • 31.

    Ribeiro MAL, Castro GVS, Souza JL, Cardoso AS, Madeira FP, Camargo LMA, Meneguetti DUO, 2019. First report of Panstrongylus lignarius (Walker, 1873) (Hemiptera: Reduviidae: Triatominae) in the State of Acre, Brazil. Rev Soc Bras Med Trop 52: e20180307.

    • Search Google Scholar
    • Export Citation
  • 32.

    Terassini FA, Stefanello C, Camargo LMA, Meneguetti DUO, 2017. First report of Panstrongylus lignarius Walker, 1873 (Hemiptera, Reduviidae, Triatominae), in the State of Rondônia, Brazil. Rev Soc Bras Med Trop 50: 547549.

    • Search Google Scholar
    • Export Citation
  • 33.

    Abad-Franch F, Pavan MG, Jaramillo N, Palomeque FS, Dale C, Chaverra D, Monteiro FA, 2013. Rhodnius barretti, a new species of Triatominae (Hemiptera: Reduviidae) from western Amazonia. Mem Inst Oswaldo Cruz 108: 9299.

    • Search Google Scholar
    • Export Citation

 

 

 

 

 

Chagas Disease Vectors of Espírito Santo, Brazil: First Report of Triatoma infestans (Klug, 1834) (Hemiptera, Triatominae) in the Brazilian State and Development of an Identification Key Based on Cytogenetic Data

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  • 1 Departamento de Ciências Biológicas, Faculdade de Ciências Farmacêuticas, Laboratório de Parasitologia, Universidade Estadual Paulista “Júlio de Mesquita Filho” (UNESP), Araraquara, Brazil

ABSTRACT

Chagas disease is a potentially life-threatening illness caused by the protozoan Trypanosoma cruzi and transmitted, mainly, by hematophagous insects of the Triatominae subfamily. In Brazil, there are currently about 66 triatomine species distributed throughout the country’s 27 states. Triatoma infestans is considered as a species of great vectorial importance, mainly because of its biological characteristics, such as the high degree of anthropophilia, adaptation to the home environment, ability to withstand long periods of fasting, and present a wide geographical distribution. Taking into account the epidemiological importance of these species, we carried out the first report of T. infestans in the Espírito Santo, Brazil, and development of an identification key for all species notified in that state, based on cytogenetic data. This information is important because they contribute to the direction of epidemiological surveillance activities carried out by vector control programs of the Espírito Santo, Brazil.

Chagas disease is a potentially life-threatening illness caused by the protozoan Trypanosoma cruzi (Chagas, 1909) (Kinetoplastida, Trypanosomatidae) and transmitted, mainly, by hematophagous insects of the Triatominae subfamily (Hemiptera, Reduviidae).1,2 An estimated 8 million people are infected with T. cruzi worldwide, mainly in Latin America where this disease remains one of the biggest public health problems, causing incapacity in infected individuals and more than 10,000 deaths per year.1

Vector control remained the most effective method of preventing transmission of this neglected disease in Latin America,1 because of the 154 species described (grouped into 19 genera and five tribes),38 more than 130 were reported in this region of the American continent,9 and all are considered as potential vectors of Chagas disease.

In Brazil, there are currently about 66 triatomine species distributed throughout the country’s 27 states,3,10 being five of them with greater importance in the domiciliary transmission of Chagas disease, namely, Triatoma brasiliensis (Neiva, 1911), Triatoma pseudomaculata (Corrêa and Espínola, 1964), Triatoma sordida (Stål, 1859), Panstrongylus megistus (Burmeister, 1835), and Triatoma infestans (Klug, 1834).3 In the state of Espírito Santo, for example, there are seven species notified (P. megistus, Panstrongylus diasi [Pinto and Lent, 1946], Panstrongylus geniculatus [Latreille, 1811], Cavernicola pilosa [Barber, 1937], Rhodnius domesticus [Neiva and Pinto, 1923], Triatoma tibiamaculata [Pinto, 1926], and Triatoma vitticeps [Stål, 1859]), with T. vitticeps being the most prevalent species.9

Triatoma infestans is considered as a species of great vectorial importance, mainly because of its biological characteristics, such as the high degree of anthropophilia, adaptation to the home environment, ability to withstand long periods of fasting, and present a wide geographical distribution.11,12 Although there are currently only rare residual foci in Rio Grande do Sul and Bahia13 (because of the success of the control programs of the Ministry of Health that resulted in a reduction of 99.3% reduction in the number of specimens captured between 1983 and 1997),13 this triatomine has been reported in 17 Brazilian states: Alagoas, Bahia, Goiás, Maranhão, Mato Grosso, Mato Grosso do Sul, Minas Gerais, Paraná, Paraíba, Pernambuco, Piauí, Rio de Janeiro, Rio Grande do Sul, Santa Catarina, Sergipe, São Paulo, and Tocantins.3

Based on a survey carried out in the entomological collection of Museum of Zoology of the University of São Paulo, São Paulo, Brazil, the presence of a specimen of T. infestans deposited from the state of Espírito Santo was observed, which was collected in 1956 (Figure 1A and D) (time when chemical control with pyrethroids had not yet been implemented in Brazil).14,15 Taking into account the epidemiological importance of these species, we carried out the first report of T. infestans in this Brazilian state and development of an identification key for all species notified in that state, based on cytogenetic data.

Figure 1.
Figure 1.

(A) Male specimens of Triatoma infestans; (B) head and thorax detail of T. infestans; (C) connexivum detail of T. infestans; and (D) specimen label. This figure appears in color at www.ajtmh.org.

Citation: The American Journal of Tropical Medicine and Hygiene 104, 2; 10.4269/ajtmh.20-0492

The morphological pattern of the specimen analyzed (and which confirms to be a T. infestans based on the keys of Lent and Wygodzinsky16 and Galvão3) was 1) black neck with a pair of yellowish side spots (Figure 1B); 2) pronotum totally black, fore lobe with a pair of disc tubers and small lateral tubers, and hide lobe rough (Figure 1B); 3) rugged black scutellum (Figure 1B); 4) legs completely black with the trochanters and base of the yellowish femurs (Figure 1B); 5) anterior and middle femurs with a pair of small subapical denticles (Figure 1B); and 6) black connexivum, being each segment with a large yellow spot away from the anterior suture, but closely close to the border of the posterior segment (Figure 1C).

Based on the keys of Borsatto et al.,17,18 cytogenetic data available in the literature (karyotype and constitutive heterochromatin pattern in chromatin and chromosomes) for the six of the seven species notified in Espírito Santo (with the exception of P. diasi that does not present cytogenetic data available in the literature) more T. infestans were grouped and used for the construction of the identification key (Table 1).3

Table 1

Key for the triatomines of the Espírito Santo state based on cytogenetic data

Identification key
1. Karyotype with 2n = 21 chromosomes (18A + X1X2Y)Panstrongylus megistus
2. Karyotype with 2n = 22 chromosomes (20A + XY)3
3a. Prophase without heterochromatin blocks dispersed inside the nucleusCavernicola pilosa
3b. Prophase with heterochromatic blocks dispersed inside the nucleus4
4a. Heterochromatin in 3–4 large pairs of autosomesTriatoma infestans
4b. Heterochromatin in some autosomesRhodnius domesticus
5. Karyotype with 2n = 23 chromosomes (20A + X1X2Y)6
6a. Prophase without heterochromatin blocks dispersed inside the nucleusPanstrongylus geniculatus
6b. Prophase with heterochromatic blocks dispersed inside the nucleusTriatoma tibiamaculata
7. Karyotype with 2n = 24 chromosomes (20A + X1X2X3Y)Triatoma vitticeps

The ento-epidemiological surveys in Espírito Santo show that T. vitticeps is the most prevalent species in the state.9 This species that has a high rate of natural infection by T. cruzi19 has already been found in domiciliary regions,20 being associated with some autochthonous cases of Chagas disease in the state.21,22 However, the prevalence of human infection by T. cruzi in this state has always been low in surveys carried out in the general population, among schoolchildren or in blood banks,21,23 which resulted in the classification of Espírito Santo as an epidemiological surveillance area where vector control measures need not be adopted.22 However, Santos et al.19 highlight that the high natural infection rates observed for Espírito Santo reinforce the need to maintain entomological surveillance in areas where this vector occurs.

Several species of triatomines have recently been reported in Brazilian states: Rhodnius montenegrensis (Rosa et al., 2012) in Amazonas24; T. sordida and Rhodnius neglectus (Lent, 1954); Rhodnius stali (Lent, Jurberg, and Galvão, 1993); R. montenegrensis, P. megistus, and Panstrongylus rufotuberculatus (Champion, 1899); Panstrongylus lignarius (Walker, 1873) in Acre2531; P. lignarius and P. megistus in Rondonia29,32; and, now, T. infestans in Espírito Santo. These ento-epidemiological surveys are of great importance for public health because the knowledge of fauna (local, regional, municipal, and/or state) of triatomines directly assists in the activities of vector control programs.

In addition to the notification of the presence of T. infestans in Espírito Santo, the development of the identification key based on cytogenetic data is also an alternative for assisting in the activities of vector control programs because the correct classification of triatomines is essential for biological, ecological, and epidemiological data to be recovered by health agents (which can direct in choosing the prophylactic measures to be adopted).

Borsatto et al.17,18 developed keys for São Paulo, Alagoas, Amapa, Ceara, Roraima, and Santa Catarina based on cytogenetic data. Although most identification keys are based on morphological data,3 the use of cytogenetic data is an alternative tool for morphological keys (mainly for species that are difficult to distinguish, such as species of the genus Rhodnius33). In addition, the classic cytogenetic techniques (such as those used to obtain the aggregated results in the Espírito Santo identification key) are extremely simple and of low cost, which allows their use by health agents.

So, we notified for the first time the presence of T. infestans in the state of Espírito Santo, and we developed an identification key based on cytogenetic data for the triatomine species present in that Brazilian state, contributing to the direction of epidemiological surveillance activities carried out by vector control programs.

ACKNOWLEDGMENTS

We especially thank Sonia Aparecida Casari and Carlos Campaner for their access and attention and support in the entomological collection. The first author (J. O.) thanks the “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior 001” (CAPES) and the second author (J. A. R.) thanks the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and thanks the “Fundação de Amparo à Pesquisa do Estado de São Paulo” (FAPESP) (Process number 2017/06460-4).

REFERENCES

  • 1.

    World Health Organization, 2020. Chagas Disease (American Trypanosomiasis). Geneva, Switzerland: WHO. Available at: http://www.who.int/chagas/en/. Accessed May 5, 2020.

    • Search Google Scholar
    • Export Citation
  • 2.

    Chagas C, 1909. Nova tripanozomiaze humana: estudos sobre a morfolojia e o ciclo evolutivo do Schizotrypanum cruzi n. gen., n. sp., ajente etiolojico de nova entidade morbida do homem. Mem Inst Oswaldo Cruz 1: 159218.

    • Search Google Scholar
    • Export Citation
  • 3.

    Galvão C, 2014. Vetores da doença de Chagas no Brasil. Curitiba, Brazil: Sociedade Brasileira de Zoologia.

  • 4.

    Dorn PL, Just AS, Dale C, Stevens L, Galvão C, Cordon RL, Monroy C, 2018. Description of Triatoma mopan sp. n. (Hemiptera, Reduviidae, Triatominae) from a cave in Belize. Zookeys 775: 6995.

    • Search Google Scholar
    • Export Citation
  • 5.

    Lima-Cordón RA, Monroy MC, Stevens L, Rodas A, Rodas GA, Dorni PL, Justi AS, 2019. Description of Triatoma huehuetenanguensis sp. n., a potential Chagas disease vector (Hemiptera, Reduviidae, Triatominae). Zookeys 820: 5170.

    • Search Google Scholar
    • Export Citation
  • 6.

    Nascimento JD 2019. Taxonomical over splitting in the Rhodnius prolixus (Insecta: Hemiptera: Reduviidae) clade: are R. taquarussuensis (da Rosa et al., 2017) and R. neglectus (Lent, 1954) the same species? PLoS One 14: 0211285.

    • Search Google Scholar
    • Export Citation
  • 7.

    Oliveira J, Ayala JM, Justi SA, Rosa JA, Galvão C, 2018. Description of a new species of Nesotriatoma Usinger, 1944 from Cuba and revalidation of synonymy between Nesotriatoma bruneri (Usinger, 1944) and N. flavida (Neiva, 1911) (Hemiptera, Reduviidae, Triatominae). J Vect Ecol 43: 148157.

    • Search Google Scholar
    • Export Citation
  • 8.

    Poinar G, 2019. A primitive triatomine bug, Paleotriatoma metaxytaxa gen. et sp. nov. (Hemiptera: Reduviidae: Triatominae), in mid-Cretaceous amber from northern Myanmar. Cretac Res 93: 9097.

    • Search Google Scholar
    • Export Citation
  • 9.

    Gorla D, Noireau F, 2017. Geographic distribution of Triatominae vectors in America. Telleria J, Tibayrenc M, eds. American Trypanosomiasis Chagas Disease. Amsterdam, The Netherlands: Elsevier, 197221.

    • Search Google Scholar
    • Export Citation
  • 10.

    Souza EDS, Von Atzingen NCB, Furtado MB, Oliveira JD, Nascimento JD, Vendrami DP, Gardim S, Rosa JA, 2016. Description of Rhodnius marabaensis sp. n. (Hemiptera, Reduviidade, Triatominae) from Pará State, Brazil. ZooKeys 621: 4562.

    • Search Google Scholar
    • Export Citation
  • 11.

    Dujardin JP, Schofield CJ, Tibayrenc M, 1998. Population structure of Andean Triatoma infestans: allozyme frequencies and their epidemiological relevance. Med Vet Entomol 12: 2029.

    • Search Google Scholar
    • Export Citation
  • 12.

    Schofield CJ, 1998. Biosystematics of the Triatominae. Service MW, ed. Biosystematics of Haematophagous Insects. Oxford, England: Claredon Press.

    • Search Google Scholar
    • Export Citation
  • 13.

    Pessoa GCD, Rosa ACL, Bedin C, Wilhelms T, Mello F, Coutinho HS, Fonseca EOL, Santos RF, Diotaiuti L, 2015. Susceptibility characterization of residual Brazilian populations of Triatoma infestans Klug, 1834 (Hemiptera: Reduviidae) to deltamethrin pyrethroid. Rev Soc Bras Med Trop 48: 157161.

    • Search Google Scholar
    • Export Citation
  • 14.

    Vinhaes MC, Dias JCP, 2000. Chagas disease in Brazil. Cad Saude Publica 16: 712.

  • 15.

    Dias JC, Silveira AC, Schofield CJ, 2002. The impact of Chagas disease control in Latin America: a review. Mem Inst Oswaldo Cruz 97: 603612.

  • 16.

    Lent H, Wygodzinsky P, 1979. Revision of the Triatominae (Hemiptera, Reduviidae), and their significance as vectors of Chagas’ disease. Bull Am Mus Nat Hist 163: 123520.

    • Search Google Scholar
    • Export Citation
  • 17.

    Borsatto KC, Azeredo-Oliveira MTV, Alevi KCC, 2019. CytoKey: identification key for the Chagas disease vectors of the largest Brazilian urban center, based on cytogenetics data. Am J Trop Med Hyg 101: 113115.

    • Search Google Scholar
    • Export Citation
  • 18.

    Borsatto KC, Azeredo-Oliveira MTV, Alevi KCC, 2018. Identification key for the Chagas disease vectors of five Brazilian states, based on cytogenetics data. Am J Trop Med Hyg 100: 303305.

    • Search Google Scholar
    • Export Citation
  • 19.

    Santos CB, Leite GR, Ferreira GEM, Ferreira AL, 2006. Infecção natural de Triatoma vitticeps (Stal, 1859) por flagelados morfologicamente semelhantes a Trypanosoma cruzi (Chagas, 1909) no Estado do Espírito Santo, Brasil. Rev Soc Bras Med Trop 39: 8991.

    • Search Google Scholar
    • Export Citation
  • 20.

    Santos UM, Pinto AFS, Almeida AZ, Zanganelli FL, Carrancho PV, Netto NA, 1969. Doença de Chagas no estado do Espírito Santo–III–Vetores do tripanosoma. Rev Soc Bras Med Trop 3: 5152.

    • Search Google Scholar
    • Export Citation
  • 21.

    Barros GC, Mayrink W, Abreu Salgado AA, Barros RCG, Sessa PA, 1975. Contribuição para o conhecimento da doença de Chagas autóctone no estado do Espírito Santo. Rev Soc Bras Med Trop 17: 319329.

    • Search Google Scholar
    • Export Citation
  • 22.

    Sessa PA, Pimentel RR, Ferreira AL, Falqueto A, 2002. Soroprevalência da doença de Chagas em crianças em idade escolar do Estado do Espírito Santo, Brasil, em 1999–2000. Cad Saúde Púb 18: 17651769.

    • Search Google Scholar
    • Export Citation
  • 23.

    Barros GC, Sessa PA, Barros RC, Matos EA, 1980. Inquérito sorológico sobre doença de Chagas no banco de sangue do hospital das Clínicas da Universidade Federal do Espírito Santo. Rev Pat Trop 9: 153156.

    • Search Google Scholar
    • Export Citation
  • 24.

    Madeira FF, Menezes ALR, Jesus AC, Moraes MHS, Oliveira J, Rosa JA, Camargo LMA, Meneguetti DLO, Berrnarde PS, 2020. First report of Rhodnius montenegrensis (Hemiptera, Reduviidae, Triatominae) in Amazonas, Brazil. Rev Soc Bras Med Trop 53: 20190436.

    • Search Google Scholar
    • Export Citation
  • 25.

    Ramos LJ, Souza JL, Souza CR, Oliveira J, Rosa JA, Camargo LMA, Cunha RM, Meneguetti DUO, 2018. First report of Triatoma sordida Stål, 1859 (Hemiptera, Reduviidae, Triatominae) in the State of Acre and Brazilian western Amazon. Rev Soc Bras Med Trop 51: 7779.

    • Search Google Scholar
    • Export Citation
  • 26.

    Ramos LJ, Castro GVS, Souza JL, Oliveira J, Rosa JA, Camargo LMA, Cunha RM, Meneguetti DUO, 2018. First report of Rhodnius neglectus (Hemiptera, Reduviidae, Triatominae) from the State of Acre, Brazil, and the Brazilian western Amazon region. Rev Soc Bras Med Trop 51: 212214.

    • Search Google Scholar
    • Export Citation
  • 27.

    Meneguetti DUO, Castro GVS, Souza JL, Oliveira J, Rosa JA, Camargo LMA, 2016. First report of Rhodnius stali (Hemiptera, Reduviidae, Triatominae) in the State of Acre and in the Brazilian Amazon. Rev Soc Bras Med Trop 49: 365368.

    • Search Google Scholar
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Author Notes

Address correspondence to Kaio Cesar Chaboli Alevi, Departamento de Ciências Biológicas, Faculdade de Ciências Farmacêuticas, Laboratório de Parasitologia, Universidade Estadual Paulista “Júlio de Mesquita Filho,” FCFAR/UNESP, Rodovia Araraquara-Jaú km 1, Araraquara 14801-902, Brazil. E-mail: kaiochaboli@hotmail.com

Authors’ addresses: Jader de Oliveira, João Aristeu da Rosa, and Kaio Cesar Chaboli Alevi, Departamento de Ciências Biológicas, Faculdade de Ciências Farmacêuticas, Laboratório de Parasitologia, Universidade Estadual Paulista “Júlio de Mesquita Filho” (UNESP), Araraquara, Brazil, E-mails: jdr.oliveira@hotmail.com, joaoaristeu@gmail.com, and kaiochaboli@hotmail.com.

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