• 1.

    World Health Organization, 2018. Chagas Disease (American trypanosomiasis). Available at: http://www.who.int/chagas/en/. Accessed August 14, 2018.

  • 2.

    Oliveira JD, Alevi KC, 2017. Taxonomic status of Panstrongylus herreri Wygodzinsky, 1948 and the number of Chagas disease vectors. Rev Soc Bras Med Trop 50: 434435.

    • Search Google Scholar
    • Export Citation
  • 3.

    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 Vector Ecol 43: 148157.

    • Search Google Scholar
    • Export Citation
  • 4.

    Dorn PL, Just SA, 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.

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

  • 6.

    Mendonça VJ, Alevi KCC, Pinotti H, Gurgel-Gonçalves R, Pita S, Guerra AL, Panzera F, Araújo RF, Azeredo-Oliveira MTC, Rosa JA, 2016. Revalidation of Triatoma bahiensis Sherlock & Serafim, 1967 (Hemiptera: Reduviidae) and phylogeny of the T. brasiliensis species complex. Zootaxa 4107: 239254.

    • Search Google Scholar
    • Export Citation
  • 7.

    Souza ES, Von Atzingen NCB, Furtado MB, Oliveira J, 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
  • 8.

    Rosa JA, Justino HHG, Nascimento JD, Mendonça VJ, Rocha CS, Carvalho DB, Falcone R, Azeredo-Oliveira MTV, Alevi KCC, Oliveira J, 2017. A new species of Rhodnius from Brazil (Hemiptera, Reduviidae, Triatominae). ZooKeys 675: 125.

    • Search Google Scholar
    • Export Citation
  • 9.

    Instituto Brasileiro de Geografia e Estatística, 2010. Available at: https://cidades.ibge.gov.br/brasil/sp/sao-paulo/panorama. Accessed August 14, 2018.

  • 10.

    Corrêa RR, Ferreira AO, 1959. Distribuição geográfica, habitats e infecção do Triatoma sordida no Estado de São Paulo, Rev Inst Med Trop São Paulo 1: 207213.

    • Search Google Scholar
    • Export Citation
  • 11.

    Rodrigues VLCC, Ferraz Filho AN, Silva EOR, Lima VLC, 1992. Prevalência, índices de infecção e hábitos alimentares de triatomíneos capturados em uma área de vigilância epidemiológica. Rev Soc Bras Med Trop 25: 183190.

    • Search Google Scholar
    • Export Citation
  • 12.

    Carvalho ME, Silva RA, Barata JM, Domingos MF, Ciaravolo RM, Zacharias F, 2003. Chagas’ disease in the southern coastal region of Brazil. Rev Saúde Públ 37: 4958.

    • Search Google Scholar
    • Export Citation
  • 13.

    Ceretti-Junior W, Vendramini DP, Matos-Junior MO, Ribeiro AR, Alvarez JV, Marques S, Duarte NA, Silva RA, Rosa JA, Marrelli MT, 2018. Occurrences of triatomines (Hemiptera: Reduviidae) and first reports of Panstrongylus geniculatus in urban environments in the city of São Paulo, Brazil. Rev Inst Med Trop São Paulo 60: e33.

    • Search Google Scholar
    • Export Citation
  • 14.

    Ribeiro AR, Oliveira RC, Ceretti-Junior W, Lima L, Almeida LA, Nascimento JD, Teixeira MM, Rosa JA, 2016. Trypanosoma cruzi isolated from a triatomine found in one of the biggest metropolitan areas of Latin America. Rev Soc Bras Med Trop 49: 183189.

    • Search Google Scholar
    • Export Citation
  • 15.

    Carbajal de la Fuente AL, Jaramillo N, Barata JMS, Noireau F, Diotaiuti L, 2011. Misidentification of two Brazilian triatomes, Triatoma arthurneivai and Triatoma wygodzinskyi, revealed by geometric morphometrics. Med Vet Entomol 25: 178183.

    • Search Google Scholar
    • Export Citation
  • 16.

    Alevi KCC, Imperador CHL, Moreira FFF, Jurberg J, Azeredo-Oliveira MTV, 2016. Differentiation between Triatoma arthurneivai and Triatoma wygodzinskyi (Hemiptera: Reduviidae: Triatominae) using cytotaxonomy. Gen Mol Res 15: 15.

    • Search Google Scholar
    • Export Citation
  • 17.

    Alevi KCC, Moreira FFF, Jurberg J, Azeredo-Oliveira MTV, 2016. Description of 161 the diploid chromosome set of Triatoma pintodiasi (Hemiptera, Triatominae). Gen Mol Res 25: 15.

    • Search Google Scholar
    • Export Citation
  • 18.

    Panzera F et al. 1998. Cytogenetics of triatomines. Carcavallo RU, ed. Atlas of Chagas Disease Vectors in the Americas. Rio de Janeiro, Brazil: Fiocruz, 621664.

    • Search Google Scholar
    • Export Citation
  • 19.

    Panzera F, Pérez R, Panzera Y, Ferrandis I, Ferreiro MJ, Calleros L, 2010. Cytogenetics and genome evolution in the subfamily Triatominae (Hemiptera, Reduviidae). Cytogenet Genome Res 128: 7787.

    • Search Google Scholar
    • Export Citation
  • 20.

    Panzera Y, Pita S, Ferreiro MJ, Ferrandis I, Lages C, Pérez R, Silva AE, Guerra M, Panzera F, 2012. High dynamics of rDNA cluster location in kissing bug holocentric chromosomes (Triatominae, Heteroptera). Cytogenet Genome Res 138: 5667.

    • Search Google Scholar
    • Export Citation
  • 21.

    Crossa RP et al. 2002. Chromosomal evolution trends of the genus Panstrongylus (Hemiptera, Reduviidae), vectors of Chagas disease. Infect Genet Evol 2: 4756.

    • Search Google Scholar
    • Export Citation
  • 22.

    Panzera F, Hornos S, Pereira J, Cestau R, Canale D, Diotaiuti L, Dujardin JP, Perez R, 1997. Genetic variability and geographic differentiation among three species of triatomine bugs (Hemiptera-Reduviidae). Am J Trop Med Hyg 57: 732739.

    • Search Google Scholar
    • Export Citation
  • 23.

    Alevi KCC, Rodas LAC, Tartarotti E, Azeredo-Oliveira MTV, Guirado MM, 2015. Entoepidemiology of Chagas disease in the western region of the state of São Paulo from 2004 to 2008, and cytogenetic analysis in Rhodnius neglectus (Hemiptera, Triatominae). Gen Mol Res 14: 57755784.

    • Search Google Scholar
    • Export Citation
 
 
 

 

 
 
 

 

 

 

 

 

 

CytoKey: Identification Key for the Chagas Disease Vectors of the Largest Brazilian Urban Center (São Paulo State), Based on Cytogenetic Data

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  • 1 Laboratório de Biologia Celular, Departamento de Biologia, Instituto de Biociências, Letras e Ciências Exatas, Universidade Estadual Paulista “Júlio de Mesquita Filho” (IBILCE/UNESP), São José do Rio Preto, Brazil;
  • | 2 Instituto de Biociências de Botucatu, Universidade Estadual Paulista “Júlio de Mesquita Filho” (IBB/UNESP), Botucatu, Brazil;
  • | 3 Laboratório de Parasitologia, Departamento de Ciências Biológicas, Faculdade de Ciências Farmacêuticas, Universidade Estadual Paulista “Júlio de Mesquita Filho” (FCFAR/UNESP), Araraquara, Brazil

Chagas disease is caused by the protozoan Trypanosoma cruzi. This disease is distributed in 21 Latin American countries, where it is mostly vector-borne. In Brazil, there are 68 triatomine species. To date, the epidemiological surveys indicate that the state of São Paulo presents 11 species of triatomines, and most of these species have already been collected in a home environment and found to be infected with T. cruzi. Problems in correctly identifying species can lead to incorrect panorama of distribution of Chagas disease vectors. Thus, we developed an identification key for the triatomines of the state of São Paulo, based on cytogenetic data. With the exception of Panstrongylus diasi that does not present cytogenetic data available in the literature, all species were differentiated by cytogenetic characteristics. We emphasize the importance of using this key as a simple and objective tool in the entoepidemiological surveys conducted by the vector control programs.

Chagas disease, also known as American trypanosomiasis, is a potential life-threatening illness caused by the protozoan Trypanosoma cruzi (Chagas, 1909).1 It is estimated that 8 million people are infected worldwide, mostly in Latin America; more than 10,000 people die every year from clinical manifestations of Chagas disease; and more than 25 million people risk acquiring the disease.1

This neglected disease is distributed in 21 Latin American countries, where it is mostly vector-borne.1 The main vector involved in the transmission of the parasite to humans is a triatomine bug, also known as “kissing bug,” and vector control remains the most useful method to prevent infection.1

Presently, there are 153 species of triatomines24 and all species are considered as potential vectors of the etiologic agent of Chagas disease. In Brazil, there are 68 species distributed in all Brazilian states,58 grouped in the genera Panstrongylus (Berg, 1879), Rhodnius (Stål, 1859), Psammolestes (Bergroth, 1911), Triatoma (Laporte, 1832), Cavernicola (Usinger, 1944), Eratyrus (Stål, 1859), Microtriatoma (Prosen and Martínez, 1952), Alberprosenia (Martínez and Carcavallo, 1977), and Belminus (Stål, 1859). To date, the epidemiological surveys indicate that the state of São Paulo, the largest Brazilian urban center with more than 11 million people,9 presents 11 species of triatomines,5,10 being that most of the species have already been collected in a home environment and found to be infected with T. cruzi (Table 1).

Table 1

List of triatomine species present in the state of São Paulo with information on Trypanosoma cruzi infection and collection sites

SpeciesInfected by T. cruziHabitat
Panstrongylus diasi (Pinto and Lent, 1946)Peridomiciliary and intradomiciliary*
Panstrongylus geniculatus (Latreille, 1811)Yes†Peridomiciliary and intradomiciliary*†
Panstrongylus megistus (Burmeister, 1835)Yes†Peridomiciliary and intradomiciliary†
Psammolestes tertius (Lent and Jurberg, 1965)Wild*
Rhodnius domesticus (Neiva and Pinto, 1923)No‡Wild*
Rhodnius neglectus (Lent, 1954)Yes†Peridomiciliary and intradomiciliary†
Triatoma infestans (Klug, 1834)Yes§Peridomiciliary and intradomiciliary†§
Triatoma rubrofasciata (De Geer, 1773)Peridomiciliary and intradomiciliary*
Triatoma sordida (Stål, 1859)Yes*Peridomiciliary and intradomiciliary*
Triatoma tibiamaculata (Pinto, 1926)Yes‡Wild*
Triatoma wygodzinskyi (Lent, 1951)Yes*Peridomiciliary and intradomiciliary*

* Galvão.5

† Rodrigues et al.11

‡ Carvalho et al.12

§ Corrêa and Ferreira.10

In the past few years, several species of triatomines have been registered in the urban perimeter of the state of São Paulo13 and the main form of identification of these vectors occurred on the basis of morphological data.13,14 However, problems in correctly identifying species can lead to an incorrect panorama of distribution of Chagas disease vectors as it happened, for example, with Triatoma arthurneivai (Lent and Martins, 1940): for more than 40 years, it was believed that this species was present in the state of São Paulo, and Carbajal de la Fuente et al.15 demonstrated that the species that exists in São Paulo is Triatoma wygodzinsky (Lent, 1951) that was incorrectly identified as T. arthurneivai (endemic to the state of Minas Gerais).5

Cytogenetic tools are contributing to the taxonomy of triatomines; for example, Alevi et al.16 recently characterized the prophase cells of T. arthurneivai and T. wygodzinsky and differentiated the species easily, highlighting the applicability of the cytological analyzes in the correct identification of the species. Based on this information, we developed an identification key for the triatomines of the state of São Paulo, based on cytogenetic data.

Cytogenetic data available in the literature1723 were grouped and used for the construction of the identification key (which we call CytoKey). From the cytogenetic characteristics (karyotype, constitutive heterochromatin pattern in chromatin and chromosomes, formation of chromocenter, and localization of 45S rDNA probes), identification key was created for triatomines of the São Paulo state (with the exception of Panstrongylus diasi (Pinto and Lent, 1946) that does not present cytogenetic data available in the literature) (Table 2).

Table 2

Key for the triatomines of the São Paulo state based on cytogenetic data

Identification key (cytokey)
1. Karyotype with 2n = 21 chromosomes (18A + X1X2Y)Panstrongylus megistus
2. Karyotype with 2n = 25 chromosomes (22A + X1X2Y)Triatoma rubrofasciata
3. Karyotype with 2n = 23 chromosomes (20A + X1X2Y)4
4a. Prophase with heterochromatic blocks dispersed inside the nucleusTriatoma tibiamaculata
4b. Prophase without heterochromatin blocks dispersed inside the nucleusPanstrongylus geniculatus
5. Karyotype with 2n = 22 chromosomes (20A + XY)6
6a. Prophase with heterochromatin blocks dispersed inside the nucleus7
6b. Prophase without heterochromatic blocks dispersed inside the nucleus8
7a. Heterochromatin in 3–4 large pairs of autosomesTriatoma infestans
7b. Heterochromatin in all autosomesTriatoma sordida
8a. Chromocenter formed by three heterochromatic corpuscles9
8b. Chromocenter formed by only one heterochromatic corpuscle10
9a. Absence of heterochromatin in autosomesRhodnius neglectus
9b. Presence of heterochromatin in some autosomesRhodnius domesticus
10a. 45S rDNA probe located in autosomesTriatoma wygodzinskyi
10b. 45S rDNA probe located in X and Y chromosomesPsammolestes tertius

Thus, from the cytogenetic data, we developed, for the first time, a key identification for the species of the state of São Paulo and we emphasize the importance of using this key as a simple and objective tool in the entoepidemiological surveys conducted by the vector control programs.

Acknowledgments:

This work was financed by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (process number 2013/19764-0), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brazil (CAPES) (Finance Code 001).

REFERENCES

  • 1.

    World Health Organization, 2018. Chagas Disease (American trypanosomiasis). Available at: http://www.who.int/chagas/en/. Accessed August 14, 2018.

  • 2.

    Oliveira JD, Alevi KC, 2017. Taxonomic status of Panstrongylus herreri Wygodzinsky, 1948 and the number of Chagas disease vectors. Rev Soc Bras Med Trop 50: 434435.

    • Search Google Scholar
    • Export Citation
  • 3.

    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 Vector Ecol 43: 148157.

    • Search Google Scholar
    • Export Citation
  • 4.

    Dorn PL, Just SA, 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.

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

  • 6.

    Mendonça VJ, Alevi KCC, Pinotti H, Gurgel-Gonçalves R, Pita S, Guerra AL, Panzera F, Araújo RF, Azeredo-Oliveira MTC, Rosa JA, 2016. Revalidation of Triatoma bahiensis Sherlock & Serafim, 1967 (Hemiptera: Reduviidae) and phylogeny of the T. brasiliensis species complex. Zootaxa 4107: 239254.

    • Search Google Scholar
    • Export Citation
  • 7.

    Souza ES, Von Atzingen NCB, Furtado MB, Oliveira J, 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
  • 8.

    Rosa JA, Justino HHG, Nascimento JD, Mendonça VJ, Rocha CS, Carvalho DB, Falcone R, Azeredo-Oliveira MTV, Alevi KCC, Oliveira J, 2017. A new species of Rhodnius from Brazil (Hemiptera, Reduviidae, Triatominae). ZooKeys 675: 125.

    • Search Google Scholar
    • Export Citation
  • 9.

    Instituto Brasileiro de Geografia e Estatística, 2010. Available at: https://cidades.ibge.gov.br/brasil/sp/sao-paulo/panorama. Accessed August 14, 2018.

  • 10.

    Corrêa RR, Ferreira AO, 1959. Distribuição geográfica, habitats e infecção do Triatoma sordida no Estado de São Paulo, Rev Inst Med Trop São Paulo 1: 207213.

    • Search Google Scholar
    • Export Citation
  • 11.

    Rodrigues VLCC, Ferraz Filho AN, Silva EOR, Lima VLC, 1992. Prevalência, índices de infecção e hábitos alimentares de triatomíneos capturados em uma área de vigilância epidemiológica. Rev Soc Bras Med Trop 25: 183190.

    • Search Google Scholar
    • Export Citation
  • 12.

    Carvalho ME, Silva RA, Barata JM, Domingos MF, Ciaravolo RM, Zacharias F, 2003. Chagas’ disease in the southern coastal region of Brazil. Rev Saúde Públ 37: 4958.

    • Search Google Scholar
    • Export Citation
  • 13.

    Ceretti-Junior W, Vendramini DP, Matos-Junior MO, Ribeiro AR, Alvarez JV, Marques S, Duarte NA, Silva RA, Rosa JA, Marrelli MT, 2018. Occurrences of triatomines (Hemiptera: Reduviidae) and first reports of Panstrongylus geniculatus in urban environments in the city of São Paulo, Brazil. Rev Inst Med Trop São Paulo 60: e33.

    • Search Google Scholar
    • Export Citation
  • 14.

    Ribeiro AR, Oliveira RC, Ceretti-Junior W, Lima L, Almeida LA, Nascimento JD, Teixeira MM, Rosa JA, 2016. Trypanosoma cruzi isolated from a triatomine found in one of the biggest metropolitan areas of Latin America. Rev Soc Bras Med Trop 49: 183189.

    • Search Google Scholar
    • Export Citation
  • 15.

    Carbajal de la Fuente AL, Jaramillo N, Barata JMS, Noireau F, Diotaiuti L, 2011. Misidentification of two Brazilian triatomes, Triatoma arthurneivai and Triatoma wygodzinskyi, revealed by geometric morphometrics. Med Vet Entomol 25: 178183.

    • Search Google Scholar
    • Export Citation
  • 16.

    Alevi KCC, Imperador CHL, Moreira FFF, Jurberg J, Azeredo-Oliveira MTV, 2016. Differentiation between Triatoma arthurneivai and Triatoma wygodzinskyi (Hemiptera: Reduviidae: Triatominae) using cytotaxonomy. Gen Mol Res 15: 15.

    • Search Google Scholar
    • Export Citation
  • 17.

    Alevi KCC, Moreira FFF, Jurberg J, Azeredo-Oliveira MTV, 2016. Description of 161 the diploid chromosome set of Triatoma pintodiasi (Hemiptera, Triatominae). Gen Mol Res 25: 15.

    • Search Google Scholar
    • Export Citation
  • 18.

    Panzera F et al. 1998. Cytogenetics of triatomines. Carcavallo RU, ed. Atlas of Chagas Disease Vectors in the Americas. Rio de Janeiro, Brazil: Fiocruz, 621664.

    • Search Google Scholar
    • Export Citation
  • 19.

    Panzera F, Pérez R, Panzera Y, Ferrandis I, Ferreiro MJ, Calleros L, 2010. Cytogenetics and genome evolution in the subfamily Triatominae (Hemiptera, Reduviidae). Cytogenet Genome Res 128: 7787.

    • Search Google Scholar
    • Export Citation
  • 20.

    Panzera Y, Pita S, Ferreiro MJ, Ferrandis I, Lages C, Pérez R, Silva AE, Guerra M, Panzera F, 2012. High dynamics of rDNA cluster location in kissing bug holocentric chromosomes (Triatominae, Heteroptera). Cytogenet Genome Res 138: 5667.

    • Search Google Scholar
    • Export Citation
  • 21.

    Crossa RP et al. 2002. Chromosomal evolution trends of the genus Panstrongylus (Hemiptera, Reduviidae), vectors of Chagas disease. Infect Genet Evol 2: 4756.

    • Search Google Scholar
    • Export Citation
  • 22.

    Panzera F, Hornos S, Pereira J, Cestau R, Canale D, Diotaiuti L, Dujardin JP, Perez R, 1997. Genetic variability and geographic differentiation among three species of triatomine bugs (Hemiptera-Reduviidae). Am J Trop Med Hyg 57: 732739.

    • Search Google Scholar
    • Export Citation
  • 23.

    Alevi KCC, Rodas LAC, Tartarotti E, Azeredo-Oliveira MTV, Guirado MM, 2015. Entoepidemiology of Chagas disease in the western region of the state of São Paulo from 2004 to 2008, and cytogenetic analysis in Rhodnius neglectus (Hemiptera, Triatominae). Gen Mol Res 14: 57755784.

    • Search Google Scholar
    • Export Citation

Author Notes

Address correspondence to Kelly Cristine Borsatto, Laboratório de Biologia Celular, Instituto de Biociências, Letras e Ciências Exatas, Universidade Estadual Paulista “Júlio de Mesquita Filho” (IBILCE/UNESP), Rua Cristóvão Colombo 2265, São José do Rio Preto 15054-000, Brazil. E-mail: kellyborsatto@gmail.com

Authors’ addresses: Kelly Cristine Borsatto, Yago Visinho dos Reis, Ariane Cristina Caris Garcia, Maria Tercília Vilela de Azeredo-Oliveira, and Kaio Cesar Chaboli Alevi, Departamento de Biologia, Instituto de Biociências, Letras e Ciências Exatas, Universidade Estadual Paulista “Júlio de Mesquita Filho”, São José do Rio Preto, Brazil, E-mails: kellyborsatto@gmail.com, yagoreis@outlook.com.br, ariane.garcia@outlook.com, tercilia@ibilce.unesp.br, and kaiochaboli@hotmail.com. Paulo Sergio de Sousa, Departamento de Zoologia, Instituto de Biociências, Universidade Estadual Paulista “Júlio de Mesquita Filho”, Botucatu, Brazil, E-mail: pssousa@prof.educacao.sp.gov.br.

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