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Sometimes, the size matters: Wing geometric morphometrics as a tool to assess domiciliation by Triatoma sordida (Stäl 1859)

ABSTRACT

Background:

Domiciliation by Triatoma sordida is a public health concern in South America. This study aimed to evaluate the morphometric changes in the domestic and peridomestic populations of T. sordida.

Methods:

Specimen hemelytra were mounted, digitized, and processed for geometric morphometric analyses.

Results:

The specimens captured in houses were smaller than those captured in peridomiciles. A large size reduction effect was observed in female peridomicile populations compared with female house populations.

Conclusions:

T. sordida house populations were smaller than peridomestic populations. Wing geometric morphometry can be used as a tool to indicate T. sordida domiciliation.

Keywords:
Triatomines; Domiciliation; Morphometry

Chagas disease (CD) is a neglected tropical disease that is transmitted by blood-sucking bugs of the Triatominae subfamily, popularly known as kissing bugs. Owing to their ability to colonize houses, some triatomine species are closely associated with Trypanosoma cruzi transmission to humans and domestic animals11. Gurgel-Gonçalves R, Galvão C, Costa J, Peterson AT. Geographic distribution of Chagas disease vectors in Brazil based on ecological niche modeling. J Trop Med. 2012:705326. Available from: https://doi.org/10.1155/2012/705326
https://doi.org/10.1155/2012/705326...
. Understanding the determinants of triatomine invasion, infestation, and house colonization provides relevant information for CD surveillance22. Ribeiro-Jr G, Abad-Franch F, de Sousa OMF, Dos Santos CGS, Fonseca EOL, Dos Santos RF, et al. TriatoScore: an entomological-risk score for Chagas disease vector control-surveillance. Parasites & Vectors. 2021;14(1):492. Available from: https://doi.org/10.1186/s13071-021-04954-5
https://doi.org/10.1186/s13071-021-04954...
.

Triatoma sordida has a wide geographic distribution, is commonly found in wild environments infected with T. cruzi, and is the most frequent synanthropic triatomine species in Brazil, where it is strongly associated with chicken coops11. Gurgel-Gonçalves R, Galvão C, Costa J, Peterson AT. Geographic distribution of Chagas disease vectors in Brazil based on ecological niche modeling. J Trop Med. 2012:705326. Available from: https://doi.org/10.1155/2012/705326
https://doi.org/10.1155/2012/705326...
. Despite its low competence to transmit T. cruzi due to its ornithophilic habits, T. sordida specimens can disperse up to 32 m in peridomestic rural areas33. Dantas ES, Gurgel-Gonçalves R, Villela DAM, Monteiro FA, Maciel-deFreitas R. Should I stay or should I go? Movement of adult Triatoma sordida within the peridomestic area of a typical Brazilian Cerrado rural household. Parasit Vectors. 2018;11:14. Available from: https://doi.org/10.1186/s13071-017-2560-3
https://doi.org/10.1186/s13071-017-2560-...
,44. Dantas ES, Gurgel-Gonçalves R, Maciel-de-Freitas R, Monteiro FA. Simultaneous external and internal marking of Triatoma sordida nymphs: trace element efficacy and microgeographic dispersal in a peridomestic Brazilian Cerrado rural household. Parasites Vectors. 2022;15(1):325. Available from: https://doi.org/10.1186/s13071-022-05451-z
https://doi.org/10.1186/s13071-022-05451...
and reach houses, maintaining the risk of CD transmission55. Dias JP, Bastos C, Araújo E, Mascarenhas AV, Martins Netto E, Grassi F, et al. Acute Chagas disease outbreak associated with oral transmission. Rev Soc Bras Med Trop. 2008;41(3):296-300. Available from: https://doi.org/10.1590/S0037-86822008000300014
https://doi.org/10.1590/S0037-8682200800...
. Thus, mapping the areas of T. sordida house infestations is extremely relevant for guiding CD prevention strategies.

Variations in the size, shape, and color of triatomines have been described as adaptive responses to different microhabitats66. Abad-Franch F, Monteiro FA, Pavan MG, Patterson JS, Bargues MD, Zuriaga MÁ, et al. Under pressure: phenotypic divergence and convergence associated with microhabitat adaptations in Triatominae. Parasit Vectors. 2021;14(1):195. Available from: https://doi.org/10.1186/s13071-021-04647-z
https://doi.org/10.1186/s13071-021-04647...
. Other studies have described a decrease in body size and sexual dimorphism as relevant markers of triatomine domiciliation77. Dujardin JP, Panzera P, Schofield CJ. Triatominae as a model of morphological plasticity under ecological pressure. Mem Inst Oswaldo Cruz. 1999;94(1):223-8. Available from: https://doi.org/10.1590/S0074-02761999000700036
https://doi.org/10.1590/S0074-0276199900...

8. Garcia ACC, de Oliveira J, Cristal DC, Delgado LMG, Bittinelli IF, Galvão C, et al. Intraspecific and Interspecific Phenotypic Differences Confirm the Absence of Cryptic Speciation in Triatoma sordida (Hemiptera, Triatominae). Am J Trop Med Hyg. 2021;105(6):1759-66. Available from: https://doi.org/10.4269/ajtmh.21-0323
https://doi.org/10.4269/ajtmh.21-0323...
-99. Gurgel-Goncalves R, Ferreira JB, Rosa AF, Bar ME, Galvao C. Geometric morphometrics and ecological niche modeling for delimitation of near-sibling triatomine species. Med Vet Entomol. 2011;25(1):84-93. Available from: https://doi.org/10.1111/j.1365-2915.2010.00920.x
https://doi.org/10.1111/j.1365-2915.2010...
. This evidence suggests that peridomestic triatomine populations can be differentiated from domestic populations, with size differences indicating an old house infestation. Geometric morphometry is widely used for evaluating triatomine populations. This approach uses anatomical landmarks and image superposition methods to analyze variations in size and shape between individuals. This technique was previously applied to differentiate T. sordida from similar species99. Gurgel-Goncalves R, Ferreira JB, Rosa AF, Bar ME, Galvao C. Geometric morphometrics and ecological niche modeling for delimitation of near-sibling triatomine species. Med Vet Entomol. 2011;25(1):84-93. Available from: https://doi.org/10.1111/j.1365-2915.2010.00920.x
https://doi.org/10.1111/j.1365-2915.2010...

10. Nattero J, Piccinali RV, Macedo Lopes C, Hernández ML, Abrahan L, Lobbia PA, et al. Morphometric variability among the species of the Sordida subcomplex (Hemiptera: Reduviidae: Triatominae): evidence for differentiation across the distribution range of Triatoma sordida. Parasit Vectors. 2017;10(1):412. Available from: https://doi.org/10.1186/s13071-017-2350-y
https://doi.org/10.1186/s13071-017-2350-...
-1111. Belintani T, Oliveira J, Pinotti H, Silva LA, Alevi KCC, Galvão C, et al. Phylogenetic and phenotypic relationships of the Triatoma sordida subcomplex (Hemiptera: Reduviidae: Triatominae). Acta Trop. 2020;212:105679. Available from: https://doi.org/10.1016/j.actatropica.2020.105679
https://doi.org/10.1016/j.actatropica.20...
and to analyze the morphometric variation of T. sordida in Brazil1111. Belintani T, Oliveira J, Pinotti H, Silva LA, Alevi KCC, Galvão C, et al. Phylogenetic and phenotypic relationships of the Triatoma sordida subcomplex (Hemiptera: Reduviidae: Triatominae). Acta Trop. 2020;212:105679. Available from: https://doi.org/10.1016/j.actatropica.2020.105679
https://doi.org/10.1016/j.actatropica.20...
. As size changes are associated with house infestation, we aimed to evaluate the existence of morphometric modifications in domestic and peridomestic populations of T. sordida. We hypothesized that 1) the wing size of T. sordida populations captured inside houses is smaller than that of peridomestic populations and 2) sexual size dimorphism is smaller among domestic populations.

Triatomine samples were collected from January 2013 to December 2014 from six localities in the municipality of Barra, Bahia (Figure 1A), according to previously described methods1212. Ribeiro-Jr G, Dos Santos CGS, Lanza F, Reis J, Vaccarezza F, Diniz C, et al. Wide distribution of Trypanosoma cruzi-infected triatomines in the State of Bahia, Brazil. Parasit Vectors. 2019;12(1):604. Available from: https://doi.org/10.1186/s13071-019-3849-1
https://doi.org/10.1186/s13071-019-3849-...
. Triatomines were identified using dichotomous identification keys in a double-verification process. The insects were marked with numbers and QR codes using Zebra® TLP 2844 printer and Zebradesign® V.2 software. All samples were deposited in the entomological collection of Fiocruz Bahia. Triatomine wing samples (hemelytra) were selected for geometric morphometric analysis owing to the method’s feasibility and reproducibility. The hemelytra were placed between glass microscope slides, fixed with a double-sided tape, and scanned at a high resolution (900 dpi). The images were edited using PhotoScape software and organized according to sex and collection environment. We digitized seven anatomical points on each wing (Type I and II) using TpsDig® software99. Gurgel-Goncalves R, Ferreira JB, Rosa AF, Bar ME, Galvao C. Geometric morphometrics and ecological niche modeling for delimitation of near-sibling triatomine species. Med Vet Entomol. 2011;25(1):84-93. Available from: https://doi.org/10.1111/j.1365-2915.2010.00920.x
https://doi.org/10.1111/j.1365-2915.2010...
to determine the coordinates (x and y). The wing size was obtained using an estimator of size (centroid size) and calculated using the coordinates of each wing anatomical point using TPSrelw® software, which also performed wing coordinate alignment and shape variable determination.

FIGURE 1:
Study area. (A) Triatoma sordida spatial distribution in Bahia state, *showing the municipality of Barra. (B) Google Earth satellite imagery of household units where triatomines were captured. The yellow markers show the sampling locations of Triatoma sordida between 2013 and 2014; São Francisco River margin locations: Estrema, Quixaba, Barro Vermelho, Sambaíba, and Lagoa do Canto; −9 = non-informed location.

A factorial analysis of variance (ANOVA) was carried out to determine the effects of sex and habitat (intradomestic or peridomestic) on the size of T. sordida specimens. Shape variables derived from the TPSrelw partial deformations were used for the principal component analysis (PCA). A factorial map of the first two principal components was created to illustrate the main results. The results of ANOVA and PCA were calculated using Statistica® software (StatSoft, Inc., Tulsa, OK, USA).

We captured 410 T. sordida specimens in Barra City (Figure 1B), found in domiciles (53.9%, n=221) and peridomiciles (46.1%, n=189), among 10 localities and 33 colonies, with an average of 12 (standard deviation=7.6) triatomines per colony (Table 1). All peridomestic colonies were found in chicken coops, while domestic colonies were found in kitchens, bedrooms, and living rooms. The wing geometric morphometric analysis of 120 adults, 63 from peridomiciles and 57 from houses (Table 1), revealed that T. sordida females captured inside houses were much smaller than those captured in peridomiciles, while male specimens showed similar sizes between the environments. As expected, sexual dimorphism was observed, with female specimens being larger than male specimens in peridomiciles. However, we did not find any size differences between males and females from the houses. Therefore, the size decrease effect between habitats (ANOVA F1.116 = 5.86, p=0.017) was more pronounced for female specimens (Figure 2A) and that size sexual dimorphism was lower in domestic populations of T. sordida. The PCA did not reveal marked wing shape differences between the domestic and peridomestic populations (Figure 2B).

TABLE 1:
Information about the colonization of houses and peridomestic environments by T. sordida in the municipality of Barra, Bahia state, by assessed location.

FIGURE 2:
(A) Factorial analysis of variance of the centroid size of male and female specimens of Triatoma sordida according to the collecting habitat. (B) Principal component analysis of the Triatoma sordida specimens’ adult wing shape collected from the intra- and peridomestic environments in the municipality of Barra, Bahia state.

Triatomine specimens captured inside houses were smaller than those captured in the peridomestic areas. In addition, the size difference between sexes decreased, mainly due to the smaller size of T. sordida female specimens captured in houses. Geometric morphometric analyses were conducted to assess any intraspecific variations1010. Nattero J, Piccinali RV, Macedo Lopes C, Hernández ML, Abrahan L, Lobbia PA, et al. Morphometric variability among the species of the Sordida subcomplex (Hemiptera: Reduviidae: Triatominae): evidence for differentiation across the distribution range of Triatoma sordida. Parasit Vectors. 2017;10(1):412. Available from: https://doi.org/10.1186/s13071-017-2350-y
https://doi.org/10.1186/s13071-017-2350-...
and to determine whether local reinfestations originated from wild or synanthropic populations with residual foci1313. Dujardin JP, Bermudez H, Casini C, Schofield CJ, Tibayrenc M. Metric differences between sylvatic and domestic Triatoma infestans (Heteroptera: Reduviidae) in Bolivia. J Med Entomol. 1997;34(5):544-51. Available from: https://doi.org/10.1093/jmedent/34.5.544
https://doi.org/10.1093/jmedent/34.5.544...
.

As expected, smaller populations were found in houses, which agrees with the results found in other species, such as T. infestans. Furthermore, the population size differences between environments were more remarkable among female specimens, and sexual dimorphism was more pronounced in the peridomestic population. Dujardin et al.1313. Dujardin JP, Bermudez H, Casini C, Schofield CJ, Tibayrenc M. Metric differences between sylvatic and domestic Triatoma infestans (Heteroptera: Reduviidae) in Bolivia. J Med Entomol. 1997;34(5):544-51. Available from: https://doi.org/10.1093/jmedent/34.5.544
https://doi.org/10.1093/jmedent/34.5.544...
demonstrated similar results when the wild and laboratory populations of T. infestans and Rhodnius domesticus were compared. They noted that the changes occurring during the transition from natural to artificial environments influence the amount and quality of food for triatomines, which is related to size the differences between male and female specimens. Dujardin et al.1313. Dujardin JP, Bermudez H, Casini C, Schofield CJ, Tibayrenc M. Metric differences between sylvatic and domestic Triatoma infestans (Heteroptera: Reduviidae) in Bolivia. J Med Entomol. 1997;34(5):544-51. Available from: https://doi.org/10.1093/jmedent/34.5.544
https://doi.org/10.1093/jmedent/34.5.544...
recommended the use of size-based sexual dimorphism as an essential tool for examining triatomine adaptation in domestic environments. Our results support the use of sexual dimorphism analysis to determine the processes of adaptation to houses and confirm the hypothesis that T. sordida has adapted to colonize houses in Barra City, Bahia.

The process of house colonization by T. sordida can be affected by inadequate management of poultry, especially domestic chickens (Gallus gallus domesticus L.)1414. Rossi JC, Duarte EC, Gurgel-Gonçalves R. Factors associated with the occurrence of Triatoma sordida (Hemiptera: Reduviidae) in rural localities of Central-West Brazil. Mem Inst Oswaldo Cruz. 2015;110(2):192-200. Available from: https://pubmed.ncbi.nlm.nih.gov/25946242/
https://pubmed.ncbi.nlm.nih.gov/25946242...
. Additionally, a strong association between T. sordida and poultry has been well-documented, explaining its high incidence in peridomestic chicken coops1515. Diotaiuti L, Azeredo BV, Busek SC, Fernandes AJ. Controle do Triatoma sordida no peridomicílio rural do município de Porteirinha, Minas Gerais, Brasil. Rev Panam Salud Publica. 1998; 3(1):21-5. Available from: https://pubmed.ncbi.nlm.nih.gov/9503959/
https://pubmed.ncbi.nlm.nih.gov/9503959/...
. The house colonization of T. sordida can be attributed to its ability to move around the peridomestic environment33. Dantas ES, Gurgel-Gonçalves R, Villela DAM, Monteiro FA, Maciel-deFreitas R. Should I stay or should I go? Movement of adult Triatoma sordida within the peridomestic area of a typical Brazilian Cerrado rural household. Parasit Vectors. 2018;11:14. Available from: https://doi.org/10.1186/s13071-017-2560-3
https://doi.org/10.1186/s13071-017-2560-...
,44. Dantas ES, Gurgel-Gonçalves R, Maciel-de-Freitas R, Monteiro FA. Simultaneous external and internal marking of Triatoma sordida nymphs: trace element efficacy and microgeographic dispersal in a peridomestic Brazilian Cerrado rural household. Parasites Vectors. 2022;15(1):325. Available from: https://doi.org/10.1186/s13071-022-05451-z
https://doi.org/10.1186/s13071-022-05451...
and is facilitated by the local human behavior of raising birds and keeping bird nests inside household units, especially for laying eggs. Thus, T. sordida specimens could enter household units either passively (as small nymphs) or actively (as nymphs and adult triatomines walking and being actively attracted by poultry) enter household unit44. Dantas ES, Gurgel-Gonçalves R, Maciel-de-Freitas R, Monteiro FA. Simultaneous external and internal marking of Triatoma sordida nymphs: trace element efficacy and microgeographic dispersal in a peridomestic Brazilian Cerrado rural household. Parasites Vectors. 2022;15(1):325. Available from: https://doi.org/10.1186/s13071-022-05451-z
https://doi.org/10.1186/s13071-022-05451...
.

The colonization of artificial anthropic environments by T. sordida has been documented, demonstrating a progressive adaptation of the species across the national territory, including the Bahia state1212. Ribeiro-Jr G, Dos Santos CGS, Lanza F, Reis J, Vaccarezza F, Diniz C, et al. Wide distribution of Trypanosoma cruzi-infected triatomines in the State of Bahia, Brazil. Parasit Vectors. 2019;12(1):604. Available from: https://doi.org/10.1186/s13071-019-3849-1
https://doi.org/10.1186/s13071-019-3849-...
. Between January 2013 and December 2014, 5,906 triatomines of 15 species were captured from 127 municipalities across all regions of Bahia. Approximately 3,500 specimens (60%) were T. sordida species, infesting 70 (55%) of the sampled municipalities1212. Ribeiro-Jr G, Dos Santos CGS, Lanza F, Reis J, Vaccarezza F, Diniz C, et al. Wide distribution of Trypanosoma cruzi-infected triatomines in the State of Bahia, Brazil. Parasit Vectors. 2019;12(1):604. Available from: https://doi.org/10.1186/s13071-019-3849-1
https://doi.org/10.1186/s13071-019-3849-...
. Therefore, it is important to investigate the factors influencing T. sordida domiciliation. The use of geometric morphometry as a surveillance tool to access domiciliation is feasible, low cost, and reproducible. This tool offers benefits such as the possibility of comparing information among different areas, strengthening the entomological surveillance system.

In addition to geometric morphometrics, genetic analyses can be used to study triatomine domiciliation. Monteiro et al.1616. Monteiro FA, Jurberg J, Lazoski C. Very low levels of genetic variation in natural peridomestic populations of the Chagas disease vector Triatoma sordida (Hemiptera: Reduviidae) in Southeastern Brazil. Am J Trop Med Hyg. 2009;81(2):223-7. Available from: https://www.arca.fiocruz.br/handle/icict/30844
https://www.arca.fiocruz.br/handle/icict...
compared the genetic structure of intradomestic and peridomestic T. sordida populations in Brazil and found low genetic variation among the peridomestic populations. The relevance of these studies is based on the current evidence for domiciliation described in our study.

New tools may strengthen surveillance of vector-borne CD. Two interesting perspectives for further characterization of domestic and peridomestic T. sordida populations in this area would be (1) to characterize the populations using microsatellites and (2) to analyze the head morphometry of nymphs found inside and outside houses. We also recommend further research in other areas of Bahia with a history of domestic (intra- and peridomestic) colonization by T. sordida to confirm the process of domestic colonization by this species, thus reinforcing its role as a potential T. cruzi vector. Finally, our results suggest the use of wing geometric morphometry as a tool to indicate T. sordida domiciliation; hence, we believe that the use of this tool could improve vector-borne CD surveillance.

● Ethics

The procedures were performed in accordance with the ethical standards of the Research Ethics Committee of the Gonçalo Moniz Institute (IGM; FIOCRUZ, Bahia, Brazil). The requirement for obtaining informed consent was waived as the analysis was performed using the Bahia Entomological Surveillance System samples. However, no personal identification data were used to ensure complete anonymity of the participants. The research did not cause any physical, psychological, moral, intellectual, social, cultural, or religious risks to the residents or animals in the study area. Additionally, this study did not include endangered or protected species.

ACKNOWLEDGMENTS

We are grateful to the Epidemiology Surveillance team of the Health Secretary of the State of Bahia (SESAB-DIVEP) for the databases and support with the triatomines and vector information.

REFERENCES

  • 1
    Gurgel-Gonçalves R, Galvão C, Costa J, Peterson AT. Geographic distribution of Chagas disease vectors in Brazil based on ecological niche modeling. J Trop Med. 2012:705326. Available from: https://doi.org/10.1155/2012/705326
    » https://doi.org/10.1155/2012/705326
  • 2
    Ribeiro-Jr G, Abad-Franch F, de Sousa OMF, Dos Santos CGS, Fonseca EOL, Dos Santos RF, et al. TriatoScore: an entomological-risk score for Chagas disease vector control-surveillance. Parasites & Vectors. 2021;14(1):492. Available from: https://doi.org/10.1186/s13071-021-04954-5
    » https://doi.org/10.1186/s13071-021-04954-5
  • 3
    Dantas ES, Gurgel-Gonçalves R, Villela DAM, Monteiro FA, Maciel-deFreitas R. Should I stay or should I go? Movement of adult Triatoma sordida within the peridomestic area of a typical Brazilian Cerrado rural household. Parasit Vectors. 2018;11:14. Available from: https://doi.org/10.1186/s13071-017-2560-3
    » https://doi.org/10.1186/s13071-017-2560-3
  • 4
    Dantas ES, Gurgel-Gonçalves R, Maciel-de-Freitas R, Monteiro FA. Simultaneous external and internal marking of Triatoma sordida nymphs: trace element efficacy and microgeographic dispersal in a peridomestic Brazilian Cerrado rural household. Parasites Vectors. 2022;15(1):325. Available from: https://doi.org/10.1186/s13071-022-05451-z
    » https://doi.org/10.1186/s13071-022-05451-z
  • 5
    Dias JP, Bastos C, Araújo E, Mascarenhas AV, Martins Netto E, Grassi F, et al. Acute Chagas disease outbreak associated with oral transmission. Rev Soc Bras Med Trop. 2008;41(3):296-300. Available from: https://doi.org/10.1590/S0037-86822008000300014
    » https://doi.org/10.1590/S0037-86822008000300014
  • 6
    Abad-Franch F, Monteiro FA, Pavan MG, Patterson JS, Bargues MD, Zuriaga MÁ, et al. Under pressure: phenotypic divergence and convergence associated with microhabitat adaptations in Triatominae. Parasit Vectors. 2021;14(1):195. Available from: https://doi.org/10.1186/s13071-021-04647-z
    » https://doi.org/10.1186/s13071-021-04647-z
  • 7
    Dujardin JP, Panzera P, Schofield CJ. Triatominae as a model of morphological plasticity under ecological pressure. Mem Inst Oswaldo Cruz. 1999;94(1):223-8. Available from: https://doi.org/10.1590/S0074-02761999000700036
    » https://doi.org/10.1590/S0074-02761999000700036
  • 8
    Garcia ACC, de Oliveira J, Cristal DC, Delgado LMG, Bittinelli IF, Galvão C, et al. Intraspecific and Interspecific Phenotypic Differences Confirm the Absence of Cryptic Speciation in Triatoma sordida (Hemiptera, Triatominae). Am J Trop Med Hyg. 2021;105(6):1759-66. Available from: https://doi.org/10.4269/ajtmh.21-0323
    » https://doi.org/10.4269/ajtmh.21-0323
  • 9
    Gurgel-Goncalves R, Ferreira JB, Rosa AF, Bar ME, Galvao C. Geometric morphometrics and ecological niche modeling for delimitation of near-sibling triatomine species. Med Vet Entomol. 2011;25(1):84-93. Available from: https://doi.org/10.1111/j.1365-2915.2010.00920.x
    » https://doi.org/10.1111/j.1365-2915.2010.00920.x
  • 10
    Nattero J, Piccinali RV, Macedo Lopes C, Hernández ML, Abrahan L, Lobbia PA, et al. Morphometric variability among the species of the Sordida subcomplex (Hemiptera: Reduviidae: Triatominae): evidence for differentiation across the distribution range of Triatoma sordida Parasit Vectors. 2017;10(1):412. Available from: https://doi.org/10.1186/s13071-017-2350-y
    » https://doi.org/10.1186/s13071-017-2350-y
  • 11
    Belintani T, Oliveira J, Pinotti H, Silva LA, Alevi KCC, Galvão C, et al. Phylogenetic and phenotypic relationships of the Triatoma sordida subcomplex (Hemiptera: Reduviidae: Triatominae). Acta Trop. 2020;212:105679. Available from: https://doi.org/10.1016/j.actatropica.2020.105679
    » https://doi.org/10.1016/j.actatropica.2020.105679
  • 12
    Ribeiro-Jr G, Dos Santos CGS, Lanza F, Reis J, Vaccarezza F, Diniz C, et al. Wide distribution of Trypanosoma cruzi-infected triatomines in the State of Bahia, Brazil. Parasit Vectors. 2019;12(1):604. Available from: https://doi.org/10.1186/s13071-019-3849-1
    » https://doi.org/10.1186/s13071-019-3849-1
  • 13
    Dujardin JP, Bermudez H, Casini C, Schofield CJ, Tibayrenc M. Metric differences between sylvatic and domestic Triatoma infestans (Heteroptera: Reduviidae) in Bolivia. J Med Entomol. 1997;34(5):544-51. Available from: https://doi.org/10.1093/jmedent/34.5.544
    » https://doi.org/10.1093/jmedent/34.5.544
  • 14
    Rossi JC, Duarte EC, Gurgel-Gonçalves R. Factors associated with the occurrence of Triatoma sordida (Hemiptera: Reduviidae) in rural localities of Central-West Brazil. Mem Inst Oswaldo Cruz. 2015;110(2):192-200. Available from: https://pubmed.ncbi.nlm.nih.gov/25946242/
    » https://pubmed.ncbi.nlm.nih.gov/25946242/
  • 15
    Diotaiuti L, Azeredo BV, Busek SC, Fernandes AJ. Controle do Triatoma sordida no peridomicílio rural do município de Porteirinha, Minas Gerais, Brasil. Rev Panam Salud Publica. 1998; 3(1):21-5. Available from: https://pubmed.ncbi.nlm.nih.gov/9503959/
    » https://pubmed.ncbi.nlm.nih.gov/9503959/
  • 16
    Monteiro FA, Jurberg J, Lazoski C. Very low levels of genetic variation in natural peridomestic populations of the Chagas disease vector Triatoma sordida (Hemiptera: Reduviidae) in Southeastern Brazil. Am J Trop Med Hyg. 2009;81(2):223-7. Available from: https://www.arca.fiocruz.br/handle/icict/30844
    » https://www.arca.fiocruz.br/handle/icict/30844
  • Financial Support:

    This work was supported by the FAPESB Edital 014 2013 (PET0023/2013) & PROEP/CPqGM, process number 400904/2013-6.

Publication Dates

  • Publication in this collection
    09 Aug 2024
  • Date of issue
    2024

History

  • Received
    01 Nov 2023
  • Accepted
    26 June 2024
Sociedade Brasileira de Medicina Tropical - SBMT Sociedade Brasileira de Medicina Tropical - SBMT, Núcleo de Medicina Tropical – UnB, Sala 43C – 70904-970, E-mails: rsbmt@uftm.edu.br | artes.rsbmt@gmail.com | sbmt@sbmt.org.br , WhatsApp: SBMT (61) 9.9192-6496, WhatsApp: RSBMT (34) 9.9996-5807 - Brasília - DF - Brazil
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