Acessibilidade / Reportar erro

Monitoring Rhodnius neglectus (Lent, 1954) populations’ susceptibility to insecticide used in controlling actions in urban areas northwest of São Paulo state

ABSTRACT

Background:

Chagas disease (CD) is caused by the flagellate protozoan Trypanosoma cruzi and can be carried by different species of triatomines, including Rhodnius neglectus, which is wild, well distributed in Brazil, and has formed colonies in palm trees located in urban areas of municipalities in the state of São Paulo. Chemical control has been routinely used to reduce population density, but each year, there has been an increase in species dispersion and density. This study aimed to evaluate the susceptibility of insects to insecticides used in control.

Methods:

The reference population was collected from Araçatuba municipality, Nilce Maia. Dilutions of deltamethrin were prepared and applied to the back of the first-stage nymphs, which were biologically synchronized. The control group received pure acetone only. Mortality was assessed after 72 h.

Results:

The mortality rate with respect to diagnostic dose was 100%. The susceptibility profile observed for this population showed RR50 ranging from 1.76 to 3.632.

Conclusions:

The populations were susceptible to the insecticides tested. It is possible that the insecticide residual effect on this ecotope has decreased the lifespan, and controlling failures may be the cause of recolonization in this environment.

Keywords:
Insecticide resistance; Rhodnius neglectus; Deltamethrin; Chagas disease; Triatominae control

INTRODUCTION

Chagas disease (CD) is caused by Trypanosoma cruzi, a flagellate protozoan. The infection occurs by contact with contaminated excrement of this triatomine vector, a hematophagous insect, in all of its developmental phases. Infection may also occur by intake of contaminated food, vertical transmission, blood transfusion, and organ transplant11. Jurberg J, Rodrigues JMS, Moreira FFF, Dale C, Cordeiro IRS, Lamas-Jr VD, et al. Atlas iconográfico dos triatomíneos do Brasil (vetores da doença de Chagas). Rio de Janeiro: Instituto Osvaldo Cruz; 2014.

CD is endemic to 21 Latin American countries and affects approximately 6-7 million people worldwide22. World Health Organization [internet]. Chagas disease (American trypanosomiasis). Disponível em: Disponível em: https://www.who.int/health-topics/chagas-disease#tab=tab_1 . 2021 [acesso em 01 fev 2021].
https://www.who.int/health-topics/chagas...
. Recently, efforts have been made to reduce the occurrence of this infection in Latin America, but high migration rates of individuals from this region to other places have enabled DCs to spread to non-endemic countries, thereby making CD a global health issue33. Basile L, Jansá JM, Carlier Y, Salamanca DD, Angheben A, Bartoloni A, et al. Chagas disease in European countries: the challenge of a surveillance system. Euro Surveill. 2011;16(37):19968..

São Paulo state was the pioneer in controlling the main vector species, Triatoma infestans, and the measures adopted have become a model for other states in Brazil and South American countries44. Souza AG, Wanderley DMV, Buralli GM, Andrade JCR. Consolidation of the control of Chagas disease in State of São Paulo. Mem Inst Oswaldo Cruz. 1984;79:125-32.,55. Rocha e Silva EO, Rodrigues VLCC, Silva RA, Wanderley DMV. Programa de Controle da Doença de Chagas no estado de São Paulo, Brasil: o controle e a vigilância da transmissão vetorial. Rev Soc Bras Med Trop. 2011;44(Suppl 2):74-84.. Because of successful control measures in the domiciliary environment of T. infestans, entomological surveillance has focused on controlling native species that are usually found in the peridomiciliary environment66. Silva RA. Estado atual da vigilância entomológica da doença de Chagas no estado de São Paulo. Brazilian Journal of Health Review. 2019;2(2):742-55..

A total of 18 genera and 154 species of triatomine are known77. Oliveira J, Alevi KCC, Almeida CE, Mendonça VJ, Costa J, Rosa JA. Triatoma brasiliensis species complex: characterization of the external female genitalia. J Vector Ecol. 2020;45(1):57-68.. In Brazil, 64 species have been registered, 13 of these in São Paulo state, including Rhodnius neglectus (Lent 1954), which is mainly found in Ribeirão Preto, São José do Rio Preto, and Araçatuba. R. neglectus is a wild species, and its natural ecotope consists of palm trees, where it finds shelter and food. However, recent studies have reported that this species is also found in urban areas, domiciles, and peridomiciles88. Diotaiuti L, Dias JCP. Ocorrência e biologia de Rhodnius neglectus, Lent, 1954 em macaubeiras da periferia de Belo Horizonte, Minas Gerais. Mem Inst Oswaldo Cruz . 1984;79(3):293-301.,99. Rodrigues VLCC, Pauliquévis-Jr C, Silva RA, Wanderley DMV, Guirardo MM, Rodas LAC, et al. Colonization of palm trees by Rhodnius neglectus and household and invasion in an urban area, Araçatuba, São Paulo, Brazil. Rev Inst Med Trop São Paulo. 2014;56(3):213-8..

Palm trees belonging to the genus Acrocomia infested by R. neglectus feeding on Pionnus maximiliani, which make their nests in these palm trees, were detected in urban areas in Araçatuba, Birigui, Guararapes, and Piacatu municipalities, located in the northwest of São Paulo state99. Rodrigues VLCC, Pauliquévis-Jr C, Silva RA, Wanderley DMV, Guirardo MM, Rodas LAC, et al. Colonization of palm trees by Rhodnius neglectus and household and invasion in an urban area, Araçatuba, São Paulo, Brazil. Rev Inst Med Trop São Paulo. 2014;56(3):213-8.. Palm trees are used in landscaping design of urban areas in many cities of the state because they present low maintenance costs and are visually pleasant in the environment. The cities analyzed have a significant quantity of palm trees in their public squares and streets, thereby generating a favorable environment for these triatomines.

Controlling actions employed for palm trees located in urban areas consist of removing leaves and dry bunches, as well as chemical control by applying pyrethroid insecticide99. Rodrigues VLCC, Pauliquévis-Jr C, Silva RA, Wanderley DMV, Guirardo MM, Rodas LAC, et al. Colonization of palm trees by Rhodnius neglectus and household and invasion in an urban area, Araçatuba, São Paulo, Brazil. Rev Inst Med Trop São Paulo. 2014;56(3):213-8.. Despite this, every year, there is an increase in the dispersion and infestation of palm trees1010. Silva RA. Relatório de avaliação do Rhodnius neglectus em área urbana de municípios da região de Araçatuba. São Paulo: Superintêndencia de Controle de Endemias; 2018.. In cases of re-infestation after pyrethroid insecticide application, recolonization may occur due to insects that survived the spraying process, operational failures when applying the insecticide, or insect resistance to the product1111. Pessoa GCD, Vinãs PA, Rosa ACL, Diotaiuti L. History of insecticide resistance of triatominae vectors. Rev Soc Bras Med Trop 2015; 48(4):380-389..

Susceptibility to insecticide resistance has already been studied for different species, but not for R. neglectus. Due to infestation persistence observed in these municipalities, where chemical control has been systemically employed for over 15 years, it is necessary to assess insect susceptibility to the insecticide used in controlling measures aiming to verify its efficacy, therefore guiding actions carried out by the teams involved in such actions.

METHODS

Triatomines for Assessment

Samples were obtained from Araçatuba, Birigui, Guararapes, and Piacatu municipalities, all of which belong to the Araçatuba administrative region, located northwest of São Paulo state (Table 1). The insects were collected from the urban areas of these municipalities from palm trees that were regularly treated with pyrethroid insecticides provided by the Brazilian Ministry of Health under systematic applications1212. Ministério da Saúde Brasil [internet]. NT-36.2012 - Orientações sobre vigilância entomológica e a utilização de inseticida de ação residual no controle de triatomíneos - vetores da doença de Chagas. Brasília; 2012 [acesso em 6 set 2020]..

TABLE 1:
Triatomine populations assessed in insecticide susceptibility test, by municipality and location. Araçatuba region, 2020.

The insects were manually collected during the investigation procedure in the palm trees by municipal teams, kept in pots for transportation, and sent to the laboratory, where they were identified using a dichotomous key for triatomine species and classified according to their evolutionary phase1313. Lent H, Wygodzinsky PW. Revision of the Triatominae (Hemiptera, Reduviidae), and their significance as vectors of Chagas disease. Bull Am Mus Nat Hist. 1979;163(1):123-520..

At the laboratory, they were kept in a breeding room with a constant temperature of 25 °C +3, an air relative humidity of approximately 75% +3, and a photoperiod of 12 h. The insects remained in crystallizers measuring 10 cm (height) x 23.5 cm (diameter), lined with filtering paper to absorb excrement and humidity, with a hive-shaped 2 mm thick pressed cardboard sheet support and covered with thick dark cotton to protect them from light. The insects were fed through an artificial method with the rustic chicken, Rhodia sp., on a weekly basis.

Reference Population

A reference population of R. neglectus was selected, in which laboratory breeding started on 12/01/2004 and the insects were from Araçatuba municipality, Nilce Maia location. Specifically, it was necessary to identify the relevant diagnostic dose under which mortality of 50% of the population was observed (LD50). The criteria for selecting the reference population followed the World Health Organization guidelines1414. Organizacion Panamericana de la Salud (PAHO). II Reunion técnica latino-americana de monitoreo de resistência a inseticidas em triatominos vectores de Chagas, OPS. Panamá: PAHO; 2005..

Tests were performed to identify the LD50 and LD99 in this population. After reading the nymph death for the eight dilution rates used, the numbers obtained were organized in a reading database for the Polo Plus® software. RR50 and RR99 were obtained by dividing the LD50 of the field population by the LD50 of the susceptible population, with correspondence to calculate the RR99. A confidence interval of 95% (CI 95%) of each population was also calculated for each population.

Insecticide Susceptibility Test

The methodology used to monitor insect resistance in the laboratory was standardized by Pessoa (2016)1515. Pessoa GCD, Silva RA, Alves RV, Costa VM, Cavalcante KRLJ, Diotaiuti L. Fortalecimento da vigilância em saúde no Brasil: Rede de Monitoramento da resistência dos triatomíneos aos inseticidas. Rev Patol Trop 2016; 45(4):417-424. and defines insect generation, nymph age, insecticide application locus, and the ideal diagnostic dose for each species. The insects collected were kept in a quarantine after arriving at the laboratory and, at the end of this period, eggs were removed and the first stage nymphs’ birth was synchronized in order to perform the experiment.

The pyrethroid deltamethrin (99.1% purity) was supplied by Bayer. A total volume of 0.1 uL was applied on the back of the nymph on the fifth day after birth. The control groups received only pure acetone on their backs. Readings were performed 72 h after application, considering the normal, intoxicated, and dead nymphs. For each dilution, 30 insects were used at the first stage, with at least eight doses necessary to determine the mortality curve. Three groups were formed, with 10 insects in each group, and the tests were carried out on different days.

Mortality data were analyzed using the Basic Probit Analysis program to estimate the slope and lethal dose (LD) in nanograms of active ingredients per treated nymph. The susceptibility classification was in accordance with the Pan American Health Organization1414. Organizacion Panamericana de la Salud (PAHO). II Reunion técnica latino-americana de monitoreo de resistência a inseticidas em triatominos vectores de Chagas, OPS. Panamá: PAHO; 2005.. After defining the R. neglectus susceptibility baseline for the reference population, 30 nymphs from each field population were subjected to a diagnostic dose of 1xLD99. The survival of at least two insects in three repetitions was interpreted as a resistance indicator.

RESULTS

The susceptibility to deltamethrin in the reference population was 0.025 ng/treated nymphs at LD50. At this diagnostic dose, 100% mortality was observed in all populations. Regarding R. neglectus samples from field populations, variations between 0.0440 and 0.0908 ng/treated nymphs were observed (Table 2). Populations from Birigui (James Mellor and Pedro de Toledo) and Guararapes (Praça Mohamed and Princesa Isabel) presented lower slopes than the reference population, indicating less homogeneous populations with a higher resistance selection likelihood.

TABLE 2:
Result of mortality of first stage triatomine nymphs of Rhodnius neglectus after topical application of deltamethrin in a reference population and in samples from different locations. Araçatuba region, 2020.

Values obtained for RR50 in the field populations were significantly different from those in the reference population, and there was no superposition of confidence interval limits at 95%.

DISCUSSION

Insecticide resistance can be understood as a decrease in mortality observed in a population that has undergone constant exposure to chemical products used for extermination1111. Pessoa GCD, Vinãs PA, Rosa ACL, Diotaiuti L. History of insecticide resistance of triatominae vectors. Rev Soc Bras Med Trop 2015; 48(4):380-389.. In the case of triatomines, such resistance is regarded as rare and unlikely, mainly because of the life cycle of these insects, which hinders the selection of resistant individuals1111. Pessoa GCD, Vinãs PA, Rosa ACL, Diotaiuti L. History of insecticide resistance of triatominae vectors. Rev Soc Bras Med Trop 2015; 48(4):380-389.. However, previous studies have demonstrated cases of triatomine populations resistant to numerous active substances in different regions of America1616. Yon C, Balta R, García N, Troyes M, Cumpa H, Valdivia A. Susceptibilidad y resistencia de Triatoma infestans y Panstrongylus herreri a los insecticidas piretroides, Perú 2001. Revista Peruana de Medicina Experimental y Salud Pública. 2004; 21(3):179-182.

17. Santos MAT, Areas MA, Reyes FG. Piretróides - uma visão geral. Alimentos e Nutrição Araraquara 2007; 18(3):339-349.
-1818. Pessoa GCD, Rosa AC, Bedin C, Wilhelms T, Mello F, Coutinho HS, et al. Susceptibility characterization of residual Brazilian populations of Triatoma infestans Klug, 1834 (Hemiptera: Reduviidae) to deltamethrin pyrethroid. Rev Soc Bras Med Trop 2015; 48:157-161..

Triatomine resistance to pyrethroids associated with ineffective field treatment has been reported in R. prolixus in Venezuela and in Triatoma infestans in Brazil, Argentina, and Bolivia1919. Depickère S, Buitrago R, Siñani E, Baune M, Monje M, Lopez R, et al. Susceptibility and resistance to deltamethrin of wild and domestic populations of Triatoma infestans (Reduviidae: Triatominae) in Bolivia: new discoveries. Mem Inst Oswaldo Cruz 2012; 107:1042-47.. After these findings, studies aimed at verifying susceptibility in Brazilian populations of Triatoma infestans, T. sordida, and T. brasiliensis were carried out and have found, in some situations, resistance to the deltamethrin pyrethroid insecticide1818. Pessoa GCD, Rosa AC, Bedin C, Wilhelms T, Mello F, Coutinho HS, et al. Susceptibility characterization of residual Brazilian populations of Triatoma infestans Klug, 1834 (Hemiptera: Reduviidae) to deltamethrin pyrethroid. Rev Soc Bras Med Trop 2015; 48:157-161.,2020. Obara MT, Otrera VCG, Gonçalves RG, Santos JP, Santalucia M, Rosa JA, et al. Monitoramento da suscetibilidade de populações de Triatoma sordida Stal, 1859 (Hemiptera: Reduviidae) ao inseticida deltametrina, na região centro-oeste do Brasil. Rev Soc Bras Med Trop 2011; 44(2):206-212.

21. Pessoa GCD, Dias LS, Diotaiuti L. Deltamethrin pyrethroid susceptibility characterization of Triatoma sordida Stal, 1859 (Hemiptera: Reduviidae) populations in the northern region of Minas Gerais, Brazil. Rev Soc Bras Med Trop 2014; 47(4):426-429.

22. Pessoa GCD, Trevizani NAB, Dias LS, Bezerra CM, Melo BV, Diotaiuti L. Toxicological profile of deltamethrin in Triatoma brasiliensis (Hemiptera: Reduviidae) in state of Ceará, northeastern Brazil. Rev Soc Bras Med Trop 2015; 48(1):39-43.

23. Pessoa GCD, Santos TRM, Salazra GC, Dias LS, Mello BV, Ferraz ML, et al. Variability of susceptibility to deltamethrin in peridomestic Triatoma sordida from Triângulo Mineiro, state of Minas Gerais, Brazil. Rev Soc Bras Med Trop 2015; 48(4):417-421.
-2424. Pessoa GCD, Rosa ACL, Cavalari L, Rezende JG, Mello BV, Diotaiuti L. Susceptibility of Triatoma sordida Stal, 1859 (Hemiptera: Reduviidae) to alpha-cypermethrin under natural climatic conditions. Rev Soc Bras Med Trop 2015; 48(4):422-426..

The first report of pyrethroid insecticide resistance in triatomines of the genus Rhodnius was observed in populations of R. prolixus species in Venezuela using dieldrin2525. Vassena C, Picollo M, Zerba E. Insecticide resistance in Brazilian Triatoma infestans and Venezuelan Rhodnius prolixus. Med Vet Entomol 2000; 14(1):51-5.. There are no reports of studies conducted in Brazil to verify insecticide resistance susceptibility in populations of Rhodnius genus, which may be due to the fact that most species from these genus do not inhabit homes, therefore posing secondary risk to human beings.

In São Paulo state, R. neglectus is the second most collected species and, currently, most samples are from urban areas where there is a superposition of controlling actions aimed at arboviruses and visceral leishmaniasis2626. Camargo-Neves VLFD, Katz G, Rodas LAC, Poletto DW, Lage LC, Spínola RMF, et al. Utilização de ferramentas de análise espacial na vigilância epidemiológica de leishmaniose visceral americana-Araçatuba, São Paulo, Brasil, 1998-1999. Cad Saúde Pública 2001; 17:1263-67.. To chemically control vectors, the Brazilian Ministry of Health provides states and municipalities with alpha-cypermethrin, a pyrethroid insecticide, as this insecticide has a low residual effect, does not remain on treated surfaces for long periods, and is subjected to weather changes, which may impair its useful life1717. Santos MAT, Areas MA, Reyes FG. Piretróides - uma visão geral. Alimentos e Nutrição Araraquara 2007; 18(3):339-349.. This insecticide is also widely used because of its low toxicity in mammals and because it does not persist in the environment2727. Narahashi T. Neuronal ion channel as the target sites of insecticides. Pharmacol Toxicol 1996; 79(1):1-14..

Chemical control employed frequently to decrease infestation of this species in urban areas has not presented satisfactory results, which may lead to metabolic changes in the insects, resulting in resistance to the insecticides applied to control them. However, results from bioassays for this triatomine species did not indicate resistance; yet, there is evidence concerning the need for management strategies to maintain the insecticide lifespan, but it is necessary to continuously test insect resistance in these insect populations.

Values obtained for RR50 in this assessment, and considering that values higher or equal to 5 are parameters to characterize insect resistance to the insecticide, indicated that controlling actions may proceed with the same insecticide; however, new management methodologies must be considered for the palm trees. Mechanical control of this vector species in this ecotope must also be prioritized, since it is a fact that this insect currently inhabits an urban area in São Paulo state and its widening distribution will bring new challenges.

Pessoa et al. (2016)1515. Pessoa GCD, Silva RA, Alves RV, Costa VM, Cavalcante KRLJ, Diotaiuti L. Fortalecimento da vigilância em saúde no Brasil: Rede de Monitoramento da resistência dos triatomíneos aos inseticidas. Rev Patol Trop 2016; 45(4):417-424. defined a reference population for R. neglectus in which the LD50 value was 0.001 ng i. a/ninfa. If this value is considered, all populations tested in this assessment would be classified as resistant, indicating that it may be necessary to locally standardize the species under study. Obara et al. (2011)2020. Obara MT, Otrera VCG, Gonçalves RG, Santos JP, Santalucia M, Rosa JA, et al. Monitoramento da suscetibilidade de populações de Triatoma sordida Stal, 1859 (Hemiptera: Reduviidae) ao inseticida deltametrina, na região centro-oeste do Brasil. Rev Soc Bras Med Trop 2011; 44(2):206-212. and Pessoa et al. (2014)2121. Pessoa GCD, Dias LS, Diotaiuti L. Deltamethrin pyrethroid susceptibility characterization of Triatoma sordida Stal, 1859 (Hemiptera: Reduviidae) populations in the northern region of Minas Gerais, Brazil. Rev Soc Bras Med Trop 2014; 47(4):426-429. also found such a need when working with T. sordida.

It is important to note that the reference population in this study was collected from the same area where samples used in this assessment were collected, that is, Araçatuba municipality, Nilce Maria location. However, spaying insecticide on the palm trees to control insect populations was not a technical standard at the time. As other vectors are also found in this area, pyrethroids are frequently used in controlling actions, which must be considered for the reference population, as they may show signs of resistance.

The fact that the slope was the same or higher than that of the reference population shows that, in most populations tested, there is little heterogeneity among them. For populations with lower slopes, resistance can be observed, which justifies the follow-up. Molecular studies have indicated less genetic diversity in areas treated with chemical treatment2828. Perez de Rosas AR, Segura EL, Garcia BA. Microssatellites analysis of genetic structure in natural Triatoma infestans (Hemiptera: Reduvidae) populations from Argentina: its implication in assessing the effectiveness of Chagas disease vector control program. Mol Ecol 2007; 16(7):1401-1412.. It is important to highlight that the mortality at the diagnostic dose was 100% in all populations. Genetic variation in populations must be considered as a factor that may directly interfere with test results2121. Pessoa GCD, Dias LS, Diotaiuti L. Deltamethrin pyrethroid susceptibility characterization of Triatoma sordida Stal, 1859 (Hemiptera: Reduviidae) populations in the northern region of Minas Gerais, Brazil. Rev Soc Bras Med Trop 2014; 47(4):426-429.,2929. Amelotti I, Catalá SS, Gorla DE. Experimental evaluation of insectidal paints against Triatoma infestans (Hemiptera: Reduvidae), under natural climatic conditions. Parasit Vectors 2009; 2:30..

Finally, it is essential to analyze triatomine resistance to insecticides through studies aiming to better understand which factors may affect the control of these vectors, in order to evaluate and enhance intervention measures, if necessary. Previous studies have reported R. neglectus populations in palm trees located in urban areas in the Federal District of Goiás, Minas Gerais, and Mato do Grosso do Sul states88. Diotaiuti L, Dias JCP. Ocorrência e biologia de Rhodnius neglectus, Lent, 1954 em macaubeiras da periferia de Belo Horizonte, Minas Gerais. Mem Inst Oswaldo Cruz . 1984;79(3):293-301.,3030. Zapata MTG, Virgens D, Soares VA, Bosworth A, Mardsen PD. House invasion by secondary triatominae species in Mambaí, Goiás-Brazil. Rev Soc Bras Med Trop 1985; 18(3):199-201.,3131. Gurgel-Gonçalves R, Duarte MA, Ramalho ED, Romaña CA, Cuba CAC. Distribuição espacial de populações de triatomíneos (Hemiptera, Reduviidae) em palmeiras da espécie Mauritia flexuosa no Distrito Federal, Brasil. Rev Soc Bras Med Trop 2004; 37(3):241-247.. It is not uncommon to find notifications to public authorities concerning these insects by inhabitants of these areas, indicating that new epidemiological settings may occur.

Recolonization of this species in the environment may be related to behavioral factors and to the fact that they are also associated with birds, which facilitate its wide distribution in municipalities within the São Paulo state99. Rodrigues VLCC, Pauliquévis-Jr C, Silva RA, Wanderley DMV, Guirardo MM, Rodas LAC, et al. Colonization of palm trees by Rhodnius neglectus and household and invasion in an urban area, Araçatuba, São Paulo, Brazil. Rev Inst Med Trop São Paulo. 2014;56(3):213-8.,3232. Forattini OP, Ferreira OA, Silva EOR, Rabello ES. Aspectos ecológicos da tripanossomíase americana. XV - Desenvolvimento, variação e permanência de Triatoma sordida, Panstrongylus megistus e Rhodnius neglectus em eótopos artificiais. Rev Saúde Pública 1979; 13(3):220-234.. Therefore, studies using field and laboratory insecticides simultaneously must be carried out to obtain results that are closer to local reality.

ACKNOWLEDGMENTS

The Triatomine Monitoring Network (REMOT) and the Ministry of Health. To Vera Lúcia Braga Tonietti and Maria Regina de Jesus Eleutério for their assistance in creating and maintaining the insectarium for triatomines and for the readings carried out.

REFERENCES

  • 1
    Jurberg J, Rodrigues JMS, Moreira FFF, Dale C, Cordeiro IRS, Lamas-Jr VD, et al. Atlas iconográfico dos triatomíneos do Brasil (vetores da doença de Chagas). Rio de Janeiro: Instituto Osvaldo Cruz; 2014
  • 2
    World Health Organization [internet]. Chagas disease (American trypanosomiasis). Disponível em: Disponível em: https://www.who.int/health-topics/chagas-disease#tab=tab_1 2021 [acesso em 01 fev 2021].
    » https://www.who.int/health-topics/chagas-disease#tab=tab_1
  • 3
    Basile L, Jansá JM, Carlier Y, Salamanca DD, Angheben A, Bartoloni A, et al. Chagas disease in European countries: the challenge of a surveillance system. Euro Surveill. 2011;16(37):19968.
  • 4
    Souza AG, Wanderley DMV, Buralli GM, Andrade JCR. Consolidation of the control of Chagas disease in State of São Paulo. Mem Inst Oswaldo Cruz. 1984;79:125-32.
  • 5
    Rocha e Silva EO, Rodrigues VLCC, Silva RA, Wanderley DMV. Programa de Controle da Doença de Chagas no estado de São Paulo, Brasil: o controle e a vigilância da transmissão vetorial. Rev Soc Bras Med Trop. 2011;44(Suppl 2):74-84.
  • 6
    Silva RA. Estado atual da vigilância entomológica da doença de Chagas no estado de São Paulo. Brazilian Journal of Health Review. 2019;2(2):742-55.
  • 7
    Oliveira J, Alevi KCC, Almeida CE, Mendonça VJ, Costa J, Rosa JA. Triatoma brasiliensis species complex: characterization of the external female genitalia. J Vector Ecol. 2020;45(1):57-68.
  • 8
    Diotaiuti L, Dias JCP. Ocorrência e biologia de Rhodnius neglectus, Lent, 1954 em macaubeiras da periferia de Belo Horizonte, Minas Gerais. Mem Inst Oswaldo Cruz . 1984;79(3):293-301.
  • 9
    Rodrigues VLCC, Pauliquévis-Jr C, Silva RA, Wanderley DMV, Guirardo MM, Rodas LAC, et al. Colonization of palm trees by Rhodnius neglectus and household and invasion in an urban area, Araçatuba, São Paulo, Brazil. Rev Inst Med Trop São Paulo. 2014;56(3):213-8.
  • 10
    Silva RA. Relatório de avaliação do Rhodnius neglectus em área urbana de municípios da região de Araçatuba. São Paulo: Superintêndencia de Controle de Endemias; 2018.
  • 11
    Pessoa GCD, Vinãs PA, Rosa ACL, Diotaiuti L. History of insecticide resistance of triatominae vectors. Rev Soc Bras Med Trop 2015; 48(4):380-389.
  • 12
    Ministério da Saúde Brasil [internet]. NT-36.2012 - Orientações sobre vigilância entomológica e a utilização de inseticida de ação residual no controle de triatomíneos - vetores da doença de Chagas. Brasília; 2012 [acesso em 6 set 2020].
  • 13
    Lent H, Wygodzinsky PW. Revision of the Triatominae (Hemiptera, Reduviidae), and their significance as vectors of Chagas disease. Bull Am Mus Nat Hist. 1979;163(1):123-520.
  • 14
    Organizacion Panamericana de la Salud (PAHO). II Reunion técnica latino-americana de monitoreo de resistência a inseticidas em triatominos vectores de Chagas, OPS. Panamá: PAHO; 2005.
  • 15
    Pessoa GCD, Silva RA, Alves RV, Costa VM, Cavalcante KRLJ, Diotaiuti L. Fortalecimento da vigilância em saúde no Brasil: Rede de Monitoramento da resistência dos triatomíneos aos inseticidas. Rev Patol Trop 2016; 45(4):417-424.
  • 16
    Yon C, Balta R, García N, Troyes M, Cumpa H, Valdivia A. Susceptibilidad y resistencia de Triatoma infestans y Panstrongylus herreri a los insecticidas piretroides, Perú 2001. Revista Peruana de Medicina Experimental y Salud Pública. 2004; 21(3):179-182.
  • 17
    Santos MAT, Areas MA, Reyes FG. Piretróides - uma visão geral. Alimentos e Nutrição Araraquara 2007; 18(3):339-349.
  • 18
    Pessoa GCD, Rosa AC, Bedin C, Wilhelms T, Mello F, Coutinho HS, et al. Susceptibility characterization of residual Brazilian populations of Triatoma infestans Klug, 1834 (Hemiptera: Reduviidae) to deltamethrin pyrethroid. Rev Soc Bras Med Trop 2015; 48:157-161.
  • 19
    Depickère S, Buitrago R, Siñani E, Baune M, Monje M, Lopez R, et al. Susceptibility and resistance to deltamethrin of wild and domestic populations of Triatoma infestans (Reduviidae: Triatominae) in Bolivia: new discoveries. Mem Inst Oswaldo Cruz 2012; 107:1042-47.
  • 20
    Obara MT, Otrera VCG, Gonçalves RG, Santos JP, Santalucia M, Rosa JA, et al. Monitoramento da suscetibilidade de populações de Triatoma sordida Stal, 1859 (Hemiptera: Reduviidae) ao inseticida deltametrina, na região centro-oeste do Brasil. Rev Soc Bras Med Trop 2011; 44(2):206-212.
  • 21
    Pessoa GCD, Dias LS, Diotaiuti L. Deltamethrin pyrethroid susceptibility characterization of Triatoma sordida Stal, 1859 (Hemiptera: Reduviidae) populations in the northern region of Minas Gerais, Brazil. Rev Soc Bras Med Trop 2014; 47(4):426-429.
  • 22
    Pessoa GCD, Trevizani NAB, Dias LS, Bezerra CM, Melo BV, Diotaiuti L. Toxicological profile of deltamethrin in Triatoma brasiliensis (Hemiptera: Reduviidae) in state of Ceará, northeastern Brazil. Rev Soc Bras Med Trop 2015; 48(1):39-43.
  • 23
    Pessoa GCD, Santos TRM, Salazra GC, Dias LS, Mello BV, Ferraz ML, et al. Variability of susceptibility to deltamethrin in peridomestic Triatoma sordida from Triângulo Mineiro, state of Minas Gerais, Brazil. Rev Soc Bras Med Trop 2015; 48(4):417-421.
  • 24
    Pessoa GCD, Rosa ACL, Cavalari L, Rezende JG, Mello BV, Diotaiuti L. Susceptibility of Triatoma sordida Stal, 1859 (Hemiptera: Reduviidae) to alpha-cypermethrin under natural climatic conditions. Rev Soc Bras Med Trop 2015; 48(4):422-426.
  • 25
    Vassena C, Picollo M, Zerba E. Insecticide resistance in Brazilian Triatoma infestans and Venezuelan Rhodnius prolixus Med Vet Entomol 2000; 14(1):51-5.
  • 26
    Camargo-Neves VLFD, Katz G, Rodas LAC, Poletto DW, Lage LC, Spínola RMF, et al. Utilização de ferramentas de análise espacial na vigilância epidemiológica de leishmaniose visceral americana-Araçatuba, São Paulo, Brasil, 1998-1999. Cad Saúde Pública 2001; 17:1263-67.
  • 27
    Narahashi T. Neuronal ion channel as the target sites of insecticides. Pharmacol Toxicol 1996; 79(1):1-14.
  • 28
    Perez de Rosas AR, Segura EL, Garcia BA. Microssatellites analysis of genetic structure in natural Triatoma infestans (Hemiptera: Reduvidae) populations from Argentina: its implication in assessing the effectiveness of Chagas disease vector control program. Mol Ecol 2007; 16(7):1401-1412.
  • 29
    Amelotti I, Catalá SS, Gorla DE. Experimental evaluation of insectidal paints against Triatoma infestans (Hemiptera: Reduvidae), under natural climatic conditions. Parasit Vectors 2009; 2:30.
  • 30
    Zapata MTG, Virgens D, Soares VA, Bosworth A, Mardsen PD. House invasion by secondary triatominae species in Mambaí, Goiás-Brazil. Rev Soc Bras Med Trop 1985; 18(3):199-201.
  • 31
    Gurgel-Gonçalves R, Duarte MA, Ramalho ED, Romaña CA, Cuba CAC. Distribuição espacial de populações de triatomíneos (Hemiptera, Reduviidae) em palmeiras da espécie Mauritia flexuosa no Distrito Federal, Brasil. Rev Soc Bras Med Trop 2004; 37(3):241-247.
  • 32
    Forattini OP, Ferreira OA, Silva EOR, Rabello ES. Aspectos ecológicos da tripanossomíase americana. XV - Desenvolvimento, variação e permanência de Triatoma sordida, Panstrongylus megistus e Rhodnius neglectus em eótopos artificiais. Rev Saúde Pública 1979; 13(3):220-234.
  • Financial Support: René Rachou Research Center (CPqRR), Oswaldo Cruz Foundation (FIOCRUZ), Health Surveillance Secretariat (SVS), Ministry of Health (MS), Endemic Disease Control Superintendence (SUCEN) and Municipal Health Secretariat of Araçatuba, Birigui, Guararapes and Piacatu.

Publication Dates

  • Publication in this collection
    25 Feb 2022
  • Date of issue
    2022

History

  • Received
    11 Sept 2021
  • Accepted
    09 Dec 2021
Sociedade Brasileira de Medicina Tropical - SBMT Caixa Postal 118, 38001-970 Uberaba MG Brazil, Tel.: +55 34 3318-5255 / +55 34 3318-5636/ +55 34 3318-5287, http://rsbmt.org.br/ - Uberaba - MG - Brazil
E-mail: rsbmt@uftm.edu.br