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Triatomine vectors of Trypanosoma cruzi in an endemic area for Chagas disease in Northeast Brazil

ABSTRACT

Background:

We assessed the distribution of triatomines in an endemic area for Chagas disease.

Methods:

This retrospective study used secondary data extracted from the Official System of the National Chagas Disease Control Program (Sistema Oficial do Programa Nacional de Controle da Doença de Chagas - SisPCDCh).

Results:

A total of 7,257 (725.7 ± 221.7 per year) specimens were collected from 2013 to 2022. Most of them (6,792; 93.6%) were collected in the intradomicile and 465 (6.4%) in the peridomicile. A total of 513 (7.1%) triatomines tested positive for the presence of trypomastigote forms, similar to Trypanosoma cruzi.

Conclusions:

The spatial analysis revealed a heterogeneous distribution of triatomines across different municipalities.

Keywords:
Triatominae; Panstrongylus; Triatoma; Infection rate; Spatial distribution; Trypanosomatidae

Triatomines (Reduviidae: Triatominae) are arthropod vectors of the protozoon Trypanosoma cruzi (Kinetoplastida: Trypanosomatidae), which is the causative agent of Chagas disease (CD)11. World Health Organization (WHO). Chagas disease (American trypanosomiasis); 2022 [updated 2022 July 12; cited 2023 Aug 2]. Available from: Available from: https://www.who.int/health-topics/chagas-disease#tab=tab_1 .
https://www.who.int/health-topics/chagas...
. CD is considered a neglected illness of great importance in Latin America. However, epidemiological changes, mainly due to population mobility, urbanization, and emigration, have increased cases in Canada, the United States, European and African countries, the Eastern Mediterranean, and the Western Pacific22. World Health Organization (WHO). Chagas disease in Latin America: an epidemiological update based on 2010 estimates. Week Epidemiol Rec. 2015;90(6):33-44.. It is estimated that globally, approximately 75 million people live in at-risk areas and 6-7 million are infected, with approximately 14,000 deaths annually. In humans, the classical transmission route is through contact with trypomastigote forms of T. cruzi shed on the feces of vectors after a blood meal².

In some Brazilian regions, precarious human dwellings are still observed, which facilitate the establishment and reproduction of triatomine species, because they may serve as shelters. Over the last few years, extensive chemical control of triatomines in households has led to the absence of T. cruzi transmission by Triatoma infestans in Brazil33. Ferreira ILM, Silva TPT. Eliminação da transmissão da doença de Chagas pelo Triatoma infestans no Brasil: um fato histórico. Rev Soc Bras Med Trop. 2006;39(5):507-9.. However, other species (e.g., Panstrongylus lutzi, Panstrongylus megistus, Triatoma brasiliensis, and Triatoma pseudomaculata) continue to play an essential role in T. cruzi transmission44. Ferreira ALS, Santana MA, Santos LVB, Monteiro DP, Campos JHF, Sena LLJ, et al. Triatoma brasiliensis Neiva, 1911 and Triatoma pseudomaculata Corrêa and Espínola, 1964 (Hemiptera, Reduviidae, Triatominae) in rural communities in Northeast Brazil. Rev Inst Med Trop Sao Paulo. 2020;62:e74.,55. Melo CM, Cruz ACFG, Lima AFVA, Silva LR, Madi RR, Jeraldo VL, et al. Triatomine fauna and recent epidemiological dynamics of Chagas disease in an endemic area of Northeast Brazil. Can J Infect Dis Med Microbiol. 2018;2018:1-13.. Most present an invasive behavior already found in domestic and peridomestic environments in regions endemic for CD66. Dias JCP. Vigilância epidemiológica em doença de Chagas. Cad Saude Publica. 2000;16:43-59.,77. Sarquis O, Carvalho-Costa FA, Toma HK, Georg I, Burgoa MR, Lima MM. Eco-epidemiology of Chagas disease in northeastern Brazil: Triatoma brasiliensis, T. pseudomaculata and Rhodnius nasutus in the sylvatic, peridomestic and domestic environments. Parasitol Res. 2012;110(4):1481-5..

An important strategy for the Chagas Disease Control Program (ChDCP) is establishing triatomine information posts (PITs). In these places, residents from endemic areas may deliver insects suspected of being kissing bugs for identification by the health surveillance service88. Souza JMB. Vigilância da Doença de Chagas: manual técnico das atividades de controle dos triatomíneos. Belo Horizonte: Instituto René Rachou; 2019. p. 28-32.. Passive surveillance has been an important measure for monitoring the triatomine population and is useful for driving strategies for CD control. A previous study conducted in the state of Pernambuco demonstrated that 8.8% of triatomines collected were naturally infected with T. cruzi, and of 10 different species collected, T. pseudomaculata, T. brasiliensis, and P. lutzi predominated99. Silva A, Beatriz M, Barreto AVMS, Silva HA, Galvão C, Rocha D, et al. Synanthropic Triatomines (Hemiptera, Reduviidae) in the State of Pernambuco, Brazil: Geographical Distribution and Natural Trypanosoma Infection Rates between 2006 and 2007. Rev Soc Bras Med Trop . 2012;45(1):60-5..

In times of rapid environmental change and marked anthropogenic influence on the degradation of natural habitats of animals and vectors, knowledge of the distribution of triatomines is pivotal for driving preventive measures against CD1010. Coura JR. Doença de Chagas. In: Coura JR, editor. Síntese das doenças infecciosas e parasitárias. 1st ed. Rio de Janeiro: Guanabara Koogan; 2008. p. 12-8.,1111. Vinhaes MC, de Oliveira SV, Reis PO, de Lacerda Sousa AC, Silva RA, Obara MT, et al. Assessing the vulnerability of Brazilian municipalities to the vectorial transmission of Trypanosoma cruzi using multi-criteria decision analysis. Acta Trop. 2014;137:105-10.. Therefore, we assessed the distribution and infection rates of T. cruzi in triatomines collected from a region endemic for CD in Northeast Brazil.

This retrospective study used secondary data (2013-2022) obtained from the Official System of the National Chagas Disease Control Program (Sistema Oficial do Programa Nacional de Controle da Doença de Chagas - SisPCDCh) in the state of Pernambuco (Consent Letter 001/2022). Triatomines were actively (Caruaru and Santa Cruz do Capibaribe) and passively obtained from the municipalities and delivered to the IV Gerência Regional de Saúde do Estado de Pernambuco (IV GERES). The database was fed daily at the municipal level and information was sent weekly to the IV GERES. The study area comprised 32 municipalities in the Agreste region located in the state of Pernambuco (Figure 1).

FIGURE 1:
Study area - Municipalities located in the Agreste region of the state of Pernambuco, Brazil.

Data on triatomine species, capture area (intradomicile or peridomicile), and life stage (adult or nymph) were obtained (Supplementary Table 1). According to ChDCP, T. cruzi infection was detected by abdominal compression of each specimen followed by microscopic analysis. The abdominal content was placed on a microscope slide with 20 microliters of 0.9% saline solution, covered with a coverslip and analyzed at different magnifications (40× and 100×).

Infection rates were determined based on absolute and relative frequencies. The chi-square test (χ²) was used to analyze the stages of development of triatomines and ecotypes (intradomicile or peridomicile) and between infected species of triatomines in the ecotypes. The G-test was used to analyze the number of triatomines captured in the intradomicile or peridomicile, the predominant species in these municipalities, and the species in the ecotypes (intradomicile or peridomicile). The significance level was set at 5%, and all analyses were performed using the BioEstat software version 5.3¹²12. Ayres M, Ayres M Jr, Santos AAS. BIOESTAT - statistical applications on the biomedical sciences. 4th ed. Belém: CNPq; 2007. 364 p..

Maps were produced using QGIS 3.22.10, in which vector layers were inserted into a shapefile obtained from the Instituto Brasileiro de Geografia e Estatística (IBGE) database. A thematic map showed the number of triatomines captured in each municipality. A second was represented by the main species captured, and the frequency was represented by a histogram grouped by the color scale.

A total of 7,257 (725.7 ± 221.7 per year) triatomines belonging to nine species were collected during the study period. Most specimens were collected in the intradomicile (6,792; 93.6%) and some (465; 6.4%) in the peridomicile area. Triatomines were collected per year as follows: 2013 (n = 911; 12.6%); 2014 (n = 735; 10.1%); 2015 (n = 1,023; 15%); 2016 (n = 815 11.2%); 2017 (n = 818 11.3%); 2018 (n = 835; 11.5%); 2019 (n = 824; 11.3%); 2020 (n = 550; 7.6%); 2021 (n = 403; 5.5%), and 2022 (n = 343; 4.8%). Caruaru (n = 2,274; 31.3%) was the municipality that registered the highest number of specimens, followed by Santa Cruz do Capibaribe (n = 1,961; 27%) and São Bento do Una (n = 686; 9.4%) (G-test = 232.5792; p = 0.0000).

A total of 6,530 (96.2%) adults and 262 (3.8%) nymphs were collected in the intradomicile, while 337 (72.5%) adults and 128 (27.5%) nymphs were found in peridomicile areas (χ² = 474.815; p = 0.0000). The most common triatomine was P. lutzi (n = 2,891; 39.8%), followed by T. brasiliensis (n = 2,617; 37%), T. pseudomaculata (n = 1,343; 18.5%), and P. megistus (n = 314; 4.32%) (G-test = 86.9616; p = 0.0000). Data for all collected triatomine species and rates of infection by T. cruzi are reported in Table 1.

Out of 7,240 triatomines tested, 7.1% (n = 513) were positive for the presence of trypomastigote forms similar to T. cruzi (Table 1). The highest number of infected triatomines (n = 114; 12.7%) was recorded in 2013. Triatoma brasiliensis (12.2%; 318/2,607), Triatoma melanocephala (10%; 1/10), and P. lutzi (6.1%; 176/2,890) presented higher rates of infection (Table 1). Some of the collected specimens were not examined (n = 17) because of inadequate sample conditions.

TABLE 1:
Triatomine species collected and examined for positivity, and infection rate by T. cruzi.

Spatial analysis revealed a heterogeneous distribution of triatomines in the study area. Of the 32 municipalities, 17 had frequencies below 50, whereas Caruaru and Santa Cruz do Capibaribe exhibited the highest frequencies of collected specimens (>1,000) (Figure 2). Panstrongylus lutzi and T. brasiliensis were predominant in Caruaru, Santa Cruz do Capibaribe, Brejo da Madre de Deus, and Belo Jardim (>50 specimens). For T. pseudomaculata and P. megistus, a homogeneous distribution was observed among municipalities (<50 specimens) (Figure 3).

FIGURE 2:
Overall distribution of triatomines collected from 2013 to 2022.

FIGURE 3:
Distribution of Panstrongylus lutzi, Panstrongylus megistus, Triatoma brasiliensis, and Triatoma pseudomaculata collected from 2013 to 2022.

This study revealed a wide distribution of triatomine vectors in an endemic area for CD, with a positivity rate of 7.1% for trypanosomatid forms, similar to T. cruzi. The collection of most triatomines in the intradomicile has been reported in previous studies, demonstrating their closer proximity to humans and facilitating T. cruzi infection on an endemic scale99. Silva A, Beatriz M, Barreto AVMS, Silva HA, Galvão C, Rocha D, et al. Synanthropic Triatomines (Hemiptera, Reduviidae) in the State of Pernambuco, Brazil: Geographical Distribution and Natural Trypanosoma Infection Rates between 2006 and 2007. Rev Soc Bras Med Trop . 2012;45(1):60-5.,1313. Silva TRM, Barros GMMR, Lima TARF, Giannelli A, Silva GM, Alves KML, et al. Spatial distribution of triatomine bugs in a Chagas disease endemic region in Brazil. Rev Soc Bras Med Trop . 2019;52:e20190278.. Currently, in most municipalities, these specimens are obtained mainly through passive surveillance, in which people collect and deliver them to each municipality's health services. This passive surveillance is likely to be a critical bias influencing the higher number of specimens collected in the intradomicile. The finding of nymphs indoors suggests adaptation and the potential ability to colonize human dwellings, posing an additional risk for human vector exposure and, consequently, T. cruzi infection55. Melo CM, Cruz ACFG, Lima AFVA, Silva LR, Madi RR, Jeraldo VL, et al. Triatomine fauna and recent epidemiological dynamics of Chagas disease in an endemic area of Northeast Brazil. Can J Infect Dis Med Microbiol. 2018;2018:1-13.,1414. Lima-Neiva V, Toma HK, Abrantes Aguiar LM, Lopes CM, Dias LP, Monte Gonçalves TC, et al. The connection between Trypanosoma cruzi transmission cycles by Triatoma brasiliensis: A threat to human health in an area susceptible to desertification in the Seridó, Rio Grande do Norte, Brazil. PLoS Negl Trop Dis. 2021;15(11):e0009919..

The rising retrieval of triatomines in peri- or intradomicile areas observed across different studies may be a consequence of two main factors: i) climate change, deforestation, and expansion of agricultural areas moving triatomine populations from the original habitat to peri- or intradomicile areas1414. Lima-Neiva V, Toma HK, Abrantes Aguiar LM, Lopes CM, Dias LP, Monte Gonçalves TC, et al. The connection between Trypanosoma cruzi transmission cycles by Triatoma brasiliensis: A threat to human health in an area susceptible to desertification in the Seridó, Rio Grande do Norte, Brazil. PLoS Negl Trop Dis. 2021;15(11):e0009919., and ii) the ability of dispersion by flying guided by artificial lights, thus favoring the invasion of houses.

P. lutzi likely has great epidemiological importance in the study area since it was reported in almost all municipalities (90.6%). Its absence in three municipalities (Barra de Guabiraba, Camocim de São Félix, and São Joaquim do Monte) may be related to its location in high-altitude areas (from 462 to 723 m above sea level), milder climate, and higher rates of rainfall. In addition, these municipalities are located in an area characterized by typical vegetation of the Atlantic Forest, which differs from the other assessed municipalities. The importance of this vector cannot be underestimated because its natural infection rate and adaptation to domiciles are high.

Currently, T. brasiliensis is considered the primary vector in Northeast Brazil99. Silva A, Beatriz M, Barreto AVMS, Silva HA, Galvão C, Rocha D, et al. Synanthropic Triatomines (Hemiptera, Reduviidae) in the State of Pernambuco, Brazil: Geographical Distribution and Natural Trypanosoma Infection Rates between 2006 and 2007. Rev Soc Bras Med Trop . 2012;45(1):60-5.. In Pernambuco, its distribution was previously assessed and found to be predominant over other triatomine species99. Silva A, Beatriz M, Barreto AVMS, Silva HA, Galvão C, Rocha D, et al. Synanthropic Triatomines (Hemiptera, Reduviidae) in the State of Pernambuco, Brazil: Geographical Distribution and Natural Trypanosoma Infection Rates between 2006 and 2007. Rev Soc Bras Med Trop . 2012;45(1):60-5.. Despite being more abundant, the infection rate of T. cruzi was lower than that of P. lutzi. In the present study, many T. brasiliensis were collected from the peridomicile, and livestock animals were observed close to the houses. The presence of animals (e.g., cattle, sheep, and goats) close to human dwellings facilitates the establishment of triatomine populations because they have a continuous feeding source1414. Lima-Neiva V, Toma HK, Abrantes Aguiar LM, Lopes CM, Dias LP, Monte Gonçalves TC, et al. The connection between Trypanosoma cruzi transmission cycles by Triatoma brasiliensis: A threat to human health in an area susceptible to desertification in the Seridó, Rio Grande do Norte, Brazil. PLoS Negl Trop Dis. 2021;15(11):e0009919..

Triatoma pseudomaculata is distributed in the Northeast, Midwest, and Minas Gerais, and can be found mainly in the wild (tree bark, rodents, and marsupial refuges), peridomestic (corrals and chicken coops), and occasionally intradomicile environments1515. de la Fuente AL, Minoli AS, Lopes CM, Noireau F, Lazzari CR, Lorenzo MG. Flight dispersal of the Chagas Disease vectors Triatoma brasiliensis and Triatoma pseudomaculata in Northeastern Brazil. Acta Trop. 2007;101(2):115-9.. The low infection rate of T. pseudomaculata in this study corroborates previous research. Triatomine is a low-efficiency vector with a small rate of infection1515. de la Fuente AL, Minoli AS, Lopes CM, Noireau F, Lazzari CR, Lorenzo MG. Flight dispersal of the Chagas Disease vectors Triatoma brasiliensis and Triatoma pseudomaculata in Northeastern Brazil. Acta Trop. 2007;101(2):115-9..

Despite this, the overall reduction in specimens collected over 10 years could be a consequence of improvements in human dwellings as well as the hygiene conditions of the population. However, it is interesting to note that the health decentralization process that occurred in Brazil in 1999 created important gaps in the control of endemic diseases. The lack of financial resources in municipalities, along with the scarcity of qualified human resources, may also contribute to the reduction in entomological surveillance.

From 2021 to 2022, the marked reduction in surveillance actions can also be explained by the Coronavirus pandemic; a mean of 336 specimens were collected annually in the study area during the 2 years cited above. In addition, the actions of the ChDCP have been executed unevenly by the municipality’s health services. For instance, in the municipalities of Caruaru and Santa Cruz do Capibaribe, there is active vigilance from a team of professionals exclusively involved in entomological surveillance. In municipalities with active vigilance, there is training of human resources involved in the parasitological examination of triatomines, which can contribute to the positivity observed in these vectors. Improving entomological surveillance (e.g., active surveillance, chemical control, and educational programs) is paramount to mitigating the risk of vector exposure for animal and human populations living in this area. Finally, the prevention of CD may not be restricted to the control of triatomine vectors by health services. It is necessary to implement educational measures to improve the awareness of the local population regarding the importance of managing the peridomicile environment and avoiding the presence of shelters for these vectors.

ACKNOWLEDGEMENTS

This article is based on the Ph.D. thesis (Graduate Program in Animal Bioscience) of the first author, developed at the Federal Rural University of Pernambuco, and supported by a grant fellowship from the Coordination for the Improvement of Personnel of Higher Education (CAPES). R.A.N.R. receives a research fellowship from CNPq (Bolsa de Produtividade; Grant No. 305971/2021-2).

REFERENCES

  • 1
    World Health Organization (WHO). Chagas disease (American trypanosomiasis); 2022 [updated 2022 July 12; cited 2023 Aug 2]. Available from: Available from: https://www.who.int/health-topics/chagas-disease#tab=tab_1
    » https://www.who.int/health-topics/chagas-disease#tab=tab_1
  • 2
    World Health Organization (WHO). Chagas disease in Latin America: an epidemiological update based on 2010 estimates. Week Epidemiol Rec. 2015;90(6):33-44.
  • 3
    Ferreira ILM, Silva TPT. Eliminação da transmissão da doença de Chagas pelo Triatoma infestans no Brasil: um fato histórico. Rev Soc Bras Med Trop. 2006;39(5):507-9.
  • 4
    Ferreira ALS, Santana MA, Santos LVB, Monteiro DP, Campos JHF, Sena LLJ, et al. Triatoma brasiliensis Neiva, 1911 and Triatoma pseudomaculata Corrêa and Espínola, 1964 (Hemiptera, Reduviidae, Triatominae) in rural communities in Northeast Brazil. Rev Inst Med Trop Sao Paulo. 2020;62:e74.
  • 5
    Melo CM, Cruz ACFG, Lima AFVA, Silva LR, Madi RR, Jeraldo VL, et al. Triatomine fauna and recent epidemiological dynamics of Chagas disease in an endemic area of Northeast Brazil. Can J Infect Dis Med Microbiol. 2018;2018:1-13.
  • 6
    Dias JCP. Vigilância epidemiológica em doença de Chagas. Cad Saude Publica. 2000;16:43-59.
  • 7
    Sarquis O, Carvalho-Costa FA, Toma HK, Georg I, Burgoa MR, Lima MM. Eco-epidemiology of Chagas disease in northeastern Brazil: Triatoma brasiliensis, T. pseudomaculata and Rhodnius nasutus in the sylvatic, peridomestic and domestic environments. Parasitol Res. 2012;110(4):1481-5.
  • 8
    Souza JMB. Vigilância da Doença de Chagas: manual técnico das atividades de controle dos triatomíneos. Belo Horizonte: Instituto René Rachou; 2019. p. 28-32.
  • 9
    Silva A, Beatriz M, Barreto AVMS, Silva HA, Galvão C, Rocha D, et al. Synanthropic Triatomines (Hemiptera, Reduviidae) in the State of Pernambuco, Brazil: Geographical Distribution and Natural Trypanosoma Infection Rates between 2006 and 2007. Rev Soc Bras Med Trop . 2012;45(1):60-5.
  • 10
    Coura JR. Doença de Chagas. In: Coura JR, editor. Síntese das doenças infecciosas e parasitárias. 1st ed. Rio de Janeiro: Guanabara Koogan; 2008. p. 12-8.
  • 11
    Vinhaes MC, de Oliveira SV, Reis PO, de Lacerda Sousa AC, Silva RA, Obara MT, et al. Assessing the vulnerability of Brazilian municipalities to the vectorial transmission of Trypanosoma cruzi using multi-criteria decision analysis. Acta Trop. 2014;137:105-10.
  • 12
    Ayres M, Ayres M Jr, Santos AAS. BIOESTAT - statistical applications on the biomedical sciences. 4th ed. Belém: CNPq; 2007. 364 p.
  • 13
    Silva TRM, Barros GMMR, Lima TARF, Giannelli A, Silva GM, Alves KML, et al. Spatial distribution of triatomine bugs in a Chagas disease endemic region in Brazil. Rev Soc Bras Med Trop . 2019;52:e20190278.
  • 14
    Lima-Neiva V, Toma HK, Abrantes Aguiar LM, Lopes CM, Dias LP, Monte Gonçalves TC, et al. The connection between Trypanosoma cruzi transmission cycles by Triatoma brasiliensis: A threat to human health in an area susceptible to desertification in the Seridó, Rio Grande do Norte, Brazil. PLoS Negl Trop Dis. 2021;15(11):e0009919.
  • 15
    de la Fuente AL, Minoli AS, Lopes CM, Noireau F, Lazzari CR, Lorenzo MG. Flight dispersal of the Chagas Disease vectors Triatoma brasiliensis and Triatoma pseudomaculata in Northeastern Brazil. Acta Trop. 2007;101(2):115-9.

Publication Dates

  • Publication in this collection
    05 Feb 2024
  • Date of issue
    2024

History

  • Received
    23 Aug 2023
  • Accepted
    17 Nov 2023
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