Occurrence and Distribution of Triatomines (Hemiptera: Reduviidae) in Municipalities of the Northeastern Region of Minas Gerais State, Brazil

Rev Soc Bras Med Trop 49(4):502-507, July-August, 2016 doi:10.1590/0037-8682-0142-2016

Short Communication

Occurrence and distribution of triatomines (Hemiptera: Reduviidae) in municipalities of the Northeastern region of Minas Gerais State, Brazil

João Victor Leite Dias[1],[2], Eduardo Geraldo Fernandes[3], Herton Helder Rocha Pires[1],[2] and João Carlos Pinto Dias[1]

[1]. Laboratório de Triatomíneos e Epidemiologia da Doença de Chagas, Centro de Pesquisas René Rachou, Fundação Oswaldo Cruz, Belo Horizonte, Minas Gerais, Brasil. [2]. Grupo de Extensão e Pesquisa em Saúde Coletiva Jequi, Universidade Federal dos Vales do Jequitinhonha e Mucuri, Diamantina, Minas Gerais, Brasil. [3]. Superintendência Regional de Saúde de Diamantina, Diamantina, Minas Gerais, Brasil.

Abstract Introduction: Triatomines are targeted for the control of Chagas disease in endemic areas of Brazil. Methods: Data regarding triatomines captured during 2001-2008 in 34 municipalities in the Northeast of Minas Gerais were analyzed. Results: In total, 11,187 triatomines from eight species were captured, mostly in henhouses and bedrooms. Trypanosomes were found in 203 samples. Main species were Triatoma sordida, Panstrongylus megistus, and Triatoma vitticeps. The number of P. megistus adults was positively correlated with temperature and precipitation, whereas the number of nymphs followed the inverse pattern. Conclusions: Occurrence of triatomines in domiciles indicates the need for sustained entomological surveillance. Keywords: Triatominae. Chagas disease. Entomological surveillance.

Although there are at least 148 living species of triatomine the Centro Regional de Saúde de Diamantina, both of which bugs, only a few of them are epidemiologically important for the implemented an entomological surveillance system. However, transmission of Trypanosoma cruzi to humans(1). In 2006, Brazil these activities were interrupted owing to political-administrative was certifi ed as free from Trypanosoma cruzi transmission by issues, thus contributing to re-establishment of intradomiciliary Triatoma infestans, the country’s main vector of this parasite. In triatomine colonies. This imposed a reactivation of vertical this context, other species have become increasingly important actions by the national Chagas Disease Control Program in Chagas disease epidemiology, mainly owing to anthropic (CDCP) in 1982, carried out by Superintendência de Campanhas (2) pressure on their natural ecotopes . de Saúde Pública(4). Since the late 1990s, entomological The Jequitinhonha Valley, located in the Northeastern region surveillance has been a responsibility of the municipalities. of Minas Gerais State, Brazil, represented a highly endemic This study aimed to characterize the triatomine infestation area for Chagas disease, with domiciles densely infested by in domiciliary environments of 34 municipalities under triatomines, mainly Panstrongylus megistus and Triatoma coordination of the Diamantina Regional Health Superintendence infestans. Since the 1950s, this region has suffered important (DRHS), most of them situated in the Jequitinhonha Valley environmental and demographic changes such as expansion of region. The total population of these municipalities is nearly eucalyptus plantations, pasture areas, and rural exodus(3). 429,515 inhabitants, with 40.2% residing in rural areas(5). Activities for controlling Chagas disease spread in this Data on the triatomines captured and examined by the region were started in the 1960s under the coordination of DRHS from October 2001 until December 2008 were obtained the Departamento Nacional de Endemias Rurais (DNERu) by consulting the records of triatomine examinations carried and continued in the 1970s under the supervision of the out in the DRHS laboratory. This period was the latest period Comissão de Desenvolvimento do Vale do Jequitinhonha and with complete information available for all the municipalities of this region. According to the routine followed for triatomine control Corresponding author: Dr. João Victor Leite Dias. actions, the insects captured in the municipalities (by means e-mail: [email protected] Received 15 April 2016 of notifi cation by residents, by investigation of notifi cation by Accepted 24 June 2016 health professional, or active search by health professionals

502 Dias JVL et al. - Triatomines in Northeast Minas Gerais even without previous notifi cation by residents) were sent (120♂, 116♀; p = 0.85). In the peridomicile, statistically to the laboratory for identification and examination for signifi cant difference between the number of males and females trypanosomatids, and the date, locality, and municipality of was recorded for P. megistus (394♂, 587♀; p < 0.01) and the capture, the site where the specimen was found, and its T. sordida (681♂, 1,095♀; p < 0.01) but not for T. vitticeps sex or evolutionary stage were registered. The frequency of (69♂, 55♀; p = 0.24), P. geniculatus (14♂, 15♀; p = 1.00), each species, capture site, presence in each municipality, sex and T. pseudomaculata (46♂, 49♀; p = 0.84). Other species or nymph instar, and trypanosomatid presence was analyzed. had few specimens; thus, statistical analysis was not possible. Chi-square test was used to compare the number of males and Although the capture site was unknown for a large part of females (α = 0.05). the records (21.1% of peridomicile and 12.4% of intradomicile Entomological data were compared to the region’s mean captures), the henhouse was the outbuilding with the temperature and monthly accumulated precipitation to correlate greatest number of triatomine bugs captured (67.2%). In the these variables and the seasonality of most often captured intradomicile, the bedroom was the most frequently infested species and their evolutionary stages. The climate data were room (50%), followed by the living room (26.6%). obtained from the climatological normals of the fi ve weather The largest number of P. megistus specimens was captured stations located in the study area. These normals comprise the between the months of October and December, with a historical average of weather data of long and relatively uniform predominance of adults between October and April (Figure 2A). periods grouped by month; in this study, we used the data from There was a strong direct correlation between the number of 1961 to 1990 (available at http://www.inmet.gov.br/portal/ adult specimens and the monthly average temperature (r = 0.71, index.php?r=clima/normaisClimatologicas). The entomological p < 0.01) and accumulated precipitation (ρ = 0.94, p < 0.01). data from October to December 2001 were excluded from the In contrast, the number of nymphs of P. megistus was strongly analysis to avoid overestimation of these months. negatively correlated with temperature (r = -0.87, p < 0.01) and Data normality was assessed by Shapiro-Wilk test, the precipitation (ρ = -0.79, p < 0.01). correlation between the number of adults and nymphs captured A greater number of T. sordida was recorded for the month of and the monthly mean compensated temperature was evaluated November, although there was no defi ned pattern in the adults/ by the Pearson linear correlation coefficient (r), and the nymphs relation for each month (Figure 2B). There was no correlation between the number of adults and nymphs and the statistically signifi cant correlation between climatic variables monthly accumulated precipitation was evaluated by Spearman's and the number of captured adults (temperature: r = -0.54, correlation coeffi cient (ρ). All the statistical analyses were p = 0.07; precipitation: ρ = -0.27, p = 0.39) or nymphs performed with Bioestat 5.0. (temperature: r = -0.17, p = 0.61; precipitation: ρ = 0.03, p = 0.93). During 2001-2008, 11,187 triatomines were collected Most T. vitticeps specimens were captured between October from all the municipalities, ranging from 5 to 2,477 specimens and November, with adults being predominant throughout per municipality. Ten species were identifi ed: Panstrongylus the year. Nymphs were captured more frequently between diasi, Panstrongylus geniculatus, Panstrongylus megistus, May and August (Figure 2C). The number of adults captured Psammolestes tertius, Rhodnius domesticus, R. neglectus, has shown a positive moderate correlation with the monthly Triatoma arthurneivai, T. pseudomaculata, T. sordida, and average temperature, although with no statistical signifi cance Triatoma vitticeps, and their distributions were examined (r = 0.55, p = 0.07). In contrast, the monthly accumulated ( ). Figure 1 average precipitation has shown a strong direct correlation with The intestinal content of 8,270 (73.9%) insects was the number of winged specimens captured (ρ = 0.74, p < 0.01). examined, and 203 (2.5%) were positive for trypanosomatids. A strong inverse correlation was observed between the number Adults were infected more frequently than nymphs, and of nymphs and temperature (r = -0.92, p < 0.01) and the number the highest infection index was observed in Panstrongylus of nymphs and precipitation (ρ = -0.74, p < 0. 01). geniculatus and T. vitticeps (Table 1). Jequitinhonha Valley represented an area of intense Regarding the capture site, 57.2% (6,401) of the insects were transmission of Chagas disease. According to the data from captured at the peridomicile; 36.7% (4,102), in the intradomicile; the National Serological Inquiry collected in the 1980s, the 2.2% (245), at other places, and for 3.9% (439) of the insects, the municipalities that now belong to the DRHS reported an average site of capture was unknown. The adult specimens were captured of 14.9% of seropositive people, while the State of Minas mainly in the intradomiciliary environments, while immature Gerais reported approximately 8.8%(6). In the 1980s, seven forms prevailed in the peridomicile. T. sordida and P. megistus species of triatomine bugs were captured in domiciles of that were mainly captured in the peridomicile, while the others region (T. infestans, P. megistus, T. sordida, T. pseudomaculata, species were mostly captured in the intradomicile (Table 1). T. vitticeps, P. geniculatus, and R. neglectus)(7). Due to intense In the intradomicile, there were signifi cantly more females activities performed by the CDCP in that region, Triatoma (♀) than males (♂) for P. megistus (716♂, 870♀; p < 0.01) and T. infestans was eliminated and the remaining species were sordida (152♂, 301♀; p < 0.01), whereas the opposite trend was controlled inside the domiciliary environment, resulting in a noted for T. vitticeps (559♂, 425♀; p < 0.01) and P. geniculatus signifi cant decrease in the transmission of Trypanosoma cruzi, (141♂, 101♀; p = 0.01). The number of males and females in as demonstrated by the low prevalence of the disease observed T. pseudomaculata was not statistically signifi cantly different in surveys performed among schoolchildren in the 2000s(8).

503 Rev Soc Bras Med Trop 49(4):502-507, July-August, 2016

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504 Dias JVL et al. - Triatomines in Northeast Minas Gerais PD OP PD OP NI Total infection (%) Positives TABLE 1 TABLE Examined trypanosome presence from October 2001 to December 2008. Captured Captured NI: no information. ; OP: other places; adults 453 1,776 45 32 255 1,601 44 22 7 1,601 77 23 19 - - - 1.19 1,957 45 32 255 10 - - 1.35 2.75 - 1,776 81 27 adults 134 - 2,087 453 - 0.51 - 151 nymphs - 0.46 NI 18 23 7 1,015 10 - - 0.99 - 2 - 1 23 25 2 adults 168 - - 1 - - 1.39 4.17 - - - 1,143 - - 981 - 1,586 - 43 - 234 nymphs 142 757 728 25 NI 77 41 2 1 - 9 - - 4 ------adults 3 15 1 105 1 - 3 15 38 - - 111 - 2.63 984 - 44 nymphs 124 0.62 7 - 4.00 9.09 3.65 27 1.19 128 5.63 621 82 21 adults 87 94 13 21 236 69 82 58 6 13 nymphs 2 2 16 2 10 13 3.53 2 2 10 - 9 3 - 7.69 4.35 - - NI - 2 1 2.44 - 9.52 5.75 9.12 - - 11.63 5 - 7.69 10.98 - 2 - - - - 13 9.34 1 - - 2 9 11 - - - adults 29 3 20 60 - - 1 242 - 15.00 2 - 1 6 - 2 1 7 - 28 35 - - nymphs ------2 - - 6 NI 17 5 4 13 - 1 - - - - adults - - 91 - - - - adults 40 13 - - - 3 4 - nymphs - - - 4 - - - - 13 5 - 1 1 adults - 1 1 ------7.69 - - adults - 5.26 - - 1 ------199 291 126 5,632 61 2,148 3 246 439 2.45 4.47 1.51 6,399 13 1.08 5.87 4,101 NI ID OP PD NI PD OP NI ID OP ID ID PD PD: peridomicile Number of triatomines captured in municipalities Diamantina Regional Health Superintendence according to species, evolutionary stage, place capture, and Triatoma sordida sordida Triatoma megistus Panstrongylus vitticeps Triatoma pseudomaculata Triatoma geniculatus Panstrongylus diasi Panstrongylus Rhodnius neglectus arthurneivai Triatoma Rhodnius domesticus Total ID: intradomicile; Species

505 Rev Soc Bras Med Trop 49(4):502-507, July-August, 2016

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FIGURE 2. Seasonal distribution of nymphs and adults of Panstrongylus megistus (A), Triatoma sordida (B) and Triatoma vitticeps (C) in municipalities of Diamantina Regional Health Superintendence, from October 2001 to December 2008, and monthly mean compensated temperature and monthly mean precipitation (D) of meteorological stations located in the DRHS region. DRHS: Diamantina Regional Health Superintendence.

The presence of P. megistus in domiciles of all the municipalities due to the ornithophilic feeding of these vectors, as indicated may be related to the conservation of this insect’s natural ecotopes by the predominance of specimens in the henhouses. in vestiges of humid forests, mainly gallery forests. Adults seem Triatoma vitticeps was observed throughout almost all the to disperse from there by ﬂ ight during the warmest and most municipalities of the region predominantly in its adult form in the humid periods of the year, as observed in municipalities of the intradomicile, thus corroborating other studies(12) (13). Such distribution midwestern part of Minas Gerais ( )(9). In that region, Figure 2D can be related to its low capability to colonize domiciles, although 22.5% of 416 P. megistus specimens had ingested human blood the presence of nymphs in domiciles suggests that the species has and 3.8% of specimens were positive for trypanosomatids, a potential for colonizing artiﬁ cial environments. Moreover, the thus surpassing the percentage reported herein (2.7%)(10). species showed a high index of infection by trypanosomatids, It is noteworthy that a high proportion of nymphs infected indicating its trophic relationship with different reservoirs of by trypanosomatids was captured inside the houses of the DRHS Trypanosoma cruzi(12). Thus, this triatomine can introduce the region (4.2%), indicating a possible intradomiciliar cycle of parasite in the domiciliary environment during its dispersion. Trypanosoma cruzi probably involving men and domestic animals as synanthropic reservoirs. Geographically, Triatoma vitticeps is associated with humid areas, and its egg hatching is dramatically affected by humidity Triatoma sordida is currently the most captured species in lower than 52%(13). The correlation between the number of Brazil(2), with peridomiciliary habit and notable ornithophilic adults and the months with higher precipitation observed herein behavior that favors the establishment of great colonies in outbuildings, especially in henhouses, where re-infestations suggest that adults disperse during this period to guarantee the often occur despite constant intervention(11). In the DRHS region, oviposition and the success of the hatching. the species comprised 41.6% of the specimens captured, with It is noteworthy that all species, except P. megistus and only 0.9% infected by trypanosomatids. These results may be T. sordida, were more dispersed throughout the region during

506 Dias JVL et al. - Triatomines in Northeast Minas Gerais the studied period than between 1975 and 1982, when the CDCP 2. Silveira AC, Dias JCP. O controle da transmissão vetorial. Rev Soc activities were more intense(7). This fact may be associated Bras Med Trop 2011; 44 (supl II):52-63. to environmental (deforestation, urban expansion) and social 3. Mendonça KFC, Ribeiro EM, Galizoni FM, Augusto HA. Formação, (migration, electrifi cation of rural domiciles) changes that sucessão e migração: trajetórias de duas gerações de agricultores do occurred in the area, as observed for T. pseudomaculata in a Alto Jequitinhonha, Minas Gerais. R Bras Est Pop 2013; 30:445-463. municipality of this region, where the presence of the species 4. Dias JCP. Vigilância epidemiológica em doença de Chagas. seems to be related to the changes in primary land coverage Cad Saude Publica 2000; 16 (supl II):43-59. and aridifi cation(14). 5. Instituto Brasileiro de Geografi a e Estatística (IBGE). Censo Despite their preference for wild habitat, reports of demográfi co 2010. Available from: http://www.ibge.gov.br/home/ estatistica/populacao/censo2010/tabelas_pdf/Minas_gerais.pdf. R. neglectus, P. diasi, and P. geniculatus in domiciliary Accessado em Janeiro 14, 2013. environments have increased, the last even being involved (2) (15) 6. Camargo ME, Silva GR, Castilho EA, Silveira AC. Inquérito in the transmission of Trypanosoma cruzi to humans . sorológico da prevalência da infecção chagásica no Brasil, Triatoma arthurneivai is a species rarely found in domestic and 1975/1980. Rev Inst Med Trop São Paulo 1984; 26:192-204. sylvatic environments and its reports are restricted to Southern (15) 7. Silveira AC, Feitosa VR, Borges R. Distribuição de triatomíneos Espinhaço Mountain Range . The fi ndings of P. tertius and capturados no ambiente domiciliar, no período 1975/83, Brasil. R. domesticus in domiciles are sporadic and probably do not Rev Bras Malariol D Trop 1984; 36:15-312. indicate changes in species behavior. 8. Luquetti AO, Passos ADC, Silveira AC, Ferreira AW, Macedo V, The changes in landscape in Jequitinhonha Valley region in Prata AR. O inquérito nacional de soroprevalência de avaliação do the last decades caused by the establishment of great pastures controle da doença de Chagas no Brasil (2001-2008). Rev Soc Bras and coffee and eucalyptus plantations will likely promote Med Trop 2011; 44 (supl II): 108-121. the dispersal of some triatomine bugs into the man-made 9. Villela MM, Souza JB, Mello VP, Azeredo BVM, Dias JCP. environments and the colonization of domiciliary structures. Vigilância entomológica da doença de Chagas na região centro- The periodic fi ndings of P. megistus and Triatoma sordida, oeste de Minas Gerais, Brasil, entre os anos de 2000 e 2003. Cad Saude Publica 2005; 21:878-886. as well as species considered secondary in the transmission of Trypanosoma cruzi, reflect the need for a sustainable 10. Villela MM, Rodrigues VLCC, Casanova C, Dias JCP. Análise da fonte alimentar de Panstrongylus megistus (Hemiptera, surveillance of these species in DRHS municipalities. Reduviidae, Triatominae) e sua atual importância como vetor do Trypanosoma cruzi, no Estado de Minas Gerais. Rev Soc Bras Med Trop 2010; 43:125-128. Acknowledgements 11. Pires HHR, Borges EC, Andrade RE, Lorosa ES, Diotaiuti L. The authors would like to thank Iderson Teixeira and Mayara Viotti for their Peridomiciliary infestation with Triatoma sordida Stal, 1859 in the support in data digitization. county of Serra do Ramalho, Bahia, Brazil. Mem Inst Oswaldo Cruz 1999; 94:147-149.

Confl ict of Interest 12. Gonçalves TCM, Rocha DS, Cunha RA. Feeding patterns of Triatoma vitticeps in the State of Rio de Janeiro, Brazil. Rev Saude The authors declare that there is no confl ict of interest. Publ 2000; 34:348-352. 13. Souza RCM, Diotaiuti L, Lorenzo MG, Gorla DE. Analysis of the Financial Support geographical distribution of Triatoma vitticeps (Stål, 1859) based on data of species occurrence in Minas Gerais, Brazil. Infect Genet This study was funded by Fundação de Amparo à Pesquisa do Estado de Evol 2010; 10:720-726. Minas Gerais (FAPEMIG), Conselho Nacional de Desenvolvimento Científi co 14. Assis GFM, Azeredo BVM, Gorla D, Diotaiuti L, Lana M. e Tecnológico (CNPq), and Fundação Oswaldo Cruz (FIOCRUZ). Entomological surveillance of Chagas disease in Berilo municipality, Jequitinhonha Valley, Minas Gerais, Brazil. Rev Soc Bras Med Trop 2009; 42:615-621. REFERENCES 15. Dias JVL, Queiroz DRM, Martins HR, Gorla DE, Pires HHR, 1. Galvão C, Paula AS. Sistemática e evolução dos vetores. In: Galvão Diotaiuti L. Spatial distribution of triatomines in domiciles of an C, organizador. Vetores da Doença de Chagas no Brasil. Curitiba: urban area of the Brazilian Southeast Region. Mem Inst Oswaldo Sociedade Brasileira de Zoologia; 2014. p. 26-32. Cruz 2016; 111:43-50.

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