Triatomines in the city: A study of Rhodnius neglectus in Jaboticabal, São Paulo, Brazil, and its epidemiological implications

ABSTRACT

Background:  Chagas disease, a significant global health concern rooted in social inequalities and political oversights, remains a challenging public health issue impacting millions worldwide. The increasing detection of triatomines, the vectors of Chagas disease, in urban areas complicates the situation.

Methods:  This study investigated the incidence of Rhodnius neglectus in the urban areas of Jaboticabal, São Paulo, Brazil, following several reports and previous collections of triatomines in the city. An educational approach was adopted, distributing informational materials and engaging the community through social networks to generate notifications that would enable the identification of triatomines. Specimens were collected using various methods, including passive surveillance actions, light traps, and active searches in palm trees.

Results:  Rhodnius neglectus was found in urban areas, invading homes in Jaboticabal, and was identified in palm trees. The educational approach led to the collection of 93 triatomines. Colonization was observed in a residence, with eggs, nymphs, and a concerning record of blood-feeding on a resident child. The houses where specimens were captured often had nearby palm trees with birds and nests, facilitating the passive transport of these insects and increasing the risk of invasion due to light attraction. No triatomines infected with Trypanosoma cruzi were identified.

Conclusions:  These findings emphasize the need for preventive measures to reduce the prevalence of R. neglectus in urban environments. The data elucidate the occurrence of R. neglectus in the city of Jaboticabal, associated with its potential behavioral adaptation in urban environments, underscoring the need for innovative control strategies.

Keywords: Chagas disease; Urbanization; Urban vectors; Vector control; Triatominae

INTRODUCTION

Chagas disease is a global health problem deeply rooted in social inequalities and political negligence^1-3. Its etiological agent, the hemoflagellate protozoan Trypanosoma cruzi (Chagas, 1909), is primarily transmitted through contact with the feces or urine of infected triatomine bugs^4-7. Endemic to 21 Latin American countries, the disease has also been reported in other regions of the world⁸.

The interaction between triatomines, trypanosomatids, and humans in the Americas dates back to the pre-Columbian period, with evidence of T. cruzi infection dating back 9,000 years^9,10. Despite this long history, it is only in recent decades that control initiatives have managed to reduce the incidence of this disease¹¹. It is estimated that 6-7 million people are infected worldwide, with thousands living in high-risk areas³. Triatominae, a subfamily of Reduviidae¹², encompasses 159 species^13-16, most of which are naturally found in wild environments and exclusively participate in the natural infection cycle⁵; however, some species have adapted to urban settings^17,18.

In Brazil, Chagas disease has spread alongside migration, particularly during the European colonization of the country's interior in recent centuries. Rapid environmental changes caused by deforestation and agricultural expansion have led to the adaptation of triatomines, vectors of the disease, to artificial environments, such as human dwellings, thereby increasing contact with humans and the risk of disease transmission¹⁸.

An example of this dynamic is the colonization of urban areas in the Metropolitan District of Caracas, where occasional outbreaks of foodborne transmission occur¹⁹. Active transmission, although less significant, was also observed, mainly by species such as Panstrongylus geniculatus (Latreille, 1811), found in domestic areas. Other species collected from these areas included Triatoma nigromaculata (Stål 1859), Triatoma maculata (Erichson, 1848), Rhodnius prolixus Stål 1859, and Panstrongylus rufotuberculatus Stål 1859¹⁹. This study highlights the transmission interface between wild and urban environments and suggests that although direct transmission to humans is limited, the cumulative risk in a large population warrants further research and preventive measures²⁰.

Comprehensive niche modeling and mapping of potential distributions of members of the T. brasiliensis complex revealed that T. b. brasiliensis Neiva, 1911 has the greatest potential to colonize new areas²¹. Although model projections do not anticipate many changes in the complex's distribution due to climate change, the epidemiological importance and dispersal abilities of the members of the complex are critical for understanding human exposure patterns²¹. This suggests that as habitable areas expand due to climate change, new infestations may occur, primarily from wild areas to urban environments²⁰.

In São Paulo, Brazil, the primary vector for Chagas disease historically was Triatoma infestans (Klug, 1834), likely introduced in the 18th century. However, successful control measures targeting this species have led to the emergence of other relevant vectors, such as Triatoma sordida (Stål, 1859), Panstrongylus tibiamaculatus (Pinto, 1926), Panstrongylus megistus (Burmeister, 1835), and Rhodnius neglectus Lent, 1954²². The increasing detection of triatomines in urban areas, with an emphasis on secondary species, raises questions regarding the ability of these vectors to occupy ecological niches traditionally dominated by primary species²³. This species replacement may indicate the greater ecological and adaptive plasticity of secondary species, allowing them to explore new habitats and food resources in urban environments²³. Secondary species may exhibit different behavioral patterns, susceptibility to insecticides, and interactions with hosts compared to primary species, requiring specific management approaches²⁴.

Between 2013 and 2017, in the state of São Paulo-Brazil’s most populous and developed state (IBGE, 2023)-over 15,000 triatomine bugs were captured across 456 municipalities, encompassing 70% of the state’s territory²². The noteworthy species for entomological surveillance in the state include P. megistus, which has a high infection rate and the ability to colonize households; T. sordida, typically found near homes with lower T. cruzi infection rates; and R. neglectus, which is concentrated in the São Paulo Plateau, with a high capture rate in urban areas²².

Rhodnius neglectus, described by Herman Lent in 1954, is found in 14 Brazilian states and in the Federal District, where it harbors T. cruzi^25-27. This triatomine prefers to feed on birds, though it also feeds on mammals, including humans²⁸. Despite their ability to fly, these insects are typically attracted to artificial light sources and move on foot in search of food⁵. Although the rate of T. cruzi infection is normally low in R. neglectus captured in artificial environment^22,29, the presence of infection in such settings remains noteworthy. R. neglectus has already been found to have an infection rate of 15.9%³⁰.

The presence of triatomines in urban areas poses a significant challenge to Chagas disease control, requiring a comprehensive approach that integrates entomological surveillance with the One Health principles^31-33. The adaptation of these vectors to urban environments, including domiciliation and blood-feeding behavior in humans, highlights the urgency of monitoring and control actions. Active surveillance-through searches, traps, and community engagement-is crucial for assessing population density, T. cruzi infection, and the presence of triatomines in urban areas, enabling the identification of at-risk areas and the implementation of targeted control measures³⁴.

Integrating data on vector distribution, T. cruzi infection, and environmental factors influencing disease transmission is essential for developing more effective control strategies and promoting the health of affected communities³⁵. In this context, the present study investigated the incidence of R. neglectus in the municipality of Jaboticabal, São Paulo, Brazil, including a description of its domiciliation and blood-feeding behavior in humans, with the aim of contributing to the understanding of Chagas disease dynamics in urban areas and supporting control actions^25,26_.

METHODS

● Geographical position and features of the study region

Jaboticabal is a municipality located in the State of São Paulo, covering a total area of 706,602 km² (or 70,660 ha) (Figure 1). As of 2021, it sustains a population of 71,821 individuals, according to data from the Brazilian Institute of Geography and Statistics (IBGE)³⁶. Situated within the metropolitan region of Ribeirão Preto, Jaboticabal has a tropical climate, characterized by mild temperatures and distinct wet and dry seasons³⁶. This region is part of the Cerrado biome, renowned for its savanna-like landscape and rich biodiversity³⁷. This environment is particularly valuable for studying R. neglectus in urban areas due to its ecological resemblance to the primary distribution areas of R. neglectus²⁵, making it an ideal model for research.

FIGURE 1:
Map of the State of São Paulo (A) with emphasis on the municipality of Jaboticabal, highlighting the area of notifications and records of R. neglectus (B). Collection points (C).

● Development of educational materials

To capture the triatomines, an awareness-raising strategy was implemented, involving the distribution of informational materials to residents of the study area, health professionals, and surveillance agents. The educational material, presented in the form of a banner, contained comprehensive information on Chagas disease, including epidemiological data, pathogenesis of the disease, clinical manifestations, guidelines for prevention and treatment, as well as the description of the vectors, their feeding habits, life cycle, and how to capture and store them. This banner was presented to community health and endemic agents, as well as to the general population through social media. Additionally, messaging applications were used to disseminate information and encourage community participation. The purpose of this material was not only to raise awareness but also to empower residents to identify potential triatomines and understand the disease cycle, fostering their active participation in surveillance efforts. The material was disseminated in health centers and through social media platforms.

● Strategy for Triatominae collection

After initially contacting the residents and obtaining preliminary information, the research team, supported by the Vector and Zoonoses Surveillance Department of the Municipality of Jaboticabal, proceeded to their homes to conduct active searches for triatomines. Light traps were installed in areas where no traces of the species were found. All information and reports provided by the residents were documented and stored. Homes where the specimens were found were inspected in detail, and residents were advised to contact local health authorities for a full risk assessment.

Specimens were collected using active methods, such as active searches and light traps, and traps based on the model proposed by Calor and Mariano³⁸. Additionally, palm trees in the vicinity of residences were scrutinized using cranes, with specimens manually collected when necessary. The team systematically gathered essential data, including detailed photographic records and georeferenced locations, which provided valuable insights. Before installing traps in residences, property owners were diligently informed, and their consent was obtained through the completion of an Informed Consent Form (Supplementary material 1). The specimens captured were categorized by type of environment, stage of development, and physiological condition (e.g., regurgitated, alive, or dead). It is important to note that the local government did not directly participate in the study, however, one of the authors, responsible for vector and zoonoses surveillance in the municipality of Jaboticabal, provided support and authorization for the field activities. This study received no financial support from local government for the research³².

● Analysis of natural infection and isolation of T. cruzi in triatomines

The investigation of natural infection by T. cruzi was carried out at the Parasitology Laboratory of the Universidade Estadual Paulista (UNESP), Faculdade de Ciências Farmacêuticas, Araraquara, SP, Brazil. The adopted technique involved examining the intestinal contents of the collected specimens under an optical microscope. The insect feces were accessed by abdominal compression, deposited on slides, diluted in phosphate-buffered saline, and covered with a coverslip for observation according to the methodology described by Ribeiro et al.³¹.

● Triatominae identification

After investigating natural infection by T. cruzi, live and dead specimens were preserved in absolute alcohol and stored at -80°C in the Laboratory of Virology at Universidade Estadual Paulista (UNESP), Faculdade de Ciências Agrárias e Veterinárias, Jaboticabal, SP. Later, they were transferred to the Parasitology Laboratory of the Universidade Estadual Paulista (UNESP), Faculdade de Ciências Farmacêuticas, Araraquara, SP, Brazil, where they were permanently stored in the laboratory's collection and identified using the key provided by Galvão²⁸. To describe the morphology, the specimens were photographed using a Leica M205 stereo microscope and Leica Application Suite X (RRID:SCR_013673) image analysis system. Subsequently, image boards were created using image editing software to compare and describe the structures. For morphological studies, the pygophores were first removed from the abdomen using forceps and then cleaned in a 20% NaOH solution for 24 h. The dissected male and female genital structures were observed and photographed in glycerol using a Leica M205 stereoscopic microscope and Leica Application Suite X (RRID:SCR_013673), following the procedure described by Oliveira et al.³⁹. The insects were examined dorsally, and the dissected male and female genitalia were evaluated. Observations and identification were performed as described by Oliveira et al.⁴⁰ to confirm the species (Figure 2).

FIGURE 2:
Female Rhodnius neglectus (A) Dorsal view. (B) Detail of the connexivum. (C) Male genitalia parameters. (D) Male pygophore median process. (E) Dorsal view of the female external genitalia. (F) Ventral view of the female external genitalia. These features contribute to the entomological identification of R. neglectus.

RESULTS

In accordance with our objectives, we present the results of this study. The primary objective was to improve public awareness and education on triatomine recognition while investigating their distribution in urban areas with increasing reports of invasions. We implemented several strategies, including disseminating information through newsletters, conducting interactive lectures, displaying banners, and establishing communication channels via popular messaging apps and social networks in the region. These efforts have resulted in significant advancements in the collection and identification of R. neglectus specimens, thereby elucidating their prevalence in the urban environments of Jaboticabal.

Collections conducted across different neighborhoods of Jaboticabal between August 21, 2019, and September 6, 2023, revealed the presence of R. neglectus in urban environments. The captured specimens were categorized and summarized as shown in Table 1. The following methods were employed for collecting insects: Passive Surveillance Action (PSA) with 22 collections, Light Trap with 3 collections, and Active Search (AS) with 2 collections. PSA was the most frequently used method, followed by light traps and AS, with AS being employed in significant collections, such as on October 1, 2019, when 42 live specimens were captured through an active search in palm trees (Table 1).

TABLE 1:
Information regarding address, date, location, ecotypes, physiological condition and quantity of triatomines collected in the Municipality of Jaboticabal, São Paulo.

Neighborhood	Collection date	Type of ecotope	Physiological Condition	Method of collection	number
Jardim Santa Rita	08/21/2019	intradomiciliary	Dead	PSA	2
Jardim Santa Rita	08/29/2019	peridomiciliary	Alive	light trap	2
Jardim Santa Rita	08/30/2019	intradomiciliary	Alive	PSA	2
Jardim Santa Rita	09/05/2019	intradomiciliary	Alive	PSA	1
Jardim Santa Rita	09/07/2019	intradomiciliary	Alive	PSA	1
Nova Jaboticabal	09/10/2019	intradomiciliary	Alive	PSA	1
Jardim Santa Rita	09/14/2019	peridomiciliary	Alive	light trap	1
Jardim Santa Rita	09/14/2019	peridomiciliary	Alive	light trap	1
Jardim Santa Rita	09/16/2019	intradomiciliary	Alive	PSA	1
Jardim Santa Rita	09/17/2019	intradomiciliary	Alive	PSA	1
Jardim Tangará	09/18/2019	peridomiciliary	Alive	PSA	1
Jardim São Marcos II	09/19/2019	intradomiciliary	Alive	PSA	1
Jardim Santa Rita	09/21/2019	intradomiciliary	Dead	PSA	1
Centro	09/21/2019	intradomiciliary	Dead	PSA	1
Jardim Santa Rita	09/26/2019	intradomiciliary	Alive	PSA	1
Nova Jaboticabal	09/26/2019	peridomiciliary	Dead	PSA	1
Jardim Santa Rita	09/28/2019	intradomiciliary	Alive	PSA	1
Nova Jaboticabal	09/30/2019	intradomiciliary	Alive	PSA	1
Colina Verde	09/30/2019	peridomiciliary	Alive	PSA	1
Jardim Santa Rita	09/30/2019	peridomiciliary	Alive	AS	16*
Jardim Santa Rita	10/01/2019	peridomiciliary	Alive	AS	42*
Jardim Tangará	10/09/2019	intradomiciliary	Alive	PSA	1
Jardim Santa Rita	10/09/2019	intradomiciliary	Dead	PSA	1
Jardim Santa Rita	10/09/2019	intradomiciliary	Dead	PSA	1
Nova Jaboticabal	10/10/2019	intradomiciliary	Dead	PSA	1
Jardim Santa Rita	10/14/2019	intradomiciliary	Alive	PSA	2
Jardim Santa Rita	10/15/2019	intradomiciliary	Dead	PSA	1
Jardim Santa Rita	10/18/2019	intradomiciliary	Dead	PSA	1
Jardim São Marcos	12/30/2019	intradomiciliary	Dead	PSA	1
Jardim Eldorado	09/06/2023	intradomiciliary	Alive	PSA	4
Total					93

• *Collection carried out through active search in palm trees. PSA: passive surveillance action; AS: active search. Numbers in bold represent invasions.

The number of insects collected varied according to location and collection method. Collections were performed in both intradomiciliary and peridomiciliary ecotopes. The majority of R. neglectus specimens were found in intradomiciliary environments, indicating a substantial presence within residences (Table 1). A total of 93 specimens were collected from seven neighborhoods in Jaboticabal based on 24 notifications from the population, with the highest single collection yielding 42 specimens (Jardim Santa Rita, October 1, 2019, AS method). Most captured insects were alive, suggesting their adaptability to urban environments. In total, 21 collections were conducted in intradomiciliary settings, while 9 occurred in peridomiciliary settings.

During the study period, multiple collections of R. neglectus across different neighborhoods of Jaboticabal revealed varying indices of the incidence of these insects in urban environments. Jardim Santa Rita neighborhood had the highest number of collections, with a total of 15 events, representing a significant infestation focus. Significantly, collections conducted on September 30 and October 1, 2019, using the AS method on palm trees, resulted in the capture of 16 and 42 live insects, respectively, indicating a high population density.

The Nova Jaboticabal neighborhood has four collections distributed between intradomiciliary and peridomiciliary environments, with a predominance of live insects. In Jardim Tangará, two intra-domiciliary collections were conducted, resulting in the capture of live insects. Jardim São Marcos II and Jardim São Marcos were collection points, each contributing to one live insect capture event. In Centro, two intradomiciliary collections captured dead insects. Finally, in Colina Verde, a peridomiciliary collection resulted in the capture of one live insect, whereas the most recent collection in Jardim Eldorado on September 6, 2023, resulted in the capture of four live insects in an intradomiciliary environment. These data indicate variability in the distribution and density of R. neglectus across different neighborhoods of Jaboticabal, with a notable presence in Jardim Santa Rita and a lower but significant incidence in other neighborhoods. The concentration of collections and the number of specimens captured suggest the need for specific control measures for each neighborhood, with a particular focus on areas with a higher vector population density.

Despite informal records of triatomine sightings, information about their biology and ecotopes remains scarce, even in ecologically favorable contexts. The present study addresses this knowledge gap, with active capture proving to be the most effective method, resulting in the capture of 58 live specimens (Table 1). Moreover, most live specimens were found on palm trees near residential areas. The presence of palm trees and birds near houses inadvertently creates a favorable environment for the vector to settle inside, corroborating the results of previous studies on triatomines.

Collections synchronized with palm tree pruning in Jardim Tangará (21°16'14.2"S, 48°18'36.2"W) and subsequent collection in Jardim Santa Rita (21°15'33.1"S, 48°18'35.4"W) revealed a notable prevalence of R. neglectus associated with palm trees, particularly the Jerivá palm (Syagrus romanzoffiana) and the Carnaúba palm (Copernicia prunifera), harboring a total of 16 specimens (Figure 3). These findings highlight the ecological importance of palm habitats for the abundance and distribution of triatomine vectors, particularly R. neglectus. Additionally, our records highlight the abundant presence of palm trees in landscaped corridors in the reported neighborhoods, emphasizing their potential roles as breeding sites and preservation areas for these vectors. For example, the palm trees identified were exotic to the Cerrado of São Paulo, primarily for landscaping purposes.

FIGURE 3:
A. Palm tree where triatomine specimens were found. B, C, and D. Record of the high number of palm trees in the collection areas, highlighting the prevalence of these plants near residences.

In the Jardim Eldorado neighborhood in September 2023. During a home visit, an adult female triatomine was found in the bedroom of the youngest child along with fertile eggs and nymphs (Figure 4). This discovery prompted medical follow-up of the family, and subsequent tests did not indicate infection (Figure 5).

FIGURE 4:
Record of the domiciliation of R. neglectus in a residence located in a middle-class neighborhood in Jaboticabal. (A) and (C) depict adults; (B) shows a nymph of R. neglectus; (D) and (E) show eggs and eggshells adhered to the bed.

FIGURE 5:
Record of a child residing in the house where R. neglectus is domiciled and had a blood meal. (A) General view of the bite region and the inflammatory process in the skin. (B) Highlight of the bite region.

The investigation of natural infection by T. cruzi was carried out at the Parasitology Laboratory of the Universidade Estadual Paulista (UNESP), Faculdade de Ciências Farmacêuticas, Araraquara, SP, Brazil. The intestinal contents of the insects were examined under an optical microscope. Insect feces were observed, and no protozoan forms were found.

Although we did not directly test the impact of our communication strategies, we observed a substantial improvement in the rate of positive notifications. This was likely due to the increased ability of the population to identify triatomines, their eggs, or traces, such as feces, which, in turn, allowed for faster confirmation of reports through collection and identification. This finding highlights the crucial role of community awareness in effective vector surveillance and control. Active community engagement further fosters a collaborative approach to disease prevention and control, instilling a sense of shared responsibility among residents. By fostering a culture of vigilance and encouraging prompt reporting of potential vector sightings, community members have become key partners in ongoing efforts to mitigate vector-borne diseases.

DISCUSSION

Vector-borne diseases, including Chagas disease, pose significant challenges to public health worldwide, affecting millions of people across various regions. Despite their widespread prevalence, a substantial gap remains in understanding the key aspects of these diseases, such as the transmission dynamics of understudied species, vectorial capacity, and the role of coinfections, particularly in urban areas³⁰. This scoping study aimed to address these gaps by providing effective communication channels and assessing the incidence of R. neglectus infections in Jaboticabal.

The study assessed the regional importance of disseminating information to health care professionals, surveillance services, and the general public. The aim was to provide a better understanding of the incidence and distribution of vectors of neglected diseases, along with their associated health risks⁴¹. It is widely recognized that education plays a crucial role in combating neglected diseases; however, the public's awareness and involvement in entomological control and surveillance efforts remain variable. Studies underscore how gaps in public knowledge can significantly hinder the effectiveness of control strategies^42-44.

Recent studies have shown that current technological resources, such as apps and the Internet, play crucial roles in advancing vector control strategies. For instance, the VetorDex application suite (https://play.google.com/store/apps/details?id=vetordex.com&hl=pt_BR) exemplifies innovative approaches aligned with current vector control objectives. TriatoDex⁴⁵, a part of this suite, provides specialized tools for identifying various triatomine species through interactive features and detailed imagery to simplify the identification process and empower users to make informed decisions. These integrated technological solutions in public health initiatives can significantly enhance the precision and efficiency of vector surveillance and control, thereby strengthening disease prevention strategies.

Rhodnius spp., known for their preference for palm trees, establish close links with these trees and use them as shelters and for access to food sources^5,28. While typically found in the nests of wild birds and palm trees, especially in the Cerrado biome⁵, R. neglectus is becoming increasingly common in urban areas^17,25,26. Triatomines feed on various sources, including birds, amphibians, mammals, and reptiles⁴⁶; however, birds have not been previously considered hosts of T. cruzi^47-49. Recent studies have challenged this perspective, suggesting that birds may serve as reservoirs of this parasite. For the first time, researchers have documented the presence of protozoan forms in wild birds, as reported by⁵⁰. Protozoa found in wild birds, as documented by Martínez-Hernández et al.⁵¹, are particularly relevant in this context because the genus Rhodnius is closely related to birds. These birds not only provide food for insect vectors but also facilitate the passive transportation of these insects into homes.

The close association between Rhodnius spp. and birds underscores the potential role of avian species in the transmission dynamics of T. cruzi. This ecological relationship highlights the need for comprehensive surveillance and control measures targeting both vector habitats and potential reservoirs to effectively mitigate the risk of Chagas disease transmission in both wild and urban environments. Understanding and addressing these complexities are crucial for developing integrated strategies to manage and reduce the burden of this neglected tropical disease.

Observations by Diotaiuti and Dias⁵² suggest that population density in the natural habitat of R. neglectus may correlate with food availability and the presence of predators. Despite a 15.9% infection rate of T. cruzi, primarily from marsupials, indicating R. neglectus is a significant sylvatic vector, this study found no evidence supporting R. neglectus as a direct transmitter of T. cruzi to humans in this area. These insights underscore the need for integrated surveillance and control strategies targeting both vector habitats and potential reservoirs to effectively manage Chagas disease transmission across diverse environments.

In urban environments, where palm trees and bromeliads are often used for landscaping, these plants play a crucial role in maintaining the enzootic cycle of T. cruzi by providing shelter and food for triatomines, mainly Rhodnius species⁵³. This study identified colonies of R. neglectus on palm trees, with 42 specimens found in Syagrus romanzoffiana (Jerivá palm) and 16 specimens from Copernicia prunifera (Carnaúba palm). Effective management of landscaped palm trees and continuous monitoring are essential to mitigate the risk of vector-borne diseases. The regular inspection and maintenance of these plants can aid in the early detection and control of Rhodnius populations, thereby reducing their potential for disease transmission.

Recently, Carbajal-del-Fuente et al.¹⁸ highlighted a significant increase in records of vectors in urban homes over the last three decades. This infestation covers cities of various sizes, from small towns to megalopolises, across the Americas, from Argentina to the United States¹⁸. In São Paulo state, some municipalities showed an increase in the capture of triatomines, such as the study in Araçatuba, municipality of São Paulo, in 2009, which collected 81 specimens of R. neglectus from human dwellings, with 2.7% of the samples indicating the presence of human blood, suggesting the possibility of transmission of the disease²⁶. In addition, triatomine specimens were collected in the capital of São Paulo, the most developed region in Brazil^31,32.

This increase in the detection of triatomines in urban areas, including secondary species such as R. neglectus, raises concerns about the adaptation of these vectors to new environments and the potential expansion of their geographical distribution¹⁸. Global warming, with rising temperatures and changing rainfall patterns, may contribute to this expansion, creating more favorable conditions for the survival and reproduction of triatomines in previously inhospitable regions.

The integration of technological innovation into health control programs, along with active community involvement and interdisciplinary collaboration, has facilitated the successful implementation of these strategies. This provides tangible benefits to the community and empowers individuals to report the presence of kissing bugs in their homes. The results underscore the crucial role of information channels, such as social networks and accessible messaging apps, in health-related contexts and Chagas disease control, even under less representative conditions. This successful approach has been replicated in other regions such as Guatemala, where a similar strategy yielded significant results in an area exposed to vectors such as Triatoma dimidiata Latreille, 1811⁴¹.

Although triatomines are typically found in socially disadvantaged areas, our results indicate a different trend⁴¹. The collections were conducted in socially developed regions, which can be characterized as middle-to high-class neighborhoods. This finding is consistent with the results of studies involving the same species in four municipalities in São Paulo²². Based on the available information, it is possible to speculate that there was a shift in the behavior of the kissing bugs. These findings indicate a worrisome trend of increasing triatomine presence in urban areas, even in developed regions, underscoring the importance of stringent vector control in preventing Chagas disease. This adaptation process is heavily influenced by human interactions and pressures, necessitating the adaptation and strengthening of vector control programs to address the shift from rural to urban environments.

The presence of vectors in urban areas poses additional challenges for Chagas disease prevention and control, highlighting the importance of ongoing surveillance and intervention. Considering these challenges, the integration of community awareness and educational initiatives with systematic specimen collection and surveillance is imperative. By empowering communities with knowledge about triatomine recognition and control measures, coupled with regular specimen collection and reporting, we can enhance early detection and response efforts, ultimately mitigating the spread of Chagas disease in urban settings.

CONCLUSION

In this study, which addressed the presence of R. neglectus in a middle-class area of Jaboticabal, São Paulo, we highlight the importance of disseminating information among health professionals, surveillance services, and the general community was to understand the distribution of the vectors of neglected diseases and their associated risks. Raising public awareness played a fundamental role, using communication channels, such as social networks and messaging applications, which allowed for a better understanding of the presence of vectors in urban areas. The results also showed changes in the behavior of R. neglectus as well as its association with palm trees and birds. Consequently, it is necessary to consider these factors when developing strategies for Chagas disease control and prevention. The findings of this study underscore the need for proactive measures to address vector-borne diseases and emphasize the importance of community involvement in surveillance and control efforts. By leveraging existing communication platforms and fostering collaboration among various stakeholders, including health authorities, researchers, and residents, it is possible to enhance vector surveillance and mitigate the risk of disease transmission. However, it is important to note that, although occasional notifications from the population living in areas infested by triatomines are valuable for surveillance, they are not sufficient for effective vector control. It is essential that notifications are followed by active search actions, chemical treatment, and environmental management, in addition to continuous educational campaigns, to ensure community participation and reduce the risk of Chagas disease transmission. Continued research and vigilance are essential to monitor vector populations, identify emerging threats, and implement targeted interventions to protect public health. Through concerted efforts and community engagement, we can work towards effectively combating vector-borne diseases and safeguarding the well-being of populations in urban areas.

ACKNOWLEDGMENTS

The authors extend their sincere appreciation to Daniel Fernandes Cavalcanti and his family for providing extensive support concerning the region and municipality. Our deep gratitude to Dr. Rinaldo Niero, associate professor and retired from the Faculty of Public Health/USP, for his support. Special thanks to everyone who directly and indirectly assisted Isabella Maxwell during the research. Appreciation to the São Paulo Research Foundation (FAPESP) for funding the researchers Jociel Klleyton Santos Santana (process 23/00423-0), Jader de Oliveira (process 19/02145-2), Vinícius Fernandes de Paiva (process 2023/09822-5) and Tiago Belintani (process 23/15240-9). We would also like to thank CNPq, process 317 358/2021-9, for the research productivity grant (PQ - 1D) granted to João Aristeu da Rosa.

REFERENCES

• ¹ Dias JCP, Silveira AC, Schofield CJ. The impact of Chagas disease control in Latin America - a review. Mem Inst Oswaldo Cruz. 2002;97(5):603-12.
• ² Dias JCP. Evolution of Chagas Disease Screening Programs and Control Programs Historical Perspective. Glob Heart. 2015;10(3):193-202.
• ³ World Health Organization (WHO). Chagas disease (also known as American trypanosomiasis). 2024. Available from: https://www.who.int/news-room/fact-sheets/detail/chagas-disease-(american-trypanosomiasis
  » https://www.who.int/news-room/fact-sheets/detail/chagas-disease-(american-trypanosomiasis
• ⁴ Lidani KCF, Andrade FA, Bavia L, Damasceno FS, Beltrame MH, Messias-Reason IJ, et al. Chagas disease: From discovery to a worldwide health problem. J Phys Oceanogr 2019;7:166.
• ⁵ Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera: Reduviidae) and their significance as vectors of Chagas disease. B Am Mus Nat Hist. 1979;163(3):123-520.
• ⁶ Costa J, Dale C, Galvão C, Almeida CE, Dujardin JP. Do the new triatomine species pose new challenges or strategies for monitoring Chagas disease? An overview from 1979-2021. Mem Inst Oswaldo Cruz. 2021;116:e210015.
• ⁷ 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.
• ⁸ Freitas LP, Lana RM, Cruz OG. Challenges for fighting Chagas disease in the 21st century. Mem Inst Oswaldo Cruz 2022;117.
• ⁹ Aufderheide AC, Salo W, Madden M, Streitz J, Buikstra J, Guhl F, et al. A 9,000-year record of Chagas’ disease. Proceedings of the National Academy of Sciences 2004;101(7):2034-9.
• ¹⁰ Steverding D. The history of Chagas disease. Parasit Vectors 2014;7(1):317.
• ¹¹ Coura JR, Dias JCP. Epidemiology, control and surveillance of Chagas disease: 100 years after its discovery. Mem Inst Oswaldo Cruz 2009;104(SUPPL. 1):31-40.
• ¹² Galvão C. Taxonomy. In: Guarneri A, Lorenzo M, eds. Triatominae - The Biology of Chagas Disease Vectors. Entomology in Focus. Cham: Springer; 2021. p. doi:10.1007/978-3-030-64548-9_2.
  » https://doi.org/10.1007/978-3-030-64548-9_2
• ¹³ Zhao Y, Fan M, Li H, Cai W. Review of Kissing Bugs (Hemiptera: Reduviidae: Triatominae) from China with Descriptions of Two New Species. Insects 2023, Vol 14, Page 450 2023;14(5):450.
• ¹⁴ Correia JPSO, Gil-Santana HR, Dale C, Galvão C. Triatoma guazu Lent and Wygodzinsky Is a Junior Synonym of Triatoma williami Galvão, Souza and Lima. Insects 2022, Vol 13, Page 591 2022;13(7):591.
• ¹⁵ de Paiva VF, Belintani T, de Oliveira J, Galvão C, da Rosa JA. A review of the taxonomy and biology of Triatominae subspecies (Hemiptera: Reduviidae). Parasitology Research 2022 2022:1-14.
• ¹⁶ Oliveira-Correia JPS, de Oliveira J, Gil-Santana HR, da Silva Rocha D, Galvão C. Taxonomic reassessment of Rhodnius zeledoni Jurberg, Rocha & Galvão: a morphological and morphometric analysis comparing its taxonomic relationship with Rhodnius domesticus Neiva & Pinto. BMC Zool 2024;9(1):6.
• ¹⁷ Carvalho DB, Congrains C, Chahad-Ehlers S, Pinotti H, De Brito RA, Da Rosa JA. Differential transcriptome analysis supports Rhodnius montenegrensis and Rhodnius robustus (Hemiptera, Reduviidae, Triatominae) as distinct species. PLoS One 2017;12(4):e0174997.
• ¹⁸ Carbajal-de-la-Fuente AL, Sánchez-Casaccia P, Piccinali RV, Provecho Y, Salvá L, Meli S, et al. Urban vectors of Chagas disease in the American continent: A systematic review of epidemiological surveys. PLoS Negl Trop Dis 2022;16(12):e0011003.
• ¹⁹ Segovia M, Schwabl P, Sueto S, Nakad CC, Londoño JC, Rodriguez M, et al. Vector mapping and bloodmeal metabarcoding demonstrate risk of urban Chagas disease transmission in Caracas, Venezuela. PLoS Negl Trop Dis 2023;17(3):e0010613.
• ²⁰ Urdaneta-Morales S. Chagas Disease: An Emergent Urban Zoonosis. The Caracas Valley (Venezuela) as an Epidemiological Model. Front Public Health 2014;2.
• ²¹ Costa J, Dornak L, Almeida C, Peterson A. Distributional potential of the Triatoma brasiliensis species complex at present and under scenarios of future climate conditions. Parasit Vectors 2014;7(1):238.
• ²² Silva RA da. Estado atual da vigilância entomológica da doença de Chagas no estado de São Paulo / Current state of the entomological surveillance of Chagas’ disease in the state of São Paulo. Brazilian Journal of Health Review 2019;2(2):742-55.
• ²³ Coura JR. The main sceneries of Chagas disease transmission. The vectors, blood and oral transmissions - A comprehensive review. Mem Inst Oswaldo Cruz 2014;110(3):277-82.
• ²⁴ Kock RA. Vertebrate reservoirs and secondary epidemiological cycles of vector-borne diseases. Revue Scientifique et Technique de l’OIE 2015;34(1):151-63.
• ²⁵ Gurgel-Gonçalves R, Cuba CAC. Predicting the Potential Geographical Distribution of Rhodnius neglectus (Hemiptera, Reduviidae) Based on Ecological Niche Modeling. J Med Entomol 2009;46(4):952-60.
• ²⁶ Silva RA da, Barbosa GL, Rodrigues VLCC. Vigilância epidemiológica da doença de Chagas no estado de São Paulo no período de 2010 a 2012. Epidemiologia e Serviços de Saúde 2014;23(2):259-67.
• ²⁷ Ramos LJ, Castro GV de S, de Souza JL, de Oliveira J, da Rosa JA, Camargo LMA, et al. First report of Rhodnius neglectus (Hemiptera, Reduviidae, Triatominae) from the State of Acre, Brazil, and the Brazilian Western Amazon Region. Rev Soc Bras Med Trop 2018;51(2):212-4
• ²⁸ Galvão C. Vetores da doença de Chagas no Brasil. In: Galvão C, ed. Vetores da doença de Chagas no Brasil. Curitiba: Sociedade Brasileira de Zoologia; 2014. p. 289. (Zoologia: guias e manuais de identificação).
• ²⁹ Barreto MP. Trypanosoma cruzi e doença de Chagas. Rio de Janeiro: Guanabara Koogan; 1979. p. 89-291. In: Brener Z Andrade ZA, editor. Trypanosoma cruzi e doença de Chagas. Rio de Janeiro: Guanabara Koogan; 1979. p. 89-291.
• ³⁰ Diotaiuti L, Dias JCP. Ocorrência e biologia do Rhodnius neglectus Lent, 1954 em macaubeiras da periferia de Belo Horizonte, Minas Gerais. Mem Inst Oswaldo Cruz 1984;79(3):293-301.
• ³¹ Ribeiro AR, Oliveira RC de Ceretti Junior W, Lima L, Almeida LA de, Nascimento JD, et al. Trypanosoma cruzi isolated from a triatomine found in one of the biggest metropolitan areas of Latin America. Rev Soc Bras Med Trop 2016;49(2):183-9.
• ³² Ceretti-Junior W, Vendrami DP, Matos-Junior MO de, Rimoldi-Ribeiro A, Alvarez JV, Marques S, et al. Occurrences of triatomines (Hemiptera: Reduviidae) and first reports of Panstrongylus geniculatus in urban environments in the city of Sao Paulo, Brazil. Rev Inst Med Trop Sao Paulo 2018;60(0).
• ³³ Pitt SJ, Gunn A. The One Health Concept. Br J Biomed Sci 2024;81.
• ³⁴ de Arias AR, Monroy C, Guhl F, Sosa-Estani S, Santos WS, Abad-Franch F. Chagas disease control-surveillance in the Americas: the multinational initiatives and the practical impossibility of interrupting vector-borne Trypanosoma cruzi transmission. Mem Inst Oswaldo Cruz 2022;117.
• ³⁵ Sereno D, Oury B, Grijalva MJ. Chagas Disease across the Ages: A Historical View and Commentary on Navigating Future Challenges. Microorganisms 2024;12(6):1153.
• ³⁶ Instituto Brasileiro de Geografia e Estatística (IBGE). Cidades@. São Paulo: Jaboticabal: Panorama. Disponível em: https://cidades.ibge.gov.br/brasil/sp/jaboticabal/panorama Accessed on: November 4, 2023.
  » https://cidades.ibge.gov.br/brasil/sp/jaboticabal/panorama
• ³⁷ Costa Santos LA, Miranda S do C de, Silva Neto C de Me. Fitofisionomias do Cerrado: definições e tendências. Rev Geo UEG 2020;9(2):1-30.
• ³⁸ Calor AR, Mariano R. UV light pan traps for collecting aquatic insects. EntomoBrasilis 2012;5(2):164-6.
• ³⁹ Oliveira J, Chaboli Alevi KC, Almeida CE, Mendonça VJ, Costa J, Rosa JA. Triatoma brasiliensis species complex: characterization of the external female genitalia. Journal of Vector Ecology 2020;45(1):57-68.
• ⁴⁰ Oliveira J, Alevi KCC, Almeida CE, Olaia N, Cacini GL, Galvão C, et al. Exploring the Hidden World of Vectors of Chagas Disease: A Fascinating Look at the Taxonomic Aspects of the Psammolestes Genus (Hemiptera, Triatominae). Life 2023;13(5):1081.
• ⁴¹ Castro-Arroyave D, Monroy MC, Irurita MI. Integrated vector control of Chagas disease in Guatemala: a case of social innovation in health. Infect Dis Poverty 2020;9(1):25.
• ⁴² Yevstigneyeva V, Camara-Mejia J, Dumonteil E. Analysis of Children’s Perception of Triatomine Vectors of Chagas Disease through Drawings: Opportunities for Targeted Health Education. PLoS Negl Trop Dis 2014;8(10):e3217.
• ⁴³ Sanmartino M, Mateyca C, Pastorino IC. What are we talking about when we talk about education and Chagas? A systematic review of the issue. Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease 2020;1866(5):165691.
• ⁴⁴ Stigler Granados P, Pacheco GJ, Núñez Patlán E, Betancourt J, Fulton L. Assessing the effectiveness of Chagas disease education for healthcare providers in the United States. BMC Infect Dis 2020;20(1):743.
• ⁴⁵ Gurgel-Gonçalves R, Abad-Franch F, Almeida MR de Obara MT, Souza R de CM de, Batista JA de S, et al. TriatoDex, an electronic identification key to the Triatominae (Hemiptera: Reduviidae), vectors of Chagas disease: Development, description, and performance. PLoS One 2021;16(4):e0248628.
• ⁴⁶ Bilheiro AB, Costa G da S, Araújo M da S, Ribeiro WAR, Medeiros JF, Camargo LMA. Identification of blood meal sources in species of genus Rhodnius in four different environments in the Brazilian amazon. Acta Trop 2022; 232:106486.
• ⁴⁷ Nery-Guimarães F. A refratariedade das aves ao “Trypanosoma (Schizotrypanum) cruzi” I. ausência de passagem para o sangue; duração da viabilidade e destruição dos parasitos na pele. Mem Inst Oswaldo Cruz 1972;70(1):37-48.
• ⁴⁸ Nery-Guimarães F, Venâncio I, Grynberg N. Refratariedade das galinhas ao “Trypanosoma (Schizotrypanum) Cruzi” III - dissociação dos fenômenos da refratariedade e da lise dos epimastigotas pelo soro das aves. Mem Inst Oswaldo Cruz 1974;72(1-2):131-6.
• ⁴⁹ Minter-Goedbloed E, A B Croon JJ. The insusceptibility of chickens to Trypanosoma (Schizotrypanum) cruzi Trans R Soc Trop Med Hyg 1981;75(3):350-3.
• ⁵⁰ Martínez-Hernández F, Oria-Martínez B, Rendón-Franco E, Villalobos G, Muñoz-García CI. Trypanosoma cruzi, beyond the dogma of non-infection in birds. Infect Gen and Evol 2022; 99, 105239.
• ⁵¹ Martínez-Ibarra JA, Grant-Guillén Y, Martínez-Grant DM. Feeding, defecation, and development times of Meccus longipennis Usinger, 1939 (Hemiptera: Reduviidae: Triatominae) under laboratory conditions. Mem Inst Oswaldo Cruz 2003;98(7):899-903.
• ⁵² Diotaiuti L, Dias JCP. Ocorrência e biologia do Rhodnius neglectus Lent, 1954 em macaubeiras da periferia de Belo Horizonte, Minas Gerais. Mem Inst Oswaldo Cruz 1984;79(3):293-301.
• ⁵³ Abad-Franch F, Lima MM, Sarquis O, Gurgel-Gonçalves R, Sánchez-Martín M, Calzada J, et al. On palms, bugs, and Chagas disease in the Americas. Acta Trop 2015;151(1):126-41.

• Financial Support:
  Financial support played no role in the study design, collection, analysis, interpretation, or manuscript writing. The Coordination for the Improvement of Higher Education Personnel (Capes, Brazil), Financing Code 001, provided financial support, but it did not influence the study design, collection, analysis, interpretation, or manuscript writing.

Publication Dates

• Publication in this collection
  15 Nov 2024
• Date of issue
  2024

History

• Received
  26 May 2024
• Accepted
  02 Oct 2024