The city of Sao Paulo, one of the largest metropolis in the world with an estimated population of 12 million, the largest in the Southern hemisphere, suffers from severe environmental stress. Because of an extensive human interference in the natural environment, the remaining forest fragments are now found only in parks, gardens and environmental protection areas8,9.
The city of Sao Paulo is located in what was formerly the Atlantic rainforest, an environment with high biodiversity considered one of the 23 “biodiversity hotspots” worldwide10. Despite the intense expansion of the city in the last five decades, there have been sporadic occurrences of triatomine bugs on the outskirts of Sao Paulo, some in unusual situations7,11.
The only occurrence of T. infestans reported in the city of Sao Paulo was in 2004 in the men’s restroom at the Dante Pazzanese Hospital, a national reference center for treatment of Chagas disease. The specimen may have escaped from the triatomine colonies maintained by the hospital for xenodiagnosis. In 2006, Brazil received the international certification for interruption of transmission of Chagas disease by this species from the Pan American Health Organization12,13.
In the State of Sao Paulo, a campaign against the vector of Chagas disease began in 195114,15. Although T. infestans was eliminated from the State by 1990 as a result of the campaign, control activities were not interrupted because of the possibility of sporadic passive reintroduction of T. infestans in isolated locations, as reported by Leite et al.14 following the finding of 109 specimens of this species in the municipality of Paulinia, in the State of Sao Paulo, between 1999 and 2000. This was the last reported occurrence of the species in the State.
One reason for continued triatomine surveillance and control activities in the city of Sao Paulo was the presence of species considered important in the transmission of T. cruzi, such as T. sordida and P. megistus, in large areas of Brazil, including the State of Sao Paulo. These species are found colonizing households mainly in annexes and outhouses. Another reason for continued surveillance was the report of invasions of households by Rhodnius neglectus in the area of the State corresponding to the Eastern Plateau, Peripheral Depression and Western Plateau and by Triatoma tibiamaculata on the State coastline15.
In the case of T. sordida, it is most likely that specimens were taken to the capture locations by passive dispersion as the residents in these locations reported that they had returned from trips to endemic regions. Another possibility is the dispersion by animals, particularly birds, as T. sordida feeds preferentially on birds16. Nymphs and eggs of the species can be dispersed over large areas extending far from the original source of infestation/colonization. The species has a widespread distribution and is found in Argentina, Bolivia, Uruguay and Paraguay and the States of Bahia, Goias, Mato Grosso, Mato Grosso do Sul, Minas Gerais, Parana, Pernambuco, Piaui, Rio Grande do Sul, Santa Catarina and Sao Paulo in Brazil17,18. In Sao Paulo and other States, it is found mainly in cerrado (savannah-like grasslands) biomes. It is the most captured vector of Chagas disease, and there have been numerous reports of the species in chicken coops in peridomestic areas with a low T. cruzi infection rate16,19,20.
Triatoma sordida populations infected by T. cruzi persist even after insecticide has been sprayed because they are autochthonous to the territories where they occur and, after sheltering in the peridomestic area, can reinfest dwellings once the residual effect of the insecticide has worn off16,21.
Most captures of P. megistus in the city of Sao Paulo have been in neighborhoods on the Southern outskirts of the city in areas close to Sao Paulo Zoo, Safari Zoo, the Botanic Gardens and the USP Science and Technology Park, all of which receive large numbers of visitors (Table 1). This suggests that populations of this species remain in forest fragments, where they can perpetuate the T. cruzi sylvatic transmission cycle within the boundaries of the municipality of Sao Paulo. In 2016, Ribeiro et al.7 reported positivity for T. cruzi in a P. megistus bug captured in an urban area of the city. In a study of epidemiological surveillance in Sao Paulo between 2010 and 2012, Silva et al.20 found that this species was the most important vector of Chagas disease in the State, a finding reflected in its increasing domiciliation and high natural-infection index (23.6%).
Panstrongylus geniculatus (Latreille 1811), which has been found naturally infected with T. cruzi, has a distribution extending from Southern Mexico to Northern Argentina. Although its habitats include a wide range of biomes and climates17,22, its most common habitat is wild forest environments, where it is found in armadillo (Dasypodidae) burrows and opossum (Didelphis) dens23,24. Although associated with wild environments, there are reports of the species attacking people24. It has been captured in pigsties and in environments occupied by humans, where it is attracted to light, although without forming colonies in the domicile23-26. Despite the limited vector potential of P. geniculatus, this triatomine can be epidemiologically important and has been involved in domestic cycles of T. cruzi in Venezuela27,28, Colombia29, Brazil23,30-32, Peru33,34, Bolivia35,36 and Argentina37, in the former in an outbreak of Chagas disease due to oral transmission at a school on the outskirts of Caracas38,39 and Colombia40.
Two occurrences of P. geniculatus in the city of Sao Paulo have been reported. The first was of an adult bug found in a neighborhood in the Southern area of the city in 1999, and the second was in July 2014 when a specimen was captured in a Culex quinquefasciatus mosquito-breeding facility next to the Pinheiros River (Figure 1). After the specimen had been identified, analysis to detect T. cruzi infectivity was conducted according to Ribeiro et al.7, with negative result. Fifteen days after the specimen was captured, an active search was conducted within a radius of about 250 m of the capture site to locate possible shelters of this triatomine, and five Noireau traps41 adapted according to Obara et al.42 were installed. However, none of the procedures resulted in any further captures.
Although the active search for triatomines was negative, the presence of colonies in the area surrounding the breeding facility cannot be completely ruled out as there are remnants of reforestation and landscaping that provide shelter for rodents and other food sources for triatomines, such as opossums and birds. This species has a wide distribution and could be authoctonous in the area17,22.
Chagas disease is associated with poverty and inadequate sanitation in the dwellings of at-risk populations2, and transmission of the disease to humans typically occurs in wild, rural and periurban areas. However, with fragmentation of the natural habitats of the vectors of the disease as a result of urbanization and the increasing use of land for crops and pastures, triatomines, which were previously found exclusively in wild environments, are now commonly found in households, particularly on the outskirts of cities39,42,43-45.
Data on occurrences of triatomines in the city of Sao Paulo indicate the importance of entomological surveillance of these vectors even in urban centers. Although the possibility of vector transmission of Chagas disease in major urban centers is very small, it cannot be ignored. If infected, triatomines that have invaded households and other buildings, to which they are attracted to by various factors, including light, can transmit the etiological agent of Chagas disease to humans and animals. As triatomines can contaminate food and other household items with their urine and feces, it is also important to consider the risk of oral transmission, the main form of transmission of T. cruzi today. Examples of this type of transmission have been reported in urban centers in recent decades and include a case involving T. sordida in the State of Bahia, Brazil, and another involving P. geniculatus in Caracas, Venezuela, in which contaminated water and guava juice, respectively, were ingested39,46. Accidents as a result of handling of the insect by humans or ingestion by domestic animals can also occur in large urban centers, where people are often not familiar with the appearance of these vectors.
These facts imply that in order to prevent the eventual transmission of T. cruzi in the municipality of Sao Paulo, the community is encouraged to send any suspicious insects to the local Health Supervisors (SUVIS) and that the communication between the laboratories that participated in this article, together with the Department of Health Coordination Sanitary Surveillance (COVISA) and Superintendence of Control of Endemic Diseases (SUCEN) are further narrowed, allowing a faster flow of specimens for identification and parasitological examinations, as well as more effective sharing of information.