Distribution and natural infection status of synantrophic triatomines (Hemiptera: Reduviidae), vectors of Trypanosoma cruzi, reveals new epidemiological scenarios for chagas disease in the Highlands of Colombia

Introduction Updating the distribution and natural infection status of triatomine bugs is critical for planning, prioritizing, and implementing strategies to control Chagas disease (CD), especially after vector reduction programs. After carrying out a control program, the Department of Boyaca contains the highest number of Colombian municipalities certified by PAHO to be free of intradomiciliary transmission of Trypanosoma cruzi by Rhodnius prolixus. The present work describes the spatial distribution, natural infection (NI), and molecular characterization of T. cruzi in synanthropic triatomines from the Department of Boyaca in 2017 and 2018. Materials and methods An entomological survey was conducted in 52 municipalities in Boyaca known to have had previous infestations of triatomine bugs. Insects were collected through active searches carried out by technical personnel from the Secretary of Health and community members using Triatomine Collection Stations (PITs-acronym in Spanish). For evaluation of natural infection, triatomines were identified morphologically and grouped in pools of one to five individuals of the same species collected in the same household. DNA derived from the feces of each pool of insects was analyzed by PCR for the presence of T. cruzi using primers flanking the satellite DNA of the parasite. SL-IR primers were used to differentiate TCI from the other DTUs and to identify different genotypes. The distribution of the collected triatomines was analyzed to determine any vector hotspots using spatial recreation. Results A total of 670 triatomine bugs was collected, belonging to five species: Triatoma dimidiata (73.2%), Triatoma venosa (16.7%), Panstrongylus geniculatus (5.7%), Rhodnius prolixus (4.4%), and Panstrongylus rufotuberculatus (0.4%), from 29 of the 52 municipalities. In total, 71.6% of the bugs were collected within houses (intradomiciliary) and the rest around the houses (peridomiciliary). Triatoma dimidiata was the most widely distributed species and had the highest natural infection index (37.8%), followed by T. venosa and P. geniculatus. TcI was the only DTU found, with the TcI Dom genotype identified in 80% of positive samples and TcI sylvatic in the other insects. Spatial analysis showed clusters of T. dimidiata and T. venosa in the northeast and southwest regions of Boyaca. Conclusions After some municipalities were certified free of natural transmission within houses (intradomiciliary transmission) of T. cruzi by R. prolixus, T. dimidiata has become the most prevalent vector present, and represents a significant risk of resurgent CD transmission. However, T. venosa, P. geniculatus, and P. rufotuberculatus also contribute to the increased risk of transmission. The presence of residual R. prolixus may undo the successes achieved through vector elimination programs. The molecular and spatial analysis used here allows us to identify areas with an ongoing threat of parasite transmission and improve entomological surveillance strategies.
Author summary Chagas disease is one of the most important tropical diseases in the Americas. Since 2010, Colombia has implemented programs to interrupt the intradomiciliary transmission of T. cruzi by R. prolixus, Colombia’s primary vector. Boyaca, located in this country’s central region, is one of the most endemic departments for Chagas disease. Control measures have been implemented, and the intradomiciliary transmission of T. cruzi by R. prolixus has been significantly reduced in 24 municipalities, according to PAHO certifications. Currently, the main risks in these certified municipalities are the presence of secondary vectors and certain ecological conditions favorable to triatomines. In the present study, we provide evidence that T. dimidiata and T. venosa have become the most common species. We observed a cluster of these infected species in the northeast and southwest regions of Boyaca. P. geniculatus and P. rufotuberculatus were present but less abundant, and residual R. prolixus populations remain in some certified-free municipalities. The overall natural infection index of secondary vectors was 31%, and spatial analysis identified priority areas for implementing surveillance and control actions. We identified T. cruzi in municipalities above 2,000 meters above sea level, which traditionally are considered non-endemic regions in Colombia. This suggested new epidemiological scenarios for Chagas disease transmission in Colombia’s highlands and requires more studies to examine these scenarios.