Presence of Rhodnius prolixus Stäl, 1859 (Hemiptera: Reduviidae) in Oaxaca, Mexico, ten years after the certification of its elimination

Triatomines, commonly known as kissing bugs, are hematophagous insects that belong to the subfamily Triatominae. Triatomines are important natural vectors of Trypanosoma cruzi that causes Chagas disease (Ballesteros-Rodea et al. 2018, Flores-Ferrer et al. 2018). A total of 151 species, representing fifteen genera, have been described globally (Justi and Galvão 2017). In Mexico, there are 32 triatomine species grouped into eight genera; Triatoma is the most abundant (19 species), followed by Meccus (6), Belminus (1), Dipetalogaster (1), Eratyrus (1), Paratriatoma (1), Panstrongylus (2), and Rhodnius (1) (Galvão et al. 2003, Schofield and Galvão 2009). Most of these species have been found naturally infected with T. cruzi (Ramsey et al. 2015). Rhodnius prolixus is considered one of the most efficient vectors of T. cruzi and has a high adaptability to domestic and peridomestic habitats. It was originally described in Venezuela and Colombia in South America, but its presence was reported in the city of San Salvador in Central America in 1915. Rhodnius prolixus subsequently spread to El Salvador, Guatemala, Honduras, Nicaragua, Costa Rica, and southern Mexico (Dujardin et al. 1998, Hashimoto and Schofield 2012). In Mexico, the presence of R. prolixus was discovered in regions connected to Guatemala in the State of Oaxaca in 1938 and in Chiapas in 1949 (Hashimoto and Schofield 2012). The state of Oaxaca, Mexico, is considered a Chagas endemic area, which also hosts eleven triatomine species (Cruz-Reyes and Pickering-López 2006). Rhodnius prolixus was reported from five localities. However, the last report of this species in the country was from Nejapa de Madero, Oaxaca, in 1998 (Ramsey et al. 2000, Vidal-Acosta 2000). Due to the apparent absence of R. prolixus, even after repeated surveys, the certification of elimination of this vector was awarded to Chiapas and Oaxaca, Mexico, in 2009 (Hashimoto and Schofield 2012). It should be noted that Mexico, since 2004, and as of 2013 together with Central America, belong to the Central America and Mexico Initiative for the prevention and control of Chagas disease. The present study reports the presence of R. prolixus in the municipalities of Nejapa de Madero and San Carlos Yautepec in southern Oaxaca, Mexico, ten years after Mexico was certified to be free of this vector. Both sampled municipalities have a warm-humid climate. Nejapa de Madero has an annual temperature range of 12–26° C, and the annual precipitation range is 400–1600 mm. San Carlos Yautepec has an annual temperature range of 8–28° C, and the annual precipitation range is 400–2,500 mm. In 2017, one R. prolixus was collected in a dwelling in the municipality of San Carlos Yautepec by its inhabitant on a bedroom wall of a dwelling behind the bed. This person subsequently contacted our research group in order to identify the specimen. Seeking additional information, we interviewed people who live in this community, as well as people from the neighboring municipality of Nejapa de Madero, where triatomine species have previously been found (Ramsey et al. 2000, Vidal-Acosta 2000). Based on the above, we decided to survey both locations. The search for triatomines was performed manually as indicated by the Mexican Norm NOM-032-SSA2-2014, for a week in the spring of 2019. Each sample was placed in a plastic container and labeled for transportation. Samples, which included exochorion, nymphs, and adults, were found only in Nejapa de Madero (Table 1). Twenty-five triatomines were collected in the Nejapa de Madero locality, and one triatomine was collected in the San Carlos Yautepec locality. In Nejapa de Madero, of the ten houses visited, triatomines were only found inside two houses and in an empty lot close to other human dwellings (Figure 1). In San Carlos Yautepec, the only specimen was found inside under a bed (Figure 1). The identification of the specimens was carried out at the Laboratory of Medical Entomology of Escuela Nacional de Ciencias Biologicas, Instituto Politecnico Nacional, Mexico City, following the classification of Lent and Wygodzinsky (1979). The identification of the nymphs was made at the genus level according to Lent and Wygodzinsky (1979), considering that only one species of Rhodnius has been described for Mexico. Some specimens had reached adulthood and their identification was confirmed. All field-collected triatomines were identified as R. prolixus. Feces from each sample were obtained from spontaneous defecations after feeding on New Zealand rabbits reared in the laboratory. Fecal samples were mixed with 1X PBS and examined for the presence of T. cruzi by optical microscopy (LEICA DM500®) at 400X. The sample from San Carlos Yautepec tested positive for T. cruzi infection (Table 1). The 25 triatomines were maintained in the insectary at 28° C with 60% relative humidity (RH). 5 (1nd) 3 (2nd) 16 ° 36 ′ 0 ″ N 95 ° 59 ′ 0 ″ W 16 ° 30 ′ 0 ″ N 96 ° 6 ′ 0 ″ W Rhodnius prolixus (Figure 2) has an average length of 17.34 mm; its general color is yellowish-brown with dark brown markings. The head is long and narrow with slender four-segmented antennae. The rostrum is large, with the second segment extending to the level of the ocelli. Eyes have black and red ommatidia. The pronotum has some prominent carinae, submedian carinae, and a light yellowish brown lateral margin. The scutellum is dark, with 1+1 light yellowish brown lines along the edges of the central depression. The hemelytra have narrowly margined veins that are light yellow; the rest are dark brown. The connexivum is yellowish-brown with a black spot that occupies one-third to one-half of each of the urosternites, similar to that described by Lent and Wygodzinsky (1979). According to local citizens, the spraying of insecticide is carried out in households where triatomines are reported; however, houses that are abandoned or not inhabited are excluded from the spraying. Therefore, there is a possibility that these non-sprayed sites function as a refuge for triatomines. There is also a possibility that these triatomines developed resistance to the pesticides used, because resistance of R. prolixus has been reported to different pesticides, mainly pyrethroids (Vassena et al. 2000, Flores-Ferrer et al. 2018). Moreover, it is important to note that the areas where triatomines were collected are semi-urban, and most of the sampled houses are built mainly with adobe, wood, metal sheets, and palm, and this last material is considered a natural habitat of R. prolixus (Dujardin et al. 1998). In Oaxaca, there is no recent information on the prevalence of Chagas disease; however, there are different studies from blood banks indicating a prevalence that ranges between 1.10% (Guzmán-Bracho et al. 1998) and 0.24% (Novelo-Garza et al. 2010). In addition, the municipalities sampled in this study are within the area where human populations are reported to be exposed to triatomines infected with T. cruzi (Ramsey et al. 2015). Therefore, the households and yards colonized with R. prolixus located less than 20 m from dwellings in an area in which some residents have been diagnosed with Chagas disease suggests active vector-mediated T. cruzi transmission. Furthermore, the presence of nymphs, exuviae, and exochorion suggest a process of R. prolixus colonization, which may cause a major problem for vector control and T. cruzi transmission in the population living in these areas. It is important to note that the inhabitants of these municipalities could identify common triatomines in these areas. When they were shown color photographs of the main triatomine species in the state, they particularly identified Meccus phyllosomus. However, inhabitants were unable to identify R. prolixus as a T. cruzi vector due to the large morphological differences between these triatomine species. It is extremely important to design rational pesticide spraying strategies to avoid triatomines hiding in non-sprayed areas. In this way, there will be control over the domestic and peri-domestic populations avoiding the re-infestation and development of pesticide-resistant triatomines. Further surveillance is required, since wild bugs often show high infection rates and may establish new peri-domestic and domestic cycles of T. cruzi (Vidal-Acosta et al. 2000). The determination of the geographical distribution of triatomines is fundamental to better understanding the eco-epidemiology of Chagas disease, considering environmental changes such as: deforestation, agriculture, shifts in land use, and climatic changes that can alter the displacement of vectors and reservoirs in new areas, directly influencing transmission dynamics of T. cruzi. We thank the people of Nejapa de Madero and San Carlos Yautepec for allowing us to search for triatomines in their homes.