|Year : 2022 | Volume
| Issue : 1 | Page : 86-90
New records of Triatoma huehuetenanguensis in an urban area of Southwest Mexico
Carlos A Espinosa-Gonzalez1, Eduardo Dávalos-Becerril2, Fabián Correa-Morales2, Cassandra González-Acosta3, Royer López-Bello1, J Miguel Alvarado-Estrada1, Luis M Esquinca-Calvo1, Claudia V García-Gutiérrez1, Cinthia A Gómez-Maldonado1, Eduardo Cuevas-González1, César Reyes-Figueroa1, Miguel Moreno-García4
1 Unidad de Investigación Entomológica y Bioensayos-Servicios de Salud de Chiapas. Rio Shumula 228, Paraíso II, C.P. 29049. Tuxtla Gutiérrez, Chiapas, Mexico
2 Centro Nacional de Programas Preventivos y Control de Enfermedades. Benjamín Franklin 132, Escandón, C.P. 11800. Ciudad de México, Mexico
3 Servicios de Salud de Morelos. Coordinación de Enfermedades Transmitidas por Vector y Zoonosis. Callejón Borda 3, Centro, C.P. 62000, Cuernavaca, Morelos, Mexico
4 Unidad de Investigación Entomológica y Bioensayos-Centro Regional de Control de Vectores Panchimalco-Servicios de Salud de Morelos. Emiliano Zapata 95, C.P. 62900. Jojutla, Morelos, Mexico
|Date of Submission||10-Aug-2021|
|Date of Acceptance||06-Oct-2021|
|Date of Web Publication||07-Jun-2022|
Unidad de Investigación Entomológica y Bioensayos-Centro Regional de Control de Vectores Panchimalco-Servicios de Salud de Morelos. Emiliano Zapata 95, C.P. 62900. Jojutla, Morelos
Source of Support: None, Conflict of Interest: None
The recently described Triatoma huehuetenanguensis, has been reported in Mexico, Guatemala, Belize and Honduras. In Mexico, the species has been collected primarily in rural areas; it has the potential to colonize human dwellings, however, its contribution to Chagas outbreaks remains unclear. In 2021, T. huehuetenanguensis was first observed at Tuxtla Gutierrez city, Chiapas; then a collection for the species was performed. A total of 308 houses were inspected in the intra and peridomestic structures. Only 3 houses (0.97%) were infested. Triatoma huehuetenangensis was the only triatomine specie recorded and four males were collected. None of the bugs tested positive for Trypanosoma infection. We do not have evidence to suggest that urban human-vector contact still limited, and a possible domestication process is possible. The presence of reservoirs, the vector species and the parasite demonstrate that Tuxtla Gutierrez could be at risk of a Chagas disease outbreak.
Keywords: Chagas disease; México; Triatoma huehuetenanguensis; urban areas.
|How to cite this article:|
Espinosa-Gonzalez CA, Dávalos-Becerril E, Correa-Morales F, González-Acosta C, López-Bello R, Alvarado-Estrada J M, Esquinca-Calvo LM, García-Gutiérrez CV, Gómez-Maldonado CA, Cuevas-González E, Reyes-Figueroa C, Moreno-García M. New records of Triatoma huehuetenanguensis in an urban area of Southwest Mexico. J Vector Borne Dis 2022;59:86-90
|How to cite this URL:|
Espinosa-Gonzalez CA, Dávalos-Becerril E, Correa-Morales F, González-Acosta C, López-Bello R, Alvarado-Estrada J M, Esquinca-Calvo LM, García-Gutiérrez CV, Gómez-Maldonado CA, Cuevas-González E, Reyes-Figueroa C, Moreno-García M. New records of Triatoma huehuetenanguensis in an urban area of Southwest Mexico. J Vector Borne Dis [serial online] 2022 [cited 2022 Jun 25];59:86-90. Available from: https://www.jvbd.org/text.asp?2022/59/1/86/331410
Triatomines, also known as kissing bugs, are insects of medical importance. They are the natural vectors of Trypanosoma spp. including T. cruzi, the etiologic agent of American trypanosomiasis also known as Chagas disease. Chagas disease is a seriously neglected tropical disease. Currently, almost six million people are infected by T. cruzi worldwide, with most infected people currently living in Latin America. The health load of Chagas disease imposes a substantial financial burden on the healthcare system and society.
A total of 154 kissing bugs species has been described in the world, assigned to five tribes and 19 genera; the majority of species are found in the Neotropical and southern Nearctic regions and the Antilles. In Mexico, biodiversity of triatomine is represented by 32 species grouped into eight genera, most of which have been reported to be naturally-infected with T. cruzi,,,. Triatoma occurrence has been commonly associated to rural areas. Nevertheless, local and non-local human transit might cause accidental introductions to urban areas, with high population densities and domestic animals (e.g., dogs, cats) or other urban fauna (e.g., rats, birds) acting as the main source of blood.
Triatoma dimidiata Latreille 1811 has been considered as one of the most significant species in the epidemiology of Chagas disease. The species shows a great phenotypic, genotypic, and behavioural diversity,,. Genetic studies have recognized T. dimidiata as four lineages including three different species: T. dimidiata s. str., Triatoma sp. aff dimidiata cave (currently described as Triatoma mopan Dorn, Justi, Dale 2018),, and Triatoma sp. aff dimidiate (currently described as Triatoma huehuetenanguensis Lima-Cordón, Monroy, Stevens, Rodas, Rodas, Dorn, Justi 2019).
Triatoma huehuetenanguensis holotype, paratypes and inferred specimens of T. huehuetenanguensis has been collected at Guatemala, Belize, Honduras and Mexico. Information regarding its life cycle, number of meals required to molt, feeding and defecation behaviours, fecundity and high natural infection rates with T. cruzi (78–90%) imply a highly possible vector role,. Triatoma huehuetenanguensis can be found in intradomiciliary environments, near to tropical forest suggesting that the species could be exploiting the housing conditions. In Mexico, the species (and inferred specimens) has been collected primarily in rural areas and occasionally at urban localities. However, its potential to colonize human dwellings and contribution to Chagas epidemics remains unclear.
In 2021, T. huehuetenanguensis was first observed at Tuxtla Gutierrez city, Chiapas. Since this represents a new record for the city, and monitoring of vector species is one of the core responsibilities of vector control programmes, a collection for the species was performed. In this study we report the results of the survey and highlight the importance of continuous monitoring of current and emerging vectors at urban areas. Chiapas is ranked as one of the top states for rural Chagas disease; however, the disease remains as a neglected illness among the urban population. Therefore, information regarding the disease and its vectors will enforce Triatoma surveillance.
| Material & Methods|| |
Tuxtla Gutiérrez city is the capital and the largest city of the Mexican southeastern state of Chiapas [Figure 1], comprising an area of 340.74 km2, with surrounding areas consisting of forests. According to the INEGI 2020 census, the total population is 604,147 citizens. It is located at central valley region of the state, at an elevation of 200-1500 masl, between the parallels 16°38′-16°51′ N and 93°02′-93°15′ W. The predominant climate is warm/ semi-warm sub-humid with rains in summer; the average temperature oscillates between 20–28°C and rainfall of 800–1200 mm (information retrieved from: Prontuarios de información geográfica municipal de los Estados Unidos Mexicanos, INEGI). Survey was performed at a Southwest area of the city and in Copoya (district belonging to Tuxtla Gutiérrez; 16°42′50″ N, 93°07′10″ W). Collecting areas are near the surroundings of Mactumatzá Hill located at the Southwest of the city [Figure 1]. The hill vegetation is tropical deciduous/sub deciduous forest with shrubs and herbaceous plants. In the last two seasons, wildfires raged across large areas of Mactumatzá Hill.
|Figure 1: A. Chiapas State, B. Tuxtla Gutierrez location and C) Surveyed areas (red polygons) and positive sites (yellow dots). MH= Mactumatzá Hill; EZ= El Zapotal Ecological Preserve.|
Click here to view
A cross-sectional entomologic survey (active and passive) was conducted from April to June 2021. Bugs were collected in intradomiciles, peridomiciles and peridomestic annexes (e.g., cat/dog houses, birdcages, corrals, storerooms, wood/gravel-piles). The intradomiciliary searches focused on places where triatomines could hide, such as cracks in the walls, floors, roofs and furniture. Collecting times were from eight in the morning to noon and eight in the evening to midnight. House location was recorded using a Global Positioning System. In each house the intradomestic and peridomestic habitats were examined by the one person-hour-house method, bugs were collected individually using metallic forceps. Collected specimens were placed in individually labelled plastic containers and were transported, deposited and identified in the Entomological and Bioassay Research Unit of Chiapas using available taxonomic keys,.
The intestinal contents of the insects were obtained by abdominal compression and analyzed for the presence of Trypanosoma spp. by microscopy. The infection index (100 x number of infected individuals/total number of analyzed individuals) was calculated.
| Results and Discussion|| |
A total of 308 houses were inspected in the intra and peridomestic structures. Only three houses (0.97%) were infested with triatomines. Triatoma huehuetenanguensis was the only triatomine species recorded [Figure 2], four males were collected. In Copoya, one male was found inside a bedroom with brick walls, concrete floor and concrete slab roof. In Tuxtla Gutiérrez, two bugs were found in a one room house, at the walls of the bedroom area; the room had concrete floor with cracks, wood/tarred-cardboard walls and corrugated metal roof. In a peridomicile of Tuxtla Gutiérrez, with dirt floor, shrubs, trees, palms and presence of pets, one bug, at the floor, was collected at night. None of the bugs tested positive for Trypanosoma spp. infection.
|Figure 2: Triatoma huehuetenanguensis male from Tuxtla Gutiérrez, Chiapas (ventral and dorsal view)|
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Identification of T. huehuetenanguensis preferred urban habitats in Tuxlta Guitiérrez is limited by the low number of bugs captured at each site of collection. However, some results in this paper are consistent with previous observations. Michel-Parra et al. had speculated that, since only adult specimens have been collected, T. huehuetenanguensis has limited capacity to colonize human dwellings. Additionally, it is possible that T. huehuetenanguensis have an active dispersal from the forest to the nearby houses attracted by the urban lights. The fact that houses where bugs were collected are near sylvatic areas suggest that dispersion of T. huehuetenanguensis occur between sylvatic and domestic environments. Active flight or walking dispersal, from sylvatic to domestic areas, have been considered an important (and more frequent than assumed) mechanism of colonization. In the last three decades Tuxtla Gutiérrez has experienced significant growth of the urban area, leading to changes in land use. Also, recent wildfires in the Mactumatzá Hill may be changing the habitat and behaviours of the specie, inciting bug dispersion and shifting preferred blood-feeding sources. The loss of conserved areas increases the likelihood of the vector coming into contact with humans.
Related, low vector abundance could be associated to recent bug invasions from external foci or because recent establishment of urban houses. Alvedro et al. proposed that low triatomine numbers is because they may have less access to blood-feeding due to a lower abundance of hosts associated to enhanced constructions and animal management. In this study, the interior dwellings in the collecting areas show a mixture of constructing materials (concrete, wood, cardboard, metal, clay tile, etc.), occasionally with indoor presence of pets (e.g., dogs, cats, caged birds), non-structural cracks and lack of cohesion among floors, roofs and walls. While peridomiciles have dirt, cement or grass floors, rock/wood/pottery-junk piles, cluttered yard/ storerooms/annexes and presence of domestic animals (with or without kennels). The presence of stray dogs in the areas was also conspicuous. All these features could facilitate further triatomine presence in the area,,,. Invasion/colonization of T. huehuetenanguensis in Tuxtla Gutierrez is unclear and warrants further research.
At Chiapas, a relatively high seropositivity and active transmission has been detected at the North of the state (Central Mountains and Lacandon forest) and coastal zone. However, the central zone of the State (i.e. Tuxtla Gutierrez) has not been extensively studied. At the Ecological Park “El Zapotal”, near our collecting areas [Figure 1], sylvatic cycle has been found; however, low infection rate was detected in reservoir vertebrates. It has been proposed that this could be a reflection of the low density of triatomine, however, a low prevalence of the parasite in the area is also possible; this needs further research. Seropositive stray dogs and infected T. dimidiata have also been found in Tuxtla Gutierrez,. Information available on seroprevalence indicates that in Tuxtla Gutierrez antibodies have been detected in native and non-native residents of the city. Contrary to previous observations,, no infection was detected in the captured specimens. We do not have enough evidence to suggest that human-vector contact still limited in the area. Despite that risk factors related to triatomine infestation can be different in different regions, the presence of reservoirs, infected vectors and the parasite suggest that Tuxtla Gutierrez could be at risk of a Chagas disease outbreak.
A critical goal of monitoring vector-borne diseases is quantifying transmission risk to humans in the presence of vectors. Our study creates a starting point for future efforts aimed to addressing T. huehuetenanguensis distribution across the city. A permanent surveillance for colonization of domestic environments by sylvatic species of triatomine vectors in the city is highly encouraged. Special attention should be devoted to the forest/city interface areas.
| Acknowledgements|| |
We are grateful to the Minister of Health of Chiapas, Dr. José Manuel Cruz-Castellanos for all his support to this research. We are also thankful with Dr. Leticia Jarquin-Estrada, Dr. Alam Porfirio Campos-Cruz, L.E. Aarón Manuel Morales-Domínguez and Biol. Félix González-Cruz for their guidance and encouragement. We thank the entomological staff of the Prevention and Dengue Control Department at the Jurisdicción Sanitaria I for their assistance in the field. We would like to thank two anonymous reviewers for their helpful suggestions and comments.
| References|| |
Lent H, Wygodzinsky P. Revision of the triatominae (Hemiptera, Reduviidae), and their significance as vectors of Chagas’ disease. Bull Am Mus Nat Hist
1979; 163: 124–520.
Guhl F. Geographical distribution of Chagas disease
. In: Telleria J, Tibayrenc M, editors. American Trypanosomiasis Chagas disease. One hundred years of research, 2nd ed. Amsterdam, The Netherlands: Elsevier 2017; p. 89–106.
Lee BY, Bacon KM, Bottazzi ME, Hotez PJ. Global economic burden of Chagas disease: a computational simulation model. Lancet Infect Dis
2013; 13: 342–348.
Zhao Y, Jiang M, Wu Y, Song F, Cai W, Li H. Mitochondrial genomes of three kissing bugs (Reduviidae: Triatominae) and their phylogenetic implications. Int J Biol Macromol
Aguilar RA, Nogueda-Torres B, Cortéz-Jiménez M, Jurberg J, Galvão C, Carcavallo RU. Triatoma bassolsae
sp. n. do México, com uma chave para as espécies do complexo ‘phyllosoma’ (Hemiptera, Reduviidae). Mem Inst Oswaldo Cruz
1999; 94: 353–359.
Galvão C, Carcavallo RU, Rocha DS, Jurberg J. A checklist of the current valid species of the subfamily Triatominae Jeannel, 1919 (Hemiptera: Reduviidae) and their geographical distribution, with nomenclatural and taxonomic notes. Zootaxa
Salazar-Schettino PM, Rojas-Wastavino GE, Cabrera-Bravo M, Bucio-Torres MI, Martínez-Ibarra JA, Monroy-Escobar MC, et al
. Revision of thirteen species of Triatominae (Hemiptera: Reduviidae) vectors of Chagas disease in Mexico. J Selva Andina Res Soc
2010; 1: 57–80.
Ramsey JM, Peterson AT, Carmona-Castro O, Moo-Llanes DA, Nakazawa Y, Butrick M, et al
. Atlas of Mexican Triatominae (Reduviidae: Hemiptera) and vector transmission of Chagas disease. Mem Inst Oswaldo Cruz
Lounibos LP. Invasions by insect vectors of human disease. Annu Rev Entomol
2002; 47: 233–66.
Pech-May A, Mazariegos-Hidalgo CJ, Izeta-Alberdi A, López-Cancino SA, Tun-Ku E, et al
. Genetic variation and phylogeography of the Triatoma dimidiata
complex evidence a potential center of origin and recent divergence of haplogroups having differential Trypanosoma cruzi
and DTU infections. PLoS Neglected Trop Dis
2019; 13: e0007044.
Dorn PL, Monroy C, Curtis A. Triatoma dimidiata
(Latreille, 1811): a review of its diversity across its geographic range and the relationship among populations. Infect Genet Evol
Bargues MD, Klisiowicz DR, Gonzalez-Candelas F, Ramsey JM, Monroy C, Ponce C, et al
. Phylogeography and genetic variation of Triatoma dimidiata
, the main Chagas disease vector in Central America, and its position within the genus Triatoma. PLoS Neglected Trop Dis
2008; 2: e233.
Dorn PL, de la Rúa NM, Axen H, Smith N, Richards BR, Charabati J, et al
. Hypothesis testing clarifies the systematics of the main Central American Chagas disease vector, Triatoma dimidiata
(Latreille, 1811), across its geographic range. Infect Genet Evol
2016; 44: 431–443.
Justi SA, Cahan S, Stevens L, Monroy C, Lima-Cordon R, Dorn PL. Vectors of diversity: Genome wide diversity across the geographic range of the Chagas disease vector Triatoma dimidiata
sensu lato (Hemiptera: Reduviidae). Mol Phylogenet Evo
2018; 120: 144–150.
Lima-Cordón RA, Monroy MC, Stevens L, Rodas A, Rodas GA, Dorn PL, Justi SA. Description of Triatoma huehuetenanguensis
sp. n., a potential Chagas disease vector (Hemiptera, Reduviidae, Triatominae). ZooKeys
2019; 820: 51–70.
Michel-Parra JG, Martínez-Ibarra JA, Montañez-Valdez OD,Nogueda-Torres B. Life cycle of Triatoma huehuetenanguensis
Lima-Cordón, Monroy, Stevens, Rodas, Rodas, Dorn, Justi 2019 (Hemiptera: Reduviidae: Triatominae) from Mexico, J Vector Ecol
2021; 46(1): 57–64
De Fuentes-Vicente JA, Gómez-Gómez A, Santos-Hernández NG, Ruiz-Castillejos C, Gómez-Sánchez E, Vidal-López D, et al
. First report of an infected triatomine bug in an urban area of Tuxtla Guitiérrez, Chiapas, México. BIOCYT
2021; 14: 1009–1020
Trujillo-Rincón JH. Cómo gestionar un destino turístico emergente y vivir para contarlo - Construcción de una estrategia competitiva a partir de la complejidad territorial de una ciudad capital: El caso de Tuxtla Gutiérrez. Turismo y Sociedad
OPS. Control, interrupción de la transmisión y eliminación de la enfermedad de Chagas como problema de salud pública. Guía de evaluación, verificación y validación. Washington, DC: Organización Panamericana de la Salud 2019; 76 p.
Lobbia PA, Alvarez R, Picollo MI, Mougabure-Cueto G. First record of domestic colonies of the dark chromatic variant of Triatoma infestans
(Hemiptera: Reduviidae). Rev Soc Entomol Arg
Silva M, Garcia A, Hernando A. Crecimiento de la mancha urbana en la Zona Metropolitana de Tuxtla Gutiérrez (Chiapas, México). Quehacer Cient Chis
2015; 10: 35–41.
Bonilla-Aldana DK, Suárez JA, Franco-Paredes C, Vilcarromero S, Mattar S, Gómez-Marín JE, et
al. Brazil burning! What is the potential impact of the Amazon wildfires on vector-borne and zoonotic emerging diseases? - A statement from an international experts meeting. Travel Med Infect Dis
2019; 31: 101474.
Gajate PP, Bottazzi MV, Pietrokovsky SM, Wisnivesky-Colli C. Potential colonization of the peridomicile by Triatoma guasayana
(Hemiptera:Reduviidae) in Santiago del Estero, Argentina. J Med Entomol
1996; 33(4): 635–639.
Gaspe MS, Fernández MD, Cardinal MV, Enriquez G, Rodriguez-Planes L, Macchiaverna N, et al
. Urbanization, risk stratification and house infestation with a major vector of Chagas disease in an endemic municipality of the Argentine Chaco. Parasites Vectors
2020; 13: 316.
Alvedro A, Gaspe MS, Milbourn H, Macchiaverna NP, Laiño MA, Enriquez GF, et al. Trypanosoma cruzi
infection in Triatoma infestans
and high levels of human–vector contact across a rural-to-urban gradient in the Argentine Chaco. Parasites Vectors
Gürtler RE, Cécere MC, Petersen RM, Rubel DN, Schweigmann NJ. Chagas disease in north-west Argentina: association between Trypanosoma cruzi
parasitaemia in dogs and cats and infection rates in domestic Triatoma infestans. Trans R Soc Trop Med Hyg
1993; 87: 12–15.
Sandoval-Ruiz CA, Guevara R, Ibáñez-Bernal S. Household risk factors associated to infestation of Triatoma dimidiata
, the Chagas disease vector in Central Region of Veracruz, Mexico. Salud Publ Mex
2014; 56: 213–220.
Nieto-Sanchez C, Baus EG, Guerrero D, Grijalva MJ. Positive deviance study to inform a Chagas disease control program in southern Ecuador. Mem Inst Oswaldo Cruz
Carbajal-de-la-Fuente AL, Provecho YM, Fernández MDP, Cardinal MV, Lencina P, Spillmann C, Gürtler RE. The eco-epidemiology of Triatoma infestans
in the temperate Monte Desert ecoregion of mid-western Argentina. Mem Inst Oswaldo Cruz
Mazariego-Arana MA, Monteón VM, Ballinas-Verdugo MA, Hernández-Becerril N, Alejandre-Aguilar R, Reyes PA. Seroprevalence of human Trypanosoma cruzi
infection in diferent geografic zones of Chiapas, México. Rev Soc Bras Med Trop 2001; 34
Solís-Franco RR, Romo-Zapata JA, Martínez-Ibarra JA. Wild reservoirs infected by Trypanosoma cruzi
in the ecological park “El Zapotal”, Tuxtla Gutiérrez, Chiapas, México. Mem Inst Oswaldo Cruz
1997; 92: 163–4.
Jimenez-Coello M, Ortega-Pacheco A, Guzman-Marin E, Guiris-Andrade DM, Martinez-Figueroa L, Acosta-Viana KY. Stray dogs as reservoirs of the zoonotic agents Leptospira interrogans, Trypanosoma cruzi
, and Aspergillus
spp. in an urban area of Chiapas in southern Mexico. Vector-Borne Zoonotic Dis
Guillen-Ortega F, Pérez-Vargas A, Estrada-Suárez A, Moleres-Villegas J, Ricárdez-Esquinca J, Monteón-Padilla V, et al
. Anticuerpos contra Trypanosoma cruzi
en pacientes con miocardiopatía dilatada en Tuxtla Gutiérrez, Chiapas. Arch Cardiol Mex
(Supl. 3): 49–54.
Black CL, Ocaña S, Riner D, Costales JA, Lascano MS, Davila S, et al
. Household risk factors for Trypanosoma cruzi
seropositivity in two geographic regions of Ecuador. J Parasitol
2007; 93(1): 12–6.
[Figure 1], [Figure 2]