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| ABSTRACT |
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| INTRODUCTION |
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Because of the partial efficacy of existing drugs and the absence of a vaccine, the control of triatomine vectors is the only way to control Chagas disease in various countries of South America. In Mexico, the existence of a wide diversity of sylvatic vector species hampers the efficacy of the current control strategy, mainly based on insecticide pulverization in infested dwellings.
More accurate information regarding Mexican triatomine behavior and risk factors for infestation of human dwellings is also needed. In the whole country, 33 species of triatomines have been described, of which 3 principal species were recorded in occidental and central states: Triatoma longipennis (Usinger, 1939), Triatoma pallidipennis (Stal, 1872), and Triatoma picturata (Usinger, 1939).12,13 All three belong to the phyllosoma complex and are sylvatic vectors.14,15 The presence of T. longipennis and T. pallidipennis have been documented in human dwellings in the states of Morelos, Jalisco, Colima, and Nayarit.1520 However, most of the T. longipennis specimens were collected outdoors, with scarce intradomicilary populations, except in the state of Colima, where the vector was mainly collected in intradomicilary areas.20 Specimens were generally collected in brick or tile piles, chicken-coops, pigsties, and garbage dumps.
The epidemiologic importance of T. longipennis is supported by significant rates of human seroprevalence in areas where this vector is predominant and highly infected by T. cruzi.21 Although T. longipennis is rarely observed indoors and is mainly present in peridomicilary compounds, even in Chagas disease transmission areas, information about T. longipennis behavior in peridomicilary areas is still limited, and risk factors for peridomicilary infestation are not known.5,19
In the occidental and central parts of Mexico, the species of the phyllosoma complex are the most abundant. Specimens of Triatoma barberi, a species that belongs to the protracta complex, are occasionally found indoors, but they are not very abundant in the villages. Their real epidemiologic significance for Chagas disease transmission is unknown.14,18,19,22 However, in the southern part, T. barberi is a recognized domestic and peridomestic vector of T. cruzi.23
To better understand the peridomicilary infestation process by T. longipennis, a large entomologic and ethnographical survey was carried in Los Guerrero, a rural community in the Jalisco State (Mexico) where eight seropositive patients have been identified.24 Inhabitants occasionally report the presence of vectors inside their houses. Of 1,821 specimens collected in peridomestic structures, T. longipennis was the dominant species (93.2% of adults) and Triatoma barberi was the second most prominent (6.6%). The study of the entomologic index was submitted elsewhere.24 This study clarifies the nature of peridomicilary habitats of T. longipennis and further clarifies the risk factors of peridomestic area infestation.
| MATERIALS AND METHODS |
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Definition of the peridomestic area and its structures. Formerly, authors showed arbitrariness in discriminating peridomestic area boundaries. Some of them define the peridomestic area as the surface situated around living quarters with a radius of 10 to 100 m,17,25 whereas others do not refer to space but to artificial structures and define the peridomestic area as all of the structures built by men around the domiciles: chicken-coops, storage shelters, pigsties, etc.20,26 In this study, we define the peridomestic area (a private space organized and used by human around their domicile) as the full area around the house supporting permanent or temporary structures built and used by humans or by their domestic animals. When peridomestic areas were fenced, they were delimited by theses fences. Inside each peridomestic area, various items were recorded. They are referred to as follows. 1) Permanent (or built) structures (covered with a roof or not) are storage shelters, animal shelters, corrals, and chicken-coops. They have three different architectural patterns, with each one named in the local language: the closed ones have four walls and a door, the roofed-unclosed ones have three walls and no door, and the open ones have no walls. 2) Temporary (or mobile) structures are piles of wood, brick, tile, or various goods and ends. They can be displaced promptly but may remain in place for years. 3) Natural structures are trees (cultivated or not), rocks, and all kinds of cultivated plants. Trees where chicken rest fit in this class, as well as bird nests restricted to peridomestic trees. 4) Domestic animals are mammals, fowl, and birds. Mammals may be divided into small mammals (dog, cat, rabbit, and guinea pig) and farm mammals (goat, sheep, cow, pig, and horse). Birds kept inside cages were regarded as pets.
Survey design. From July to September 2003 (rainy season), a team of well-trained health workers, assisted by an entomologist, visited the peridomestic areas of the selected 100 dwellings, drew their limits, described their structures, interviewed their inhabitants, and captured triatomines. Permanent, temporary, and natural structures of each peridomestic area were recorded, numbered, plotted on the map, and described, following a standardized form. Density indexes (number of structures per 100 m2) were determined for each kind of structure. Distances from each peridomicilary structure to domicile were noted. A standard questionnaire was submitted to each householder concerning the number of inhabitants, age and origin, use of insecticide, and type and number of animals. Insects were collected by a direct manual search in the peridomestic area, using a flashlight but not a repellent product. The collection lasted the time necessary to visit all the available structures and to collect all the bugs present at each positive site. The captured insects were put in a labeled plastic flask with filter paper, using one flask per capture site. They were transported to the laboratory for morphologic identification according to the taxonomic keys of Lent and Wygodzinsky (1979) and for further processing (parasite infection rate, collection of wings, legs, and blood meals).27
Data analysis.
Data were computerized and statistically analyzed using the Statview program. The dependent variables were the absence or presence of T. longipennis, in 1) peridomicilary structures and 2) peridomestic areas. We considered a structure or a peridomestic area to be infested when at least one triatomine was captured. A total of seven independent variables were tested for association with the infestation of a given structure by
2 tests and Fisher exact tests (all multinomial except distance from the house). A total of 28 independent variables were tested in multivariate analyses for association with peridomestic area infestation. Parts of the variables were computerized as binomial variables (15): presence or absence of chicken-coop, corral, storage shelter in adobe, cattle, horse, pig, dog, cat, rabbit, and fowl; presence or absence of mesquite (Prosopis laevigata) and guamúchil (Pithecellobium dulce); use of insecticide inside house and in peridomicile and presence of more than one house in the peridomicile. Other data were computerized as continuous variables (13): age of dwellers, number of high walls (> 2 m) limiting peridomicile, distance from peridomicile to the surrounding fields, surface area of the peridomicile and domiciles, length of fence made in baked clay (adobe or brick), numbers of permanent structures, temporary structures, storage shelters, brick piles, tile piles, wood piles, and fruit trees.
Finally, 12 variables were chosen for multivariate logistic regression analysis because their unadjusted association with the dependent variable was significant (P < 0.05). The 12 variables chosen for the model were as follows: 1) distance to the natural environment, 2) surface of the peridomestic area, 3) presence of more than one house (two houses may share the same peridomestic area), 4) number of closed and roofed-unclosed storage shelters, 5) number of brick and tile piles, 6) length of clay fences (adobe and brick), 7) presence in the peridomestic area of an adobe storage shelter, 8) presence of a mesquite tree, 9) presence of a fowl, 10) presence of a horse, 11) age of the inhabitant, and 12) use of insecticide inside domicile. All selected variables were put in the model, and variables with a high P value were removed one by one until all the remaining variables were P
0.05. The previously excluded variables were included one by one in the most parsimonious model and eventually retained according to their significance. Finally, only significant independent variables remained in the model.
| RESULTS |
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The vegetation was not densely implanted in the village and was mostly composed of small fruit trees. The overall density index for trees was 0.88/100 m2. Trees were seldom used by fowl to rest or breed.
All the recorded domestic animals were present in the peridomestic area during the survey. They included a total of 400 mammals and 771 fowl. The majority of dwellings accommodated one or two dogs, one or two cats, and a few poultry (mean = 17 ± 11). Pigs (mean = 3 ± 1) were present in 21 houses, goats or sheep (8 ± 3) in 12 houses, cows (3 ± 1) in 15 houses, and horses in 16 houses. Only seven dwellings had rabbits. The density index was 0.54/100 m2 for small mammals, 0.59/100 m2 for farm mammals, and 1.98/100 m2 for fowl. Rodent feces were frequently observed during the triatomine search. Fowl were left wandering on the whole peridomicilary area, in neighboring peridomestic areas, and even in the street. They slept mainly in chicken-coops. Horses were generally kept in a large corral and had a roofed open structure to rest.
Collection and peridomicilary habitats of triatomines.
Of 629 structures, 369 were visited. The other were not because they obviously had no hiding places for bugs (concrete walls of corrals), they were too large to be searched (high brick piles), or they were locked (closed storage shelters). The numbers of visited structures remained generally proportional to each type (Figure 1
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60 insects) of T. longipennis were observed in five structures. It is worth noting that the infection rates of the two species are similar and reach 46% for the entire population (nymphs and adults).
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The presence of domestic mammals or poultry near a peridomicilary structure has no significant effects on its infestation with T. longipennis (P = 0.15). None of the observed colonies were associated with an animal except the two largest ones with dogs.
Twenty sites were infested with T. barberi, six of which were heavily infested (1024). No statistical analysis was performed because of the small number of registered sites. Nevertheless, the features of peridomicilary habitats presented some trends. T. barberi was captured more often in storage shelters and on baked clay material. It was not associated with the presence of any animals, and it was not localized at a particular distance from the domicile. It was associated with T. longipennis in 17 sites, with a significant co-occurrence. Indeed, according to the frequencies of the infested sites by T. longipennis and T. barberi in the village, and the null hypothesis of absence of association (random co-occurrence) of the two species, the expected frequency of the sites with the two species was 0.016, corresponding to six sites. The
2 test performed for observed and expected values gave a significant P < 0.01.
Characteristics of the peridomestic areas associated with T. longipennis infestation.
A total of 60 peridomestic areas were infested with T. longipennis and 16 with T. barberi. Descriptive factors associated with T. longipennis infestation are shown in Tables 2
and 3
(binary and continuous variables, respectively). They relate to the central localization of the peridomestic areas (distance to field
200 m, P < 0.0185) and to the peridomestic area composition (number of storage shelters, numbers of brick and tile piles, number of houses in dwelling, length of fences made with brick or adobe, presence of an adobe storage shelter, and presence of fowl) and suggest a role of human habits on peridomestic area infestation (age of the inhabitant, use of insecticide in the house, and presence of horses, which is a mean of transport in Los Guerrero).
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200 m. The other factors were not significant in the model.
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| DISCUSSION |
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Although available information regarding the potential habitat of T. longipennis in peridomestic area is scarce, previous studies have already shown that the vector was regularly collected in brick and tile piles, chicken-coops, pigsties, and garbage dumps.15,19 Our results are partly consistent with previous observations. At Los Guerrero, T. longipennis was also mainly collected inside the storage shelters (where garbage dumps are numerous), corrals, chicken-coop, and piles of brick and tiles. On the contrary, none of the pigsties were infested, because they were frequently built with low cement walls and left no hiding place for insects. The pigsty characteristics were probably different in the villages visited in previous works. This study is the first one in Mexico to focus on the peridomestic habitats of T. longipennis and to state the relative infestation rates of each structure. In the Los Guerrero context, T. longipennis was more often associated with permanent structures (storage shelters, corrals, chicken-coops) than with temporary ones and with storage shelters than with piles of brick and tile. The main material for both was clay, and they were both numerous. Closed (or roofed-unclosed) storage shelters provided quiet places and good shelter from wind and rain, whereas piles of material were more often exposed to bad weather. These results fit with previous data collected in the state of Colima indicating that triatomines of phyllosoma complex are mainly captured in shaded and dry areas of the peridomestic area.20 However, this study in Los Guerrero was performed during the rainy season, and it is possible that results would be slightly different during the dry months. The survey also confirmed that T. longipennis, a terrestrial vector, occupies preferably mineral materials (brick, tile, adobe) present in the peridomestic area. However, the vector may build colonies in other materials (such as wood) and thus is able to adapt to new ecotopes in the peridomicilary context.
In Los Guerrero, the organization of human dwellings is quite homogeneous, and the majority of peridomestic areas harbor potential habitats for triatomines. Only four peridomestic areas had no storage shelters and no piles of brick and tile. Therefore, what are the risk factors that determine the infestation of a specific peridomestic area? Only two studies have analyzed the risk factors for peridomestic area triatomine infestation in Mexico. They both concern T. pallidipennis, another vector of the phyllosoma complex that was collected indoors and outdoors in the rural town of Chalcatzingo (Morelos State).18,28 The risk factors for peridomicilary infestation related mainly to number of animals (rabbit, dog, cat) and the presence of junk piles. In Los Guerrero, the risk factors were slightly different. The bivariate analyses and the logistic regression model confirmed that the accumulation of storage shelters and piles of brick and tile in peridomicilary area were risk factors. Their presence in a peridomiciliary area increased by two the odds of being infested. Finally, the presence of more than one house in the peridomestic area also increased the odds of infestation by a factor of 4. It should be pointed out that the overall surface area of the habitat unit (domicile and peridomicile) was not significantly associated to the peridomestic area infestation and that the peridomestic areas with two or more houses did not significantly differ (P > 0.1) from those with one house in term of superficial area, animal numbers, number of permanent and temporary structures, and location in the village. The pile of brick or the closed shelter presented risks by themselves (they are good habitats for triatomine) but also by their accumulation (more shelters for insects and greater difficulty to search and eliminate them). These results fit with the fact that open structures are less infested than closed ones, as mentioned above. Dwellings located in the central part of the village (distance to field
200 m) were not associated with higher number of storage shelter, brick or tile piles, or number of houses in the peridomicile. However, their odds of being infested was three times higher than the dwelling located at < 200 m from the fields. We suggest that structural organization of the village plays a more important role in the infestation process than the role at each specific structure. This probably relates to microclimatic conditions, favorable for T. longipennis, which are not yet clearly elucidated.
Furthermore, there is no clear association of animal presence and animal numbers with peridomestic area infestation. However, the presence of rats was noted during the survey, and a first analysis in our laboratory indicated that the rat is the main blood-meal source of T. longipennis (
40.5% of the identified blood-meal sources) in Los Guerrero village.29 Rats seem to be an important host for T. longipennis and may easily hide in closed storage shelters, in huge piles of brick, and in overcrowded peridomiciles, where there are numerous places to hide.
Although this study provides no clear evidence for human activities playing a role on triatomine infestation, some factors such as the presence of horses and fowl or use of insecticides should be considered in further studies, focusing on dispersion of triatomines. Their importance may be occulted in this study, designed to analyze the risk factors of triatomine installation in peridomicilary areas.
In this study, it was not possible to identify the familiar peridomestic habitat of T. barberi because the number of infested sites was too small for statistics. Remarkably, this species was mainly collected with T. longipennis (sympatric condition). Past reports have provided evidence of remarkable host specificity of the species belonging to the protracta complex.30 Indeed, T. barberi was first reported around the house.25 Later, this species was considered to be completely domiciliated because sylvatic specimens were not seen.12 Last, a predictive model of geographical distribution of triatomines species showed that T. barberi presents a high overlapping location with Neotoma mexicana.31 Also, specimens of this species were found in cornfields in Morelos state and in rocks (Oaxaca State).28,31 During a survey in the Ameca valley (20022005), we captured 368 sylvatic triatomines (adults and nymphs) in rock pile boundary walls, but no T. barberi specimens were collected in this ecotope.32 Whatever the primitive ecological niche of T. barberi is, these results showed its trend toward colonization of a diversity of peridomestic sites in sympatric conditions with other species. Moreover, previous studies in the village of Tepehuaje de Morelos situated 5 km far from Los Guerrero showed that intradomicilary colonization was absent.16 The exact role of this secondary vector species in the transmission of Chagas disease remains to be determined.
The results offered in this paper provide some information about the peridomicilary ecotope of T. longipennis, point out accumulation of insect habitats as the main risk factor, suggests a probable role of the urban structure in the infestation process, confirms the trend of T. barberi toward colonization, and indicates that a better comprehension of the triatomine infestation process is related to better knowledge of peridomicilary ecology. As described for other triatomines species, further population genetics studies will contribute to increasing our understanding of the movement of populations (expansion, colonization) between ecotopes and different ecosystems.
Received November 16, 2005. Accepted for publication November 27, 2006.
Financial support: This study received financial support from the PAHO, Communicable Disease programme, TDR Grant ID A30442, and the Institut de Recherche pour le Développement (IRD).
* Address correspondence to Simone F. Brenière, Institut de Recherche pour le Développement (IRD), UR 008 Pathogénie et Epidémiologie des Trypanosomatidés, 911 Av. Agropolis, BP 64501, 34394 Montpellier Cedex 5, France. E-mail: breniere{at}mpl.ird.fr ![]()
Authors addresses: Annie Walter, Institut de Recherche pour le Développement (IRD), UR016, Control et Caractérisation des Populations de Vecteurs, 911 Av. Agropolis, BP 64501, 34394 Montpellier Cedex 5, France, E-mail: annie.walter{at}ird.fr. Felipe Lozano-Kasten, Centro Universitario de Ciencias de la Salud, Departamento de Salud Pública, AP 2-136, Universidad de Guadalajara, Guadalajara, Jalisco, Mexico, E-mail: f_lozano_k{at}hotmail.com. Marie-France Bosseno, Institut de Recherche pour le Développement (IRD), UR 008 Pathogénie et Epidémiologie des Trypanosomatidés, 911 Av. Agropolis, BP 64501, 34394 Montpellier Cedex 5, France, E-mail: Marie-France.bosseno{at}mpl.ird.fr. Eloy Gualberto Castillo Ruvalcaba, Centro Universitario de Ciencias de la Salud, Departamento de Salud Pública, AP 2-136, Universidad de Guadalajara, Guadalajara, Jalisco, Mexico, E-mail: eloy_castillo{at}hotmail.com. Margarita Soto Gutierrez, Centro Universitario de Ciencias de la Salud, Departamento de Salud Pública, AP 2-136, Universidad de Guadalajara, Guadalajara, Jalisco, Mexico, E-mail: msg0059_2001{at}hotmail.com. Christian Eloy Montañ Luna, Centro Universitario de Ciencias de la Salud, Departamento de Salud Pública, AP 2-136, Universidad de Guadalajara, Guadalajara, Jalisco, Mexico, E-mail: Chemolu @hotmail.com. Françise Baunaure, Institut de Recherche pour le Développement (IRD), UR 008 Pathogénie et Epidémiologie des Trypanosomatidés, 911 Av. Agropolis, BP 64501, 34394 Montpellier Cedex 5, France, E-mail: fbaunaure{at}univ-montp2.fr. Pascale Phéinas, Institut de Recherche pour le Développement (IRD), UR003, Travail et Mondialisation, 911 Av. Agropolis, BP 64501, 34394 Montpellier Cedex 5, France, E-mail: phelinas{at}ird.fr. Ezequiel Magalló-Gastéum, Centro Universitario de Ciencias de la Salud, Departamento de Salud Pública, AP 2-136, Universidad de Guadalajara, Guadalajara, Jalisco, Mexico, E-mail: mge28525{at}cucs.udg.mx. Simone F. Brenière, Institut de Recherche pour le Développement (IRD), UR 008 Pathogénie et Epidémiologie des Trypanosomatidés, 911 Av. Agropolis, BP 64501, 34394 Montpellier Cedex 5, France, E-mail: breniere{at}mpl.ird.fr.
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