|ABSTRACT||The prevalence of Trypanosoma cruzi infection in Triatoma infestans, Triatoma guasayana, and Triatoma sordida was evaluated in Amamá and other neighboring rural villages in northwestern Argentina for five years after massive spraying with deltamethrin in 1992 and selective sprays thereafter. Local residents and expert staff collected triatomines in domiciliary and peridomestic sites. During 19931997, the prevalence of T. cruzi was 2.4% in 664 T. infestans, 0.7% in 268 T. guasayana, and 0.2% in 832 T. sordida. T. cruzi infection was more frequently detected in adult bugs and in triatomines collected at domiciliary sites. The infected T. guasayana and T. sordida were nymphs and adults, respectively, captured at peridomestic sites. The prevalence of T. cruzi infection in T. infestans decreased from 7.7% to 1.5% during the surveillance period, although that change was not statistically significant. Comparison of T. infestans infection rates before the control program and during surveillance showed a highly significant decrease from 49% to 4.6% in bedrooms, as well as a fall from 6% to 1.8% in peridomestic sites. Because of its infection with T. cruzi and frequent invasion of domiciliary areas and attacks on humans and dogs, T. guasayana appeared implicated as a putative secondary vector of T. cruzi in domestic and peridomestic sites during the surveillance period. T. sordida was the most abundant species, but it was strongly associated with chickens and showed little tendency to invade bedrooms.|
Triatoma infestans, the main vector of Trypanosoma cruzi, is currently the subject of an elimination program through the massive spraying of residual insecticides as part of the Southern Cone Initiative, which includes the countries of Argentina, Bolivia, Brazil, Chile, Paraguay, Peru, and Uruguay (1). In Argentina, controlling T. infestans in the province of Santiago del Estero, in the northwestern part of the country, has been historically difficult (2). Young men from the province have had nearly the highest rate of seropositivity for T. cruzi among those drafted into military service in Argentina (3). In a five-year follow-up of rural villages in Santiago del Estero after a single massive spray of deltamethrin and selective treatments thereafter, T. infestans was not eliminated locally but its abundance was reduced to very low levels in bedroom areas (4, 5). Peridomestic sites were the principal source of T. infestans and the origin of domiciliary reinfestations. In this study we describe the initially sharp and then sustained decline in the prevalence of T. cruzi in T. infestans as a consequence of the control program.
Several species of sylvatic or peridomestic triatomines that are not control targets at present might turn into secondary vectors of T. cruzi during or after the elimination of T. infestans (6). In the Southern Cone, Triatoma sordida and Triatoma guasayana have been considered potential candidates to replace T. infestans in the domestic environment (79). It is not known if those triatomines maintain or contribute to the transmission of T. cruzi in domiciliary and peridomestic sites when T. infestans populations are absent or exist in only small numbers.
The prevalence of T. cruzi infection in domiciliary populations is closely connected to the risk of human infection. Bug infection rates depend on the prevalence rates of human and mammal infection and the level of contact between hosts and vectors (10). Part of a wider project, this study had two objectives: 1) assessing the long-term effects of control actions on the prevalence of T. cruzi in T. infestans populations from domiciliary and peridomestic sites and 2) evaluating the importance of T. sordida and T. guasayana in peridomestic or domestic sites as vectors of T. cruzi during the surveillance phase. These results contribute to understanding the dynamics of transmission of T. cruzi by primary and secondary triatomine vectors during the surveillance phase.
The effects that the control program had on house recolonization by T. infestans and seropositivity for T. cruzi in the human population will be reported elsewhere.
MATERIALS AND METHODS
Field studies were carried out in five rural villages in the province of San tiago del Estero, Argentina: Amamá, Trinidad, Mercedes, Villa Matilde, and Pampa Pozo (27° S, 63° W). Previous articles described the area and its history of infestation by T. infestans (5, 11). Amamá is located on a paved road, 610 km from the other villages. Those villages consist of two geographic clusters, Trinidad-Pampa Pozo and Mercedes-Villa Matilde, which are connected with each other by dirt roads.
Homes in the study communities typically had adobe walls, a thatched roof, one or two bedrooms, and a front porch. Such a dwelling covered by a single roof defined the domiciliary (bedroom) area. In the cases where a storeroom or a kitchen shared the same roof as a bedroom, those spaces were also considered part of the domiciliary area since there was no absolute separation between these adjacent rooms. The peridomestic area consisted of the patio; storerooms, kitchens, pens, and other structures that were not connected to the roof that was over the bedrooms; and other potential vector hiding places located within the area of human activity, including trees, pieces of wood, etc.
Before the October 1992 spraying campaign, in March of that year, two experts from the National Chagas Service (NCS) searched all the houses in Amamá, Trinidad, and Mercedes for live T. infestans. The experts spent 30 min per house in the bedroom area (one person-hour total per house) and 10 min per house in peridomestic sites (1/3 person-hour total per house) (5, 12). Searches were assisted with a flushing-out agent (0.2% tetramethrin, Icona®, Buenos Aires). Findings of T. guasayana and T. sordida in peridomestic sites were disregarded because these species were not considered control targets at that time. After the deltamethrin spraying in October (see Control actions below), local residents and research team members collected the triatomines knocked down during the first 24 h after treatment. These bugs provided further evidence of house infestation and served as samples to estimate bug infection rates.
In mid-December 1992, an average of three (range, two to five) sensor boxes (Biosensor Detector de Vinchucas, Biocientifica de Avanzada®, Buenos Aires) were placed indoors or on the porch of each house to monitor reinfestation by triatomine bugs, as described elsewhere (5). All the sensing devices were inspected for evidence of bug infestation every six months from May 1993 through December 1997. Every 12 months from October 1993 through December 1997 three skilled bug collectors from the NCS searched for triatomines in the bedroom areas and in the peridomestic areas using 0.2% tetramethrin as before. Peridomestic structures were 4100 m away from the bedrooms (i.e., domiciliary areas) and included kitchens, storerooms, goat and pig pens, and other likely refuges for triatomines. For 30 min per house, two men searched the bedrooms (one person-hour total per house) while another man searched peridomestic sites (1/2 person-hour per house). Additional searches for bugs were carried out at peridomestic sites each May from 1995 through 1997. Beginning in May 1993, each household received labeled self-sealing plastic bags to keep any triatomine that the residents captured in domiciliary or peridomestic sites. At each six-month visit, residents were asked for the bugs they had collected and for information on where they had captured them. However, since most of the triatomines the residents collected were dead when the research team received them, these bugs were not examined for infection. The finding of at least a T. infestans nymph was taken as an indication of colonization.
The number, stage, location, and species of triatomine collected at each house in each survey was recorded on independent data sheets. At the field laboratory, all the bugs were later identified by species and stage, using standard keys (13, 14). Live or moribund triatomines were individually examined for T. cruzi infection within 1015 days of capture, except in December 1997, when feces from three T. guasayana and T. sordida collected at the same site were examined in pools. When a positive pool was detected, the bugs were reexamined individually. In December 1997, extra efforts were made to examine as many bugs as possible. Fecal drops obtained by abdominal compression from each bug were diluted with one drop of saline solution, covered with a 22x22-mm cover slip, and thoroughly examined at 400x magnification for active trypanosomes. T. cruzi and Blasthocrithidia sp. were diagnosed on the basis of their morphology.
In mid-October 1992, following standard procedures, NCS staff sprayed all 93 existing houses in Amamá, Trini - dad, and Mercedes and their peridomestic outbuildings with deltamethrin (2.5% suspension concentrate at 25 mg a.i./m2 of sprayed surface). After that, searches for residual foci were carried out, as were selective insecticide treatments (4). The neighboring villages of Villa Matilde and Pampa Pozo, totaling 13 houses, were added to the study after being sprayed with deltamethrin between October 1993 and May 1994.
From 1993 to 1995, all sites with T. infestans nymphs, but not other triatomines, were treated focally with deltamethrin as before. For example, when a goat pen was found recolonized by T. infestans, only this site was treated. The first treatment during the surveillance phase was carried out in peridomestic sites of a house in late 1993.
In November 1995, an additional step in the control process was taken, assessing if there were still any bugs in the houses with triatomine dejecta in the sensing devices. The measure may also have contributed to controlling any triatomine reinfestation in the bedrooms. The 31 houses that had had triatomine fecal smears in the sensor boxes in the preceding 12 months or where the residents reported the bedrooms as infested were treated with one or two insecticide (deltamethrin, g-BHC and DDVP) fumigant canisters (Agufog, Aguvac®, Buenos Aires) per bedroom. Two houses too open for effective treatment with fumigant canisters were sprayed with deltamethrin. Additional sprayings were carried out in peridomestic sites at 8 homes, in the bedrooms of 1 house, and in both areas at another house.
A progressive transfer of surveillance activities from the research team to the affected communities started in November 1995. Three four-hour workshops were conducted in the schools of Amamá and Mercedes, in November 1995, May 1996, and November 1996. In these workshops, local residents were briefed on the main results of the research project. They also learned how to assemble and inspect sensor boxes, apply fumigant canisters, and spray their homes and outbuildings with insecticide. Members of 47 of 51 families (92%) from Amamá and 43 of 54 families (80%) from the other villages participated in at least one of the workshops. Each geographic cluster chose a member who would receive notifications of T. infestans captures, store the insecticide and sprayer, keep records, and help affected families treat their homes. The elected leaders were three men 3045 years old, two of whom already held one of the scarce paid permanent jobs with the provincial government, but doing some other kind of work.
During 1996, deltamethrin spraying was done in the bedrooms of 16 houses, in peridomestic sites at 3 houses, and at both those locations at 4 houses. In addition, fumigant canisters were applied in 4 other houses.
In 1997, deltamethrin sprayings were done in bedrooms at 7 houses, plus in both the bedrooms and the peridomestic sites at 13 other houses.
The relationships between infection with T. cruzi (the dependent variable) and survey year were studied by maximum likelihood logistic regression analysis using the logistic-binomial model for indistinguishable data from EGRET software (15). Logistic regression analysis was chosen instead of standard linear regression because the data for T. cruzi infection are binary for an individual bug, and for a sample of bugs yield fractions between 0.0 and 1.0 that tend to have a binomial distribution. Infected was indexed as 1, and noninfected as 0. Survey years were enumerated from 1 to 5.
Of 1 764 triatomines examined for infection during 19931997, only 20 bugs (1.1%) were infected with T. cruzi (Table 1). Over that period, the prevalence of T. cruzi was 2.4% in T. infestans, 0.7% in T. guasayana, and 0.2% in T. sordida, and differed significantly among species, according to the chi-square test (c2 = 15.9, degrees of freedom [df] = 2, P < 0.001). The percentage of infection was significantly greater for T. infestans collected in domiciliary sites (4.6%) than in peridomestic sites (1.8%) (c2 = 3.96, df = 1, P = 0.046). The 20 infected triatomines were collected at 15 different houses; a single infected bug was captured at each of 12 houses, 2 infected bugs at each of 2 houses, and 4 infected bugs at a single house over a period of two surveys. Blastocrithidia sp. was detected in 1 female T. guasayana and 2 male T. sordida.
Triatoma infestans was the only species infected with T. cruzi in bedroom areas (Table 1). Nearly half (7/16) of all the infected T. infestans were collected there (in one case, two infected bugs were found in a single home). Three of these six findings of infected T. infestans in bedroom areas were isolated adults captured in houses that had no evidence of current or subsequent domiciliary colonization, therefore suggesting recent immigration from elsewhere. In peridomestic sites, six of the seven findings (86%) of infected T. infestans occurred in sites colonized by this species at the time of capture. The infected peridomestic T. infestans were caught in two different kitchens, a storeroom, a patio, a bathroom, a goat pen, and a timber pile. These seven findings comprised nine infected T. infestans bugs because three bugs were found at a single residence.
Trypanosoma cruzi was detected in 15 adults, 4 fifth-instar nymphs, and 1 fourth-instar nymph (Table 2). In T. infestans, the prevalence of T. cruzi infection steadily increased from 0.0% in second- and third-instar nymphs to 5.9% in adult bugs. Only 2 T. guasayana fifth-instar nymphs (captured in May 1995 in a chicken nest made with piled branches and pieces of clothing) and 2 T. sordida males (captured in 1996 and 1997, in a pig pen and a tree where chickens roosted) were infected with T. cruzi (Table 2). These 4 all came from peridomestic colonies of the respective species in Amamá.
The overall prevalence of T. cruzi infection in T. infestans decreased from 7.7% in 1993 to 1.5% in 1997 (Table 3), though the change was not statistically significant (c2 = 2.96, df = 1, P = 0.086). Bug infection rates did not differ significantly among Amamá (3%), Trinidad-Pampa Pozo (3%), and Mercedes-Villa Matilde (1%) (c2 = 3.4, df = 2, P = 0.18). Infected T. infestans were found in five of eight surveys during the surveillance period in Amamá, in two surveys during the third and fourth year after spraying in Trinidad-Pampa Pozo, and only once during the fourth year after spraying in Mercedes-Villa Matilde. All 13 houses in Villa Matilde and Pampa Pozo and a logging operation near Trinidad were found infested by T. infestans in 1993, and none had been sprayed with insecticides. The prevalence of T. cruzi in the domiciliary T. infestans (24/84, or 29%) found in these 13 unsprayed houses was significantly higher than what was found in the domiciliary sites of the study villages over the five-year period (4.6%) (c2 = 27.5, df = 1, P < 0.001).
The percentage of T. cruzi-infected T. infestans correlated positively and significantly with the log-transformed total number of T. infestans collected in bedroom areas (r = 0.72, n = 9, P < 0.05), but not in peridomestic sites (r = 0.03, n = 9, P > 0.1) (Figure 1).
Figure 2A compares the prevalence of T. cruzi in T. infestans from Amamá and the four other control program villages before the deltamethrin spraying in 1992 and during the triatomine surveillance period of 19931997. Bug infection rates decreased significantly from 49% (646/1 316) to 4.6% (7/153) in bedroom areas (c2 = 110, df = 1, P < 0.001). In peridomestic sites, rates fell from 6% (19/328) to 1.8% (9/511) (c2 = 10.1, df = 1, P < 0.002). The overall prevalence of infection for the two types of sites decreased by a factor of 17, from 40.5% (665/1 644) before spraying to 2.4% (16/664) during the surveillance period. For comparison, Figure 2B shows that in 1984, before Amamá was sprayed with delta-methrin for the first time, the domiciliary T. infestans infection rate in the village was 57% (471/833). Without any further control actions, reinfestation levels later recovered, reaching a prevalence rate of infection of 21% (108/514) in 19881989 (16).
Among the main results of this research are that: 1) T. cruzi was detected mainly in T. infestans in both the domiciliary and peridomestic sites, and marginally in T. guasayana and T. sordida in peridomestic sites, 2) the control program initially produced a sharp reduction and then a sustained decline in the prevalence of T. cruzi in T. infestans, and 3) T. guasayana appeared implicated as a putative secondary vector of T. cruzi in domestic and peridomestic sites during the surveillance phase.
Most triatomines infected with T. cruzi were collected in bedroom or peridomestic areas where dogs, cats, and humans rest at night. The source of these triatomine infections may be traced to feeding on infected dogs or cats, which are more infective to bugs than humans are (10). In contrast, all three species of triatomines frequently captured in goat or pig pens and chicken coops were rarely infected with T. cruzi in our study area and elsewhere (17).
The impact of the control program on the prevalence of T. cruzi in T. infestans was greater in domiciliary sites (bug infection rates falling from 49% to 4.6%) than in peridomestic sites (rates falling from 6% to 1.8%). The control programs effectiveness was also reflected in much lower rates of infection by instar during the surveillance period. These low infection rates in both the domiciliary and peridomestic sites were likely associated with low T. infestans densities and low rates of domiciliary recolonization as a consequence of selective deltamethrin sprays in the study villages combined with massive sprays in the province of Santiago del Estero. These interventions brought about a steady, very similar decline in the prevalence of dogs seropositive for T. cruzi in all five villages, from 65% in 1992 to 39% in 1994 and 15% in 1996 (18). Moreover, no autochthonous cases of seroconversion for T. cruzi were detected among local children (unpublished results). As a further indication of the impact of sustained surveillance (2), the 4.6% prevalence of T. cruzi in domiciliary T. infestans achieved in 19931997 was nearly 5 times lower than the 21% level of 19881989, when there was no surveillance (16). Therefore, even though the control program did not eliminate T. infestans and there was even a relative resurgence in 19961997, the actions implemented produced a sustained decline in the prevalence of T. cruzi in T. infestans that was accompanied by a progressive decline in dog and human infection rates. Given that rates of both dog and human seropositivity for T. cruzi were nearly the same for all five villages, it remains unclear why infected T. infestans were detected more frequently in Amamá than in the other villages and why all the infected T. guasayana and T. sordida came from Amamá.
Our study shows a direct relationship between the total number of T. infestans collected in domiciliary areas in each survey and the percentage of T. cruzi-infected T. infestans in these samples over time. This finding is in line with data recorded before the spraying campaign, when each house was taken as the unit of analysis (10). Regardless of the underlying mechanism giving rise to such relationships, the clear implication is that reduction of T. infestans abundance to low levels involves a decrease in the proportion of infected bugs.
In peridomestic sites, T. infestans had a low prevalence of infection both before and during the control program, indicating that T. cruzi transmission there had a lower intensity than in bedroom areas. However, the total number of infected triatomines of any species collected in peridomestic sites was nearly double that in the bedrooms, and nearly all of these peridomestic triatomines belonged to established peridomestic colonies. This strengthens the view that the infected bugs likely acquired the infection in those peridomestic ecotopes. T. infestans and the other triatomines more rapidly recolonized peridomestic sites than they did bedroom areas. Possible reasons for that may have been that the effectiveness of insecticidal sprays in peridomestic sites was reduced; that the peridomestic area was large and housed an abundant supply of refuges and hosts (4), including dogs and cats; and that the flushing-out method had a reduced sensitivity in complex ecotopes.
Triatoma guasayana was very abundant in peridomestic ecotopes, mainly goat pens, and frequently invaded but did not colonize bedroom areas (5). However, the two infected T. guasayana found were nymphs from peridomestic colonies sited 1030 m away from bedrooms, which makes it unlikely that they came from other houses or sylvatic ecotopes due to the nymphs presumed limited dispersal capacity. Researchers studying peridomestic ecotopes of the village of Trinidad collected a few adult T. guasayana dispersing by flying that were infected with T. cruzi (19), but the infections may have originated elsewhere. Similarly, in sylvatic ecotopes in and around Trinidad in 1993, after deltamethrin spraying, the prevalence of T. cruzi infection in a mixed sample of T. guasayana and T. sordida, as determined by microscopic examination of feces, was 0.6% (1/164). That prevalence rose to 10.9% when groups of bugs were examined by polymerase chain reaction (PCR) (20). In our study, microscopic examination of triatomine feces likely underestimated the true bug infection rates. However, according to a paired comparison with PCR (21), this bias might be smaller for T. infestans than for other triatomines. In addition, a T. infestans found microscopically to be infected with T. cruzi was also weakly positive by PCR in a blind examination performed by Dr. Jacqueline Búa of the Dr. Mario Fatala Chabén National Parasitology Institute (unpublished research). T. guasayana appeared implicated as a putative secondary vector of T. cruzi in domestic and peridomestic sites during the surveillance phase and a potential link between transmission cycles of T. cruzi encompassing sylvatic, peridomestic, and domestic ecotopes because of: 1) its infection with T. cruzi, 2) frequent invasion of domiciliary areas and attacks on humans and dogs, and 3) its significant association with young native dogs seropositive for T. cruzi born during the surveillance period (18). More data are needed to assess the actual infection rates of T. guasayana, using enhanced detection procedures and carefully designed sampling programs.
Triatoma sordida was the most abundant triatomine in peridomestic areas, where it was strongly associated with trees where chickens roosted. T. sordida rarely attacked humans and showed a low rate of domiciliary invasion (5). These characteristics reduce its potential contribution to T. cruzi transmission and may explain its low prevalence of infection. Similar results were recorded in northeastern Argentina, where T. sordida invaded but did not colonize domiciliary areas and was not infected with T. cruzi (22). In Brazil, long-term surveillance data showed very low rates of T. sordida domiciliary colonization, and T. cruzi infection rates ranging from 1%4% (9, 23). In certain parts of Bolivia, however, the pattern may be quite different (24).
Our study was initially focused on T. infestans. Therefore, we did not collect baseline data to assess the impact of control actions on the prevalence of T. cruzi in T. guasayana and T. sordida. To our knowledge, the present data may be the first of such an extended nature for these species in Argentina.
The peridomestic environment includes key sites to eliminate triatomine infestations and T. cruzi transmission. Peridomestic ecotopes: 1) are more easily colonized by triatomines than domiciliary areas, 2) sustain abundant populations of different species of triatomines that invade domiciliary areas and attack humans and domestic animals, and 3) host such important reservoirs of T. cruzi as dogs, cats, and rodents. Triatomine control or elimination programs should include combined insecticidal sprays and environmental management measures specifically designed for peridomestic sites.
Acknowledgments. This study was supported by grants from the Rockefeller Foundation, New York, to Rockefeller University, New York, for a collaborative research project on modeling transmission dynamics and control of Chagas disease in Argentina (Ricardo Gürtler, Joel E. Cohen, and Roberto Chuit, principal investigators); from the Fundación Alberto J. Roemmers, Argentina; and from the University of Buenos Aires. We thank Dr. Abel Hurvitz and his staff at the National Chagas Service of Argentina for their active support throughout this study. For their expert assistance during the fieldwork, thanks go to Griseldo Roldán, Isaac Ochoa, Emilio Vigil, Juan Luna, Humberto Pérez, Aníbal Rodríguez, and Mario Arrieta, all of the NCS. Dr. Jacqueline Búa kindly performed PCR assays. Mrs. María Mo yano and Mr. Omar Sitatti generously provided field accommodations.
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Manuscript received on 15 January 1998. Revised version accepted for publication on 22 December 1998.
Infección por Trypanosoma cruzi en Triatoma infestans y otros triatómidos: efectos a largo plazo de un programa de control en una zona rural del noroeste de Argentina
|Durante los cinco años posteriores a una fumigación masiva con deltametrina realizada en 1992 y seguida de fumigaciones selectivas, se investigó la prevalencia de la infección por Trypanosoma cruzi en Triatoma infestans, Triatoma guasayana y Triatoma sordida en Amamá y otras poblaciones rurales vecinas del noroeste de Argentina. Los triatómidos fueron recogidos en los domicilios y en el área peridoméstica por los propios residentes y por personal experto. Durante el quinquenio 19931997, la prevalencia de T. cruzi fue de 2,4% en 664 T. infestans, de 0,7% en 268 T. guasayana y de 0,2% en 832 T. sordida. La infección por T. cruzi se detectó con mayor frecuencia en las chinches adultas y en los triatómidos recogidos en los domicilios. T. guasayana y T. sordida fueron, respectivamente, ninfas y adultos recogidos en el área peridoméstica. Durante el período de vigilancia, la prevalencia de la infección por T. cruzi en T. infestans disminuyó de 7,7% en 1993 a 1,5% en 1997, aunque este cambio no fue estadísticamente significativo. La comparación de las tasas de infección de T. infestans antes del programa de control (1992) y durante el período de vigilancia (19931997) reveló una disminución altamente significativa, de 49% a 4,6%, en los dormitorios y también en las áreas peridomésticas (de 6% a 1,8%). Debido a su infección por T. cruzi y a su frecuente invasión de las áreas domésticas con ataques a los humanos y a los perros, T. guasayana parecía estar implicado como vector secundario de T. cruzi en las áreas domésticas y peridomésticas durante el período de vigilancia. T. sordida fue la especie más abundante, pero estaba estrechamente asociada a los pollos y mostró escasa tendencia a invadir los dormitorios.|
1 Universidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales, Departamento de Ciencias Biológicas, Laboratorio de Ecología General. Send correspondence and requests for reprints to: R.E. Gürtler, Departamento de Biología, Ciudad Universitaria, 1428 Buenos Aires, Argentina. Fax: 54-11-4576-3384. E-mail: email@example.com
2 Servicio Nacional de Chagas, Centro de Reservorios y Vectores de la Enfermedad de Chagas, Córdoba, Argentina.
3 Academia Nacional de Medicina, Centro de Investigaciones Epidemiológicas, Buenos Aires, Argentina.