Acta Tropica 97 (2006) 331–338

Epidemiological risk for Trypanosoma cruzi transmission by species of Phyllosoma complex in the occidental part of Mexico Ezequiel Magall´on-Gast´elum a , Felipe Lozano-Kasten a , Margarita Soto Gutierr´ez a , Angelica Flores-P´erez b , Beatriz S´anchez b , Bertha Espinoza b , Marie-France Bosseno c , Simone F. Breni`ere c,∗ a

b

Departamento de Salud P´ublica del centro Universitario de Ciencias de la Salud, Universidad de Guadalajara, Apartado postal 4-119, Guadalajara, Jalisco, M´exico Instituto de Investigaciones Biom´edicas, Universidad Nacional Aut´onoma de M´exico, AP 70228, CP 04510, M´exico D.F. c Institut de Recherche pour le D´ eveloppement (IRD), UR 008 Patholog´enie et Epid´emiologie des Trypanosomatid´es, BP 64501, CP 34394 Montpellier, France Received 28 June 2005; received in revised form 15 December 2005; accepted 2 January 2006

Abstract Domestic and peridomestic triatomine populations were collected in three rural Mexican communities of Jalisco, Nayarit and Zacatecas states. Triatoma longipennis and T. picturata (Phyllosoma complex) were the principal species unequally distributed in the villages: T. longipennis was the main species in two communities and T. picturata in the third one. Peridomestic infestation and colonization indexes were remarkably high ranging from 26.1% to 50% and from 58.3% to 85.7%, respectively. Moreover, domestic (indoor) infestation was observed in only one of the communities infested by T. longipennis. The preliminary study of temporal variation indicates increasing trend of the triatomine population and infestation rates during the dry season. Triatomine infection rates ranged from 41.2% to 60.2% and all the flagellate isolates were assigned to T. cruzi I. The majority of the dwellings were built with modern building materials and the sanitary conditions were generally good. High peridomestic infestations must be considered as a risk factor of Chagas disease transmission and further studies are needed to better understand the peridomestic conditions favoring the establishment of the triatomines. The contribution of such study to enlarger knowledge of epidemiological features of Chagas disease in Mexico is considered. © 2006 Elsevier B.V. All rights reserved. Keywords: Triatomine; Triatoma longipennis; Triatoma picturata; Chagas disease; Epidemiology

1. Introduction Chagas disease, one of the most important vectors borne disease in Latin America, is known to be endemic in various Mexican states (Z´arate and Z´arate, 1985;

∗

Corresponding author. Tel.: +33 4 67 41 63 72; fax: +33 4 67 41 63 31. E-mail address: [email protected] (S.F. Breni`ere). 0001-706X/$ – see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.actatropica.2006.01.006

Velasco-Castrej´on et al., 1992). Seropositivity of human blood transfusion has been estimated to 1.5% (Trujillo Contreras et al., 1993; Guzman Bracho et al., 1998a; Rangel et al., 1998) and seroprevalence rates up to 20% have been reported in various endemic regions (Tay et al., 1992; Dumonteil, 1999; Mazariego-Arana et al., 2001; Rangel-Flores et al., 2001). Moreover, various clinical cases of Chagas disease have been diagnosed (Gloss et al., 1990; Tay et al., 1992; Guzman-Bracho et al., 1998b; Dumonteil, 1999; Gonzalez-Zambrano et al.,

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1999; Moreno Lopez et al., 2001; Monteon-Padilla et al., 2002). In Mexico, 31 species of triatomine vectors are known to occur, 18 of them being naturally infected with Trypanosoma cruzi, the agent of Chagas disease (Lent and Wygodzinsky, 1979; Carcavallo et al., 1997). The majority of the species found in human dwellings and peridomestic areas are primarily sylvatic (Z´arate and Z´arate, 1985; Velasco-Castrej´on and Guzm´an-Bracho, 1986). As the vectors of Chagas disease concerned are not strictly domiciliated but can reinfest dwellings from sylvatic ecotopes, it will be necessary to develop control strategies appropriate to the local entomological conditions. The Phyllosoma complex, exclusively found in the xeric coastal and high plains areas of the Pacific coast of Mexico, includes multiple species, several ones being of epidemiological relevance: Triatoma longipennis (Usinger, 1939), Triatoma pallidipennis (Stal, 1872) and Triatoma picturata (Usinger, 1939). All of these species invade dwellings and they were recorded in Colima, Jalisco, Morelos and Nayarit states (Martinez-Ibarra et al., 2001; Rangel-Flores et al., 2001; Espinoza-Gomez et al., 2002; Breni`ere et al., 2004; Enger et al., 2004). Actually little information regarding basic entomological patterns in infested villages, ecological conditions of the different species, relationship between vectors infestation and habitat, and the relationships between domestic and sylvatic transmission cycles are available. The study of such factors in different villages will contribute to better define the models of transmission of Chagas disease in Mexico in order to adapt control achievement. The current work supplies a primary entomological and parasitological evaluation of three distant commu-

nities in the occidental part of Mexico, which have never been submitted to vectors control. Entomological indexes for indoors and outdoors infestation as well as parasitological rates and data of the human habitats are recorded. The results clearly showed different epidemiological contexts contributing to improve the knowledge of the transmission systems involved in this part of Mexico.

2. Materials and methods 2.1. Study area Between April 1998 and November 1999, the Mexican communities of Felipe Carrillo Puerto (Nayarit state, 21◦ 07 N; 104◦ 51 W), Cuxpala (Zacatecas state, 21◦ 17 N; 103◦ 13 W) and Tepehuaje de Morelos (Jalisco state 20◦ 25 N; 103◦ 54 W) were surveyed for the presence of triatomine bugs (Fig. 1). These communities are located in semi arid regions and present similar atmospheric conditions. The annual rainfall average ranges between 700 and 1500 mm, with a dry season between October and June and a rain season between June and October; the annual mean temperature ranges between 14 and 26 ◦ C (Statistic, Geographic and Informatic National Institut, INEGI, data). The vegetation is deciduous seasonal forest and the main agricultural crop is corn (Zea mays). The communities are composed of around 327 (Felipe Carrillo Puerto), 202 (Cuxpala) and 641 (Tepehuaje de Morelos) households and each one are surrounded by a small-enclosed field where several domestic animals are bred (peridomestic area). These communities have never been submitted to vector control program.

Fig. 1. The smaller map identifies the States where are located the studied communities in the occidental part of Mexico. The main map showed the Nayarit, Jalisco and Zacatecas States and the banners indicate the location of the three studied communities.

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2.2. Triatomine collection and species identification According to the map of each community, 6–12% of the household selected at random in each village were visited. Bugs were collected manually during the day with the aid of flashlights in peridomestic habitats (outdoor), such as piles of tiles and bricks, firewood, inside chicken-houses, near cattle and in domestic habitats (indoor) such as mattresses, frames, posters and wall splits. The search lasts around 1 man/h in each household. The collected insects were placed in plastic flasks containing filter paper and transported to the laboratory for morphological identification according to Lent and Wygodzinsky (1979). The species of adult specimens were clearly identified while morphological similarities did not allow distinguishing species among nymphs belonging to Phyllosoma complex. 2.3. Infection rate and parasite identification Faeces from each bug were mixed with phosphatebuffered saline and checked for the presence of flagellates by direct microscopically observation at 400× magnification. Moreover, salivary glands and a drop of femur hemolymph of some adults and instars were observed for the presence of Trypanosoma rangeli. T. rangeli is a non pathogenic parasite infecting human and mammals in Central and Northern South America, which migrates to salivary glands after developing in triatomine gut, while T. cruzi does not. Nineteen parasite isolates from faeces (4 in Felipe Carrillo Puerto, 4 in Cuxpala and 11 in Tepehuaje de Morelos) were amplified at 28 ◦ C in LIT medium (Liver Infusion Tryptose; Camargo, 1964). Each parasite isolate was typified by isoenzyme analysis at 16 loci on cellulose acetate plates according to

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Ben Abderrazak et al. (1993) and compared with seven reference stocks of T. cruzi. The UPGMA (unweighted pair-group method with arithmetic average; Sneath and Sokal, 1973) was used to cluster the current zymodemes and those of reference stocks according to Jaccard’s distance matrix as previously described (Acosta et al., 2001). 2.4. Entomological indexes and statistical tests The following indexes were calculated (WHO, 1991): infestation, colonization, crowding index (see Table 1, footnotes) and infection rate (no. of triatomine with flagellate/no. of triatomine examined). The nymphal index was: no. of nymphs/no. of collected triatomine. Statistics were computed by the Statix package. χ2 test was used to compare distributions between several categories. The nonparametric test of Kruskal–Wallis was applied to compare average values obtained for two categories. 3. Results 3.1. Characteristics of human dwellings and capture sites In the three communities, the large majority of the households were built with modern building materials and the sanitary conditions presented good general state of repair and cleanliness (Fig. 2). Of the 65 dwellings examined (data were missing for other dwellings), 94% of the floors were of mosaic or cement, the walls were of bricks (86%) or stuccowork adobes (14%) and 70% of the roofs were of cement or bricks while the others were of tiles and sheet–metal (Table 1). Statistical differences were observed for floor and wall materials between

Table 1 Comparison of the house materials in three occidental Mexican communities Felipe carillo puerto, N = 22 Roof Cement Brick Tile Sheet–metal Floor Mosaic Cement Earth Walls Stuccowork brick Crude brick Stuccowork adobe

Cuxpala, N = 18

Tepehuaje de morelos, N = 25

Total, N = 65

%

χ2 value

Degree of freedom

p

7 7 5 3

9 7 1 1

14 1 4 6

30 15 10 10

46.2 23.1 15.4 15.4

4.6

2

0.10

5 14 3

13 4 1

22 3 0

40 21 4

61.5 32.3 6.2

19.4

2

10−4

13 2 7

14 2 2

23 2 0

50 6 9

76.9 9.2 13.8

10.1

2

<10−2

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Fig. 2. Typical house found in the occidental part of Mexico built with modern materials: the walls are of bricks and the flat roof is of cement.

the three communities. In Felipe Carrillo Puerto cement floors and stuccowork adobe walls were more frequently recorded than in the two other communities but the infestation was limited to outdoors while indoor infestation was only observed in Cuxpala. The indoor triatomines were mainly captured in bedrooms (96%), while the other rooms (kitchen and living room) were also examined. In peridomestic area the capture sites were very diverse. Among them, relinquished building materials appeared as a good ecotope for triatomine (32% of the sites) but triatomines were scarcely found in this ecotope in Cuxpala. The presence of domestic animals, chickens, sheeps, cows, dogs were noted in 40% of the overall habitats but were more frequent in Tepehuaje de Morelos than in the two other communities. It is worth noting that in Cuxpala bugs were collected in various places as outside walls of the houses, exterior floor, on electricity pylon, and in vegetation. 3.2. Triatomine collection, morphological identification and entomological indexes

species were sympatrically collected from pile of bricks (outdoors) in two different collection sites. Table 2 summarized the infestation, colonization, crowding and nymphal indexes showing different epidemiological trends. In Felipe Carrillo Puerto and Tepehuaje de Morelos the infestation by triatomine species of Phyllosoma complex was limited to peridomestic structures (outdoors) with important colonization indexes (85.7% and 73.7%, respectively). Remarkably, in Cuxpala, T. longipennis specimens were equally collected in domestic (indoor) and peridomestic areas (similar indexes). Any statistical difference was observed between the three communities for peridomestic infestation (χ2 = 2.8, d.f. = 2, p > 0.05), colonization (χ2 = 1.0, d.f. = 2, p > 0.05) and crowding indexes estimated by the Kruskal–Wallis no parametric test (K–W statistic = 2.6, d.f. = 2, p = 0.26). Significant difference was observed for nymphal index only (Felipe Carrillo Puerto and Tepehuaje de Morelos > Cuxpala, χ2 = 27.7 and χ2 = 33.5, respectively, d.f. = 1, p < 0.001). 3.3. Temporal variations of entomological index

A total of 514 specimens of T. longipennis, T. picturata and Triatoma barberi were collected in the three studied communities. T. barberi were scarcely collected in Tepehuaje de Morelos only (6.6% of adult specimens). The other two species were unequally distributed in the villages. T. longipennis was found in the three communities while T. picturata was the most abundant species in Felipe Carrillo Puerto (25/31, 80.6%) and absent in the others. Moreover, in Felipe Carrillo Puerto, these two

In Cuxpala and Tepehuaje de Morelos communities the triatomines were collected during two different seasons. Table 3 summarizes the entomological indexes and infection rates obtained in April (dry season) and at the beginning and end of the rainfall season in Cuxpala (June) and Tepehuaje de Morelos (November) respectively. In the two communities, the infestation rates are higher during the dry season in peridomestic

226/296 (76.3) 0/5 (0) S.D. = standard deviation. a (No. of habitat infested by Triatoma sp. adults or nymphs/no. of habitat examined) × 100. b (No. of habitat with by Triatoma sp. nymphs/no. of habitat with Triatoma sp.) × 100. c (No. of Triatoma sp. captured/no. of habitat with Triatoma sp.) × 100. d (No. of Triatoma sp. nymph captured/no. of total Triatoma sp.captured) × 100. e No calculated, sample smaller than 5. f Calculated from the total population of collected triatomines (T. longipennis + T. picturata).

18/50 (36.0)

0e 0e

15/41 (36.6) 4.2 ± 3.4

15.6 ± 19.9 1.3 ± 0.5

2.9 ± 2.6 7 (58.3) 25

38

Cuxpala

Tepehuaje de Morelos

19 (50.0) 4 (10.5)

0e 0e

14 (73.7) 0e

14 (56.0) 12 (48.0)

0 (0) 0 (0)

T. longipennis

T. longipennis T. barberi

23 Felipe Carrillo Puerto

6 (42.8)

environment but in Cuxpala only significant difference was observed (χ2 = 4.19, p < 0.05). In Tepehuaje de Morelos the nymphal index presented significant differences (χ2 = 16.0, p < 10−3 ) between April (91.2%) and November (69.7%). All the other indexes were not significantly different between the two collection times.

0e

93/119 (78.1)f 0/3e,f 14.9 ± 23.5f 6 (85.7)f 0e,f 2 (8.7) 6 (26.1) 1 (4.3) 1 (4.3) T. longipennis T. picturata

0e,f

Outdoor Indoor Outdoor Indoor Outdoor Indoor Outdoor Indoor

No. of habitats examined

Triatomine species

335

3.4. Infection rate and parasite identification

Community

Table 2 Entomological indexes in three occidental Mexican communities

Infestation indexa no. infested (%)

Colonization indexb no. with nymph (%)

Crowding indexc ± S.D.

Nymphal indexd no. nymph/no. triatomine (% nymph)

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Faecal triatomine samples from Felipe Carrillo Puerto (115), Cuxpala (80) and Tepehuaje de Morelos (290) were examined microscopically for the presence of flagellates (Table 4). Total infection rates ranged from 41% to 60% and a significant difference was observed between Felipe Carrillo Puerto and Cuxpala in peridomicile (χ2 = 5.11, p = 0.024). In Cuxpala, similar infection rates were obtained in domestic (43.3%) and peridomestic (41.2%) triatomine populations. In Felipe Carrillo Puerto and Tepehuaje de Morelos comparable infection rates were observed for adults and nymphs while significant difference was noted in Cuxpala (57.1% and 21.8%, respectively; χ2 = 6.53, p = 0.01). Furthermore no significant differences were observed between sex (p > 0.05). Among 95 salivary glands of adults and nymphs, collected in the three villages, only one sample (Felipe Carrillo Puerto) presented flagellates. The isoenzyme typing showed that all the studied stocks (19 stocks in total) isolated in the three communities were unequivocally assigned to T. cruzi I (Momen, 1999) with the reference stocks belonging to this lineage. 4. Discussion Previous report has showed that species of the Phyllosoma complex were the most abundant ones in Jalisco state; T. barberi, which is currently classified within the Protracta complex (Ryckman, 1962), was present at 5.53% and showed a large distribution over 15 out of 51 visited municipalities (Magall´on-Gast´elum et al., 1998). Moreover, this report indicated 17.5% of T. barberi captures in houses (indoors), all being adults (unpublished data). This result showed the absence of colonization in this area contrary to Oaxaca State where colonization index reached 10% (unpublished data; Ramsey et al., 2000). The current data confirms the previous ones, concluding that T. barberi can be considered as a minor vector of Chagas disease in the occidental part of Mexico. Species of the Phyllosoma complex are the most important vectors in Jalisco and Nayarit states (Magall´on-Gast´elum et al., 1998; Martinez-Ibarra et al., 2001), T. longipennis, T. pallidipennis and T. picturata

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Table 3 Temporal variation in entomological indexes Cuxpala

No. of habitats Indexesa Infestation Colonization Crowding ± S.D. Nymphal a b c

Tepehuaje de Morelos

02 July 1998, begining of rainfall

23 April 1999, dry season

28 April 1999, dry season

15 November 1999, end of rainfall

Indoor

Indoor

Outdoor

Outdoor

12

26

75% 66.6% 10.1 ± 12.3 91.2%c

38.5% 80% 20.5 ± 24.4 69.7%c

Outdoor

13 61.5% 37.5% 2.2 ± 2.2 38.9%

Outdoor

11 30.7%b 50.0% 2.50 ± 1.3 20.0%

54.5% 50.0% 3.5 ± 2.3 14.3%

72.7%b 50.0% 2.6 ± 2.6 38.1%

The different indexes are as indicated in Table 2; S.D.: standard deviation. Significant differences evaluated by χ2 test between both values (p < 0.05). Significant differences evaluated by χ2 test between both values (p < 10−3 ).

being the most abundant ones. In the previous reports information does not provide the sympatric distribution of these species. However, the current report evidences a sympatric collection of T. longipennis and T. picturata in Felipe Carrillo Puerto. In this village, the species of the adult specimens were easily determined through the use of morphological key; No hybrid morph has been observed in these sympatric conditions, which provide the potential for natural hybrid individuals. Few analyses of entomological evaluation in Mexican communities with appropriate sampling are available despite the relevance of such data towards a better understanding of the epidemiological features of Chagas disease in Mexico (Enger et al., 2004; Ramsey et al., 2005). The current comparison between the three communities gives rise to the description of different epidemiological trends. Therefore, in Tepehuaje de Morelos T. longipen-

nis, the main species, is well established in peridomestic area forming large colonies, as indicated by the high infestation index and the high proportion of nymphs in the collected sample. In Cuxpala T. longipennis should be the only vector species but entomological indexes are different from those of Tepehuaje de Morelos. The infestation is lower, small colonies are observed and infestation is not limited to peridomestic area (the triatomines similarly invaded indoor and outdoor areas). Moreover, the colonization and the nymphal indexes are the lowest ones compared with the two other communities. These observations could be related to a present process of colonization. The preliminary study of the habitats does not indicate differences in the building materials used in the three communities that could explained the indoor colonization in Cuxpala while differences in colonization indexes can be related to housing improvement (Cerece

Table 4 Microscopically evaluation of Trypanosoma cruzi infection rates in triatomine stages Infection ratea

Total indoor Total outdoor Nymphal instars 1 2 3 4 5 Adults Male Female a b c

Felipe carrillo puerto (T. longipennis + T. picturata)

Cuxpala (T. longipennis)

Tepehuaje de Morelos (T. longipennis)

0/2 68/113 (60.2%)c

13/29 (44.8%) 21/51 (41.2%)c

Absent 152/290 (52.4%)

0/1(-)b 1/1(-)b 10/13 (76.9/) 14/20 (70.0%) 33/55 (60.0%)

Absent 0/3 (-)b 0/2 (-)b 1/6 (16.7%) 5/21 (23.8%)

Absent 7/14 (50.0%) 33/65 (50.8%) 30/62 (48.4%) 42/80 (52.5%)

5/14 (35.7%) 6/10 (60.0%)

11/16 (68.8%) 17/33 (51.5%)

17/37 (45.9%) 23/32 (71.9%)

No. of specimens with T. cruzi/no. examined (%). No calculated. Significant differences of χ2 test between both values (p < 0.05).

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et al., 1998, 2002). Indeed multivariate studies of habitat and geographical data need to be developed to better evaluate risk factors of intradomiciliar colonization. In Felipe Carrillo Puerto, the epidemiological feature is more similar to Tepehuaje de Morelos with lower infestation index, since T. picturata is the principal species. The higher infestation rates observed during the dry season could be related to increase insect activities and better capacity to invade new sites when the temperature is higher (Botto-Mahan et al., 2005). Nevertheless, analysis of larger populations collected at different times during the year is necessary to establish the life cycle and the spreading out capacity of these triatomine species according to the season. The current triatomine infestation and the very high infection rate of the bugs constitute a risk of transmission of Chagas disease, which remains to be evaluated by seroprevalence surveys. Indeed in various cases, the inhabitants reported the occasional penetration of bugs inside the house. These few contacts between man and vectors should be enough to allow the transmission of Chagas disease. A vector classification based on habitat, which has implications for control, included the Phyllosoma complex species in both domestic and wild group that trends toward domesticity (WHO, 2002). This group consists of species that are principal vectors in various endemic countries; one of them is Triatoma dimidiata, a species of wide geographical distribution from northern South America to Mexico, which is genetically related to the species of the Phyllosoma complex (Flores et al., 2001; Marcilla et al., 2002). Analyses of entomological features in scale community are undoubtedly primary for other studies and are important not only for the current species but also for others which have similar ecological patterns. However, further studies are necessary to understand which are the factors allowing the (i) introduction of these species in the dwelling (passive transportation, active invasion by flying adults), (ii) those linked to the development of colonies indoors and outdoors (host accessibility, materials of hiding-places, human habits), (iii) those that retain triatomines in spite of climatic fluctuations that generally diminish the populations. Furthermore, the study of the factors linked to the establishment of the triatomine peridomestic colonies, needs investigations to adapt suitable vector control strategies to the domestic-wild species of vectors. Acknowledgments This investigation received financial support from the UNDP/World Bank/WHO Special Programme for

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Research and Training in Tropical Diseases (TDR) Grant ID 970943, the Institut de Recherche pour le D´eveloppement (IRD), DGAPA IN 224798 Universidad Nacional Aut´onoma de Mexico and Conacyt 27951M. We thank Franc¸oise Mathieu-Daud´e, the editor and reviewers for helpful comments and revision of the manuscript. References Acosta, N., Samudio, M., Lopez, E., Vargas, F., Yaksic, N., Breni`ere, S.F., Rojas de Arias, A., 2001. Isoenzyme profiles of Trypanosoma cruzi stocks from different areas of Paraguay. Mem. Inst. Oswaldo Cruz. 96, 527–533. Ben Abderrazak, S., Guerrini, F., Mathieu-Daud´e, F., Truc, P., Neubauer, K., Lewicka, K., Barnab´e, C., Tibayrenc, M., 1993. Isoenzyme electrophoresis for parasite characterization. Meth. Mol. Biol. 21, 361–382. Botto-Mahan, C., Cattan, P.E., Canals, M., Acu˜na, M., 2005. Seasonal variation in the home range and host availability of the bloodsucking insect Mepraia Spinolai in wild environment. Acta Trop. 95, 160–163. Breni`ere, S.F., Pietrokovsky, S., Magall´on Gast´elum, E., Bosseno, M.F., Soto, M.M., Ouaissi, A., Lozano Kasten, F., WisniveskyColli, C., 2004. Feeding patterns of Triatoma longipennis Usinger Hemiptera Reduviidae in peridomestic habitats of a rural community in Jalisco State Mexico. J. Med. Entomol. 41, 1015–1020. Camargo, E., 1964. Growth and differenciation in Trypanosoma cruzi I. Origin of metacyclic trypanosomes in liquid media. Rev. Inst. Med. Trop Sao Paulo 6, 93–100. Carcavallo, R.U., Gal´ındez Gir´on, I., Jurberg, J., Lent, H., 1997. VI. Bibliographic checklist of the American Triatominae (Hemiptera:Reduviidae). In: Carcavallo, RU., Gal´ındez Gir´on, I., Jurberg, J., Lent, H. (Eds.), Altlas of Chagas disease Vectors in the America. Editora Fiocruz Rio de Janeiro, pp. 15–52. Cerece, M.C., Gurtler, R.E., Chuit, R., Cohen, J.E., 1998. Factors limiting the domestic density of Triatoma infestans in north-west Argentina: a longitudinal study. Bull. World Health Organ. 76, 373–384. Cerece, M.C., Gurtler, R.E., Canale, D.M., Chuit, R., Cohen, J.E., 2002. Effects of partial housing improvement and insecticide spraying on the reinfestation dynamics of Triatoma infestans in rural northwestern Argentine. Acta Trop. 84, 101–116. Dumonteil, E., 1999. Update on Chagas’ disease in Mexico. Salud Publica Mex. 41, 322–327. Enger, K.S., Ordonez, R., Wilson, M.L., Ramsey, J.M., 2004. Evaluation of risk factors for rural infestation by Triatoma pallidipennis Hemiptera: Triatominae a Mexican vector of Chagas disease. J. Med. Entomol. 41, 760–767. Espinoza-Gomez, F., Maldonado-Rodriguez, A., Coll-Cardenas, R., Hernandez-Suarez, C.M., Fernandez-Salas, I., 2002. Presence of triatominae (Hemiptera, Reduviidae) and risk of transmission of Chagas disease in Colima, Mexico. Mem. Inst. Oswaldo Cruz. 97, 25–30. Flores, A., Magall´on Gast´elum, E., Bosseno, M.F., Ordonez, R., Lozano Kasten, F., Espinoza, B., Ramsey, J., Breni`ere, S.F., 2001. Isoenzyme variability of five principal triatomine vector species of Chagas disease in Mexico. Infect. Genet. Evol. 1, 21–28. Gloss, G., Barrera, M.R., Monteon, V.M., Reyes, P.A., 1990. American trypanosomiasis and chronic Chagas cardiopathy at the “Ignacio

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