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versão On-line ISSN 0717-7712
Parasitol. latinoam. v.62 n.3-4 Santiago dez. 2007
Parasitol Latinoam 62: 154 -164, 2007 FLAP
Triatomines (Hemiptera, Reduviidae) prevalent in the northwest of Peru: species with epidemiological vectorial capacity
CESAR AUGUSTO CUBA CUBA*, GUSTAVO ADOLFO VALLEJO** and RODRIGO GURGEL-GONCALVES*;***
* Universidade de Brasilia, Faculdade de Medicina, Área de Pato logia, Laboratorio de Parasitología Médica e Biologia de Vetares, Brasilia, DF, Brasil.
The development of strategies for the adequate control of the vector transmission of Chagas disease depends on the availability of updated data on the triatomine species present in each region, their geographical distribution, natural infections by Trypanosoma cruzi and/or T. rangeli, eco-biological characteristics and synanthropic behavioral tendencies. This paper summarizes and updates current information, available in previously published reports and obtained by the authors our own field and laboratory studies, mainly in northwest of Peru. Three triatomine species exhibit a strong synanthropic behavior and vector capacity, being present in domestic and peridomestic environments, sometimes showing high infestation rates: Rhodnius ecuadoriensis, Panstrongylus herreri and Triatoma carrioni The three species should be given continuous attention by Peruvian public health authorities. P. chinai and P. rufotuberculatus are bugs with increasing potential in their role as vectors according to their demonstrated synanthropic tendency, wide distribution and trophic eclecticism. Thus far we do not have a scientific explanation for the apparent absence ofT. dimidiata from previously reported geographic distributions in Peru. It is recommended, in the Peruvian northeastern Amazon region, the development of field studies on species of the genus Rhodnius, as well as of other triatominae, to evaluate their present Trypanosomatidae vector capacity.
Key words: Rhodnius ecuadoriensis, Panstrongylus herreri, Triatoma carrioni, Geographic distribution, vector capacity, North wester Perú.
El desarrollo de estrategias adecuadas para el control de la transmisión vectorial de la Enfermedad de Chagas depende: de la disponibilidad de datos actualizados de las especies de triatominos presentes en cada región, de su distribución geográfica, infección natural por Trypanosoma cruzi ylo T. rangeli, características eco-biológicas y tendencias de comportamiento sinantrópico. Este trabajo resume y actualiza la información disponible en la literatura y aquella obtenida en nuestros estudios de campo y de laboratorio desarrollados en los últimos años por los autores, predominantemente, en la región Nor-Occidental del Perú. El resultado de esas observaciones es la detección de que, tres especies de triatominos presentan un importante comportamiento sinantrópico y capacidad vectorial, ocupando ambientes intradomiciliares y peridomiciliares: Rhodnius ecuadoriensis, Panstrongylus herreri y Triatoma carrioni. Las tres especies deben recibir constante atención por parte de las autoridades de Salud Pública Peruana. P. chinai y P rufotuberculatus tienen potencial creciente en su papel de vectores, por la comprobada tendencia sinantrópica, distribución geográfica y eclecticismo trófico. Se desconocen las causas de la aparente ausencia actual de Triatoma dimidiata, dada su presencia constatada anteriormente en el Perú. Se recomienda que en la región Nor-Oriental Amazónica Peruana se realicen en forma urgente estudios sobre las especies del genero Rhodnius y de otros triatominos que permitan evaluar la real capacidad vectorial de los Trypano-somatideos.
Roughly 6.7 million inhabitants of Peru are estimated to live in Chagas Disease risk areas and approximately 680,000 individuals are infected by the Trypanosoma cruzi1. Information on the prevalence of human infection by Trypanosoma rangeli is practically nonexistent. Even so, the pressing need to implement an American trypanosomiasis control program in Northern Peru continues to be neglected by national public health services. Basic activities on Chagas disease epidemiology, such as large-scale serological and entomological field surveys and the control of donors to regional blood banks are poorly implemented.
Four Tribes, seven Genera and fifteen species of Triatomines have been reported in the North of Peru. This value corresponds to, approximately, 11% (15/137) of the valid species of the Triatominae Sub-Family described in the World2. According to the Triatomine list illustrated in Table 1, it is possible to observe a high species diversity in that region. The referred species are distributed in the Departments and Provinces of the Country, associated to a significant ecological diversity, comprising 15 life zones in the studied areas. Biogeographically, these zones include coastal deserts, a complex pattern of Inter- and Trans-Andean warm valleys and wet tropical forests3 (Figure 1).
I is also it is known that the basic requirements for the survival of a triatomine are the availability of food sources, shelter, and biological adaptation to the macro and micro-environmental variations where they live and prevail. Table 2 shows a group of insects, according to accepted biogeographical and behavioral aspects.
Considering those species with the greatest vector potential, our experience shows that three of them are the ones species exhibiting a strong synanthropic behavior living in human habitats. Therefore the, can be regarded as possible targets of control initiatives undertaken against domestic and peridomestic populations of vector triatomines. Following, detailed information on the geographic distribution, synanthropic behavior, natural infection, biogeography, and, eco-biological characteristics of those species are given.
Vector of the T. rangeli and/or of the T. cruzi in Peru. Our field studies show that in Andean locations, in the Departments of La Libertad and Cajamarca, domicile infestation rates exceed 35% (detected with Gomez-Nuñes sensors and by a 6-month follow-up)4. This species frequently lives in intradomiciliary settings, constituting stable and teeming colonies in human dwellings as well as in intradomiciliary breeding corrals of Cavia porcellus (mainly in the kitchens). In the peridomicile, they colonize adjacent corrals of domestic animals. The ecosystems filled between the inter and trans-Andean valleys are xerophytic and dry most of the year (6° 50' S, 78° 25' W)3,4. Recently, Patterson et al5, used morphometry techniques and multivariable statistical analysis of seven measures of head to discriminate triatomine populations collected in Ecuador and Peru. These authors categorized phenotypically sylvatic populations existing in the Manabi Province, Ecuador (1° 6' S, 80° 24 W, 130, m.a.s.1.), the domestic populations prevalent in the Southern Ecuadorian Provinces of Loja and El Oro (4° 15' S, 79°30' W, 1,500 m.a.s.1.)6,7, in the North of Peru, Suyo ( 4° 30' S, 511 m.a.s.1.) and in the Alto Chicama Valley (7° 28' S, 78° 49' W, 1,626 m.a.s.1.) (Figure 2). The authors5 put forward that possibly these insects spread toward Southern Peru carried passively by human beings. Subsequently, Abad-Franch et al8 analyzed these populations of R. ecuadoriensis of different geographical origin and ecotopes (Peru and Ecuador) using molecular markers and confirmed significant differences in the mitochondrial DNA of cytochrome b gene sequences of the Peruvian population (Chicama Valley) when compared to those from Ecuador. This would mean the existence of two diverging populational clades, perhaps associated to ecological micro-habitat adaptations. The Peruvian population would probably be undergoing speciation. Perhaps populations in the Alto Chicama Valley, Cascas. La Libertad (7°22'48" S, 78° 27' 15" W) and Cajamarca (7° 40'S, 78° 27' W) are R. ecuadoriensis populations isolated biogeogra-phically8.
It should be remembered that sylvatic ecotopes of R. ecuadoriensis in Phytelephas palm trees in the Manabi province of Ecuador and in southern border locations have been reported in previous literature9. There is no evidence to date that this species may have sylvatic ecotopes in Peru, which is of particular importance for the vector control strategy, given the possibility of domiciliary re-infestation, after insecticidal spraying, by this sylvatic populations and their later interference in the entomological evaluation.
Taken into consideration the Trypanosome vector role performed by R. ecuadoriensis in the region under study, we know today that it is predominant in T. rangeli transmission. So far T. cruzi mixed infections have not been described as far and, despite the confirmed infection of salivary glands (8.3% of natural infection in domestic triatomines - Cuba Cuba et al, unpublished data and Table 3), there is no scientific corroboration of its transmission and parasitism in humans. The species is the only one in which the complex biological cycle of T. rangeli is naturally completed and transmission occurs by biting and injecting metacyclical trypomastigotes of T. rangeli.
Soon after Herrer et al.10 reported the finding, for the first time, of T. rangeli in R. ecuadoriensis, in the Huancabamba valley in Piura, Peru, other research was carried out11 in Cajamarca. Further experimental studies with the model: vector insect - R. ecuadoriensis and guinea pigs (Cavia porcellus), using T. rangeli Peruvian strains12-15 contributed to the knowledge of the parasitism biology and of electro microscopy/morphology aspects of the parasite invading the salivary glands of the vector16.
Recent research using T. rangeli strains isolated from the species, captured in the Alto Chicama valley, La Libertad, has shown the Peruvian strains to possess two mini-circles of k-DNA (KP2 and KP3). Such molecular profile was verified by means of PCR duplex molecular analysis (k-DNA markers) and analysis of a product of the intergenic region of the 380-bp miniexon gene and, therefore, classified as KP1 (-) as established17,18.
Later, Urrea et al19 demonstrate that Peruvian strains of T. rangeli are genetically similar to those transmitted by Rhodnius pallescens in Panama and R. colombiensis in Colombia, when compared to each other. Finally, a very recent study analyzing 66 T. rangeli20 strains shows evidence of a consistent association of T.rangeli KP1 (-) with species of the Rhodnius Genus belonging to the so-called pallescens group (R. pallescens, R. colombiensis, R. ecuadoriensis) which are geographically distributed on the Pacific Ocean side. The authors conclude that the vector and flagellate populations demonstrate a certain degree of co-evolution.
Although being quoted by some authors as an important vector of Chagas Disease8,9, we can not currently evaluate the vectorial impact of R. ecuadoriensis, for T. cruzi, despite the fact that it has been identified sometimes as naturally infected by the Trypanosome21,22,2. Upon examination of the problem we arrived at the conclusion that there is a lack of studies about the geographical distribution of the triatomine as well as about the evaluation of its real role in the transmission of the Chagas disease agent. This is a relevant fact given that in the neighboring country of Ecuador and in locations near the Peruvian territory, have recently reported 4% of T. cruzi infection in domestic populations of R. ecuadoriensis7.
This species has been demonstrated to be cytogenetically identical to Panstrongylus lignarius24 and is even considered as a synonym2 of the latter, based on comparative studies using rDNA molecular markers25. Nevertheless, P. lignarius has never been found in areas of P. herreri geographical dispersion which in Peru lives in intradomiciliary ecotopes very characteristic of the Departments of San Martin26,27, Amazonas, Cajamarca and Piura6,7. As far as we know, there have not been reports of P. lignarius in the Peruvian territory. Ecologically, P. herreri is different, on its synanthropic behavior, as it has shown to have high adaptability to the human environment. This is in stark contrast to observations on P. lignarius populations in Brazil, where they behave as sylvatic species, common in Attalea32-36, Scheelea and Maximiliana palm trees from which, they can get to human dwellings lured by artificial light8. P. herreri is, thus far, the main vector of the T. cruzi in the Inter- and Trans-Andean valleys and in the "Selva Alta" (high Amazon rainforest of Peru). Its vector role has been known since the pioneer epidemiological work32,23. Recent studies have shown it to transmit the parasite of Chagas Disease in the province of Cutervo, Department of Cajamarca, with acute reported41. Recently, Vega et al42, reported average serum prevalence of anti-Z cruzi antibodies among children younger than 15 years old, in the provinces of Uctubamba (Amazonas) and Cutervo (Cajamarca) with values of 5.7% and 3.8%, respectively, with intradomiciliary presence of P. herreri. Thus, P. herreri has an active dispersion in the Departments of San Martin (approx. 5° 38' S; 76° 55' W, our observations27), Amazonas and Cajamarca35. However, currently we do not have field information which could allow us to determine the precise scale of the species' natural infection rate by T. cruzi in this vast geographical region of Peru. Reports on these subjects would be of great value for a Chagas Disease Control Program in Northern Peru.
Triatoma carrioni (Figure 3)
Species with wide altitudinal range (500-2,292 m.a.s.1.). Reports on the finding of natural infection by T. cruzi of this species in the Cutervo Province, Cajamarca, have been published23,36. In our fieldwork we have confirmed that it behaves as a species well suited to the human domicile. The verification in several locations of the Piura Department and, especially, in the Ayabaca Province, (4°46' S; 79°98' W; monthly average temperature between 19° C; relative humidity 52-31%) shows high intradomiciliary infestation rates. The following entomological parameters have been verified: domiciliary infestation rates (infested/sampled dwellings): 48.3%; density rate (bugs/dwellings sampled): 3.9; crowding rate (bugs/infested dwellings): 8.1; colonization rate (dwellings infested with nymphs/dwellings sampled): 86.6%. Still, T. carrioni was not detected in sylvatic environments until now (Cuba Cuba et al, unpublished results). The domiciliary infestation rate was higher in altitudes above 2,100 m.a.s.1., where the high percentage of T. carrioni nymphs was a remarkable sign of the existence of stable colonies. However the presence of this species in dwellings located at 530 m.a.s.1. leads us to consider the possibility of its adaptation to other ecosystems of the Peruvian coast. We believe that a greater capturing effort would be necessary in the northern region of Peru in order to confirm and quantify its presence in peridomicile and sylvatic environments and to establish its actual dispersion southward of the country. The existence of sylvatic populations would restrict a program to control the species due to the probability of re-infestation of human domiciles and domestic animal shelters.
In the meantime, emphasis and entomological surveillance should be laid on other triatomine species whose biology, geographical dispersion, habits and synanthropic tendencies characterize them as enzootic vectors of T. cruzi. For the studied area, they are the following:
Panstrongylus chinai (Figure 3)
Widely-distributed species in the Departments of Tumbes, Piura, Cajamarca, Amazonas, Lambayeque, La Libertad, and Ancash. Though described as sylvatic vector, it was found living in peridomiciliary/extradomiciliary ecotopes nearby human domiciles. In localalities of Ecuador in the vicinity of the Peruvian Departments of Tumbes and Piura, a 35% rate of domiciliary infestation has been reported7. In xerophytic ecosystems of inter and trans-Andean valleys of northwestern Peru, it is common in ecotopes such as hollow trees of Schinus molle and specially in stone walls ("pircas") built to provide shelter to animals (Figure 3). In these habitats, we could measure temperatures ranging up to 41°C, where teeming colonies of the triatomine are easily found. These ecotopes also harbored marsupials, rodents and reptiles which are an alternative triatomine's food source, also known as T. cruzi reservoirs. This fact could explain, the high rate of natural infection by T. cruzi., which is reported in the Peruvian scientific literature37,38,23.
Pollack et al39, reported an entomological census in Paredones, San Pablo Province. Cajamarca, Peru (6° 50' S, 78° 25' W, 1,350 m.a.s.1.; 14° C average temperature and relative humidity of 70%). A total of 272 specimens of P. chinai captured in 25 peridomiciliary ecotopes located in the stone walls (about 50 meters from domiciles, (Figure 3) were randomly selected and examined in each sampling location. The age structure found was as follows: 80 nymphs I; 55 nymphs II; 70 nymphs III, 45 nymphs IV. and 22 nymphs V. There was as significant predominance of I and III nymphs. No male or female adults were found. At the same time, adults captured by the above mentioned authors using artificial light traps, in two extradomiciliary ecotopes in the same location were studied morphometrically, using 8 measurement head points. Variables were analyzed by means of descriptive statistics, variation coefficient, correlation matrix, and multivariate discriminant analysis. Finally, a dendrogram of taxonomic relatedness was constructed using the unweighted-pair-group-method (UPGM) analysis to demonstrate the relationship between both populations collected. The analysis of head morphometric variables suggests that populations attracted by artificial light show some degree of phenotypic variation, describing 2 morphometric variants of adult P. chinai populations. A significant variation coefficient (CV=13.6%) was found in the post-ocular distance variable (not including neck) in male and female samples. The external distance between eyes also showed differences among female specimens studied (CV= 11.9%). The distance dendrogram (Mahalanobis distances) showed unequivocal separation in two branches (taxonomic distance = 0.054), suggesting two P. chinai population groups in the region. Could these be valuable morphometric phenotypic markers to identify sylvatic populations of P. chinai in transition or moving to a peri/domiciliary ecotope? It is a fact that adult specimens are frequently found inside dwellings despite not having colonized them. Many specimens arrive to the squares of small villages flying at night. On the other hand, the absence, in our studies, of adult specimens in peridomicile "pircas" is striking.
Panstrongylus rufotuberculatus (Figura 4).
This species has a wide biogeographical distribution in Central and South America, with sylvatic habits, though exhibiting synanthropic tendency and possibly being a T. cruzi potential vector40,41. It is present in several ecosystems of the Peruvian territory, having been reported in the Departments of Tumbes, Piura and, with domicile infestation, in Cuzco28. Our studies provide strong evidence of domiciliation of this species in the location of La Pareja-Chirinos, Suyo District, Ayabaca Province, Piura (4° 46: S, 79° 93' W, 530 m.a.s.1., 26° C average temperature and 52% relative humidity). By hand collecting procedure (men/hour per house), with previous spraying of a chemical irritant (flushing-out aquose cypermetrine 0.1%), 37 specimens were collected in 2/15 houses examined (infestation rate = 13.5%, density = 2.4). The greatest concentration of nymphs of several stages, and adults, occurred in the "cuyero", or guinea pig (Cavia porcellus) corral, located in the kitchen of an infested house. This study confirmed the existence of stable intradomiciliary colonies of P. rufotuberculatus. None insect was infected with T. cruzi (Cuba Cuba et al, unpublished).
Peruvian scientific literature described its domiciliary presence at the banks of rivers Zarumilla and Tumbes, in the Tumbes Department, nearly 50 years ago42,43. Since then, this species has not been reported in domiciles of the northwestern region of Peru. An exhaustive investigation carried out by our workgroup within dwellings in the locations of the rivers Tumbes and Zarumilla previously reported as infested, was negative to the finding of T. dimidiata. We hypothesize that climatic changes brought about by the El Niño and La Niña phenomena, which have a severe impact on the region, and the constant use of insecticides in anti-Malaria campaigns of the Ministry of Health of Peru, have modified the environment for this species. We therefore conclude this species has been eradicated from Peru at the domestic environment. The investigation should be repeated in order to confirm this assertation.
The theme of Trypanosome vector triatomines in northern Peru has been a subject of concern to the first author of this review for many years. In Peru, a well thought-out program to confront the challenge of Chagas Disease and "rangeliosis", along with aspects of their study and control, is necessary.
This is notorious in northern Peru as a whole, and particularly in the northwestern region. Yet, in order to insist on the obvious need to spread the word and urge the development of new studies on the subject, we put together the following comments which arise from findings throughout our period of observation:
The task of keeping an updated database on the biogeographical distribution of the Triatominae species in Peru is of paramount importance.
There should be support for field studies that focus on registering the behavior of species regarded as having synanthropic potential and tendencies, trophic eclecticism, and wide geographical dispersion, as is the case of Panstrongylus rufotuberculatus, Panstrongylus chinai and Panstrongylus geniculatus.
Studies on altitudinal range and remote sensing recording with satellite image geopositioning, will allow for a more precise documentation of species considered as domiciliary and/or peridomiciliary. We lay emphasis on: Rhodnius ecuadoriensis, Panstrongylus herreri and Triatoma carrioni, which should be under permanent surveillance from the entomological services of the Ministry of Heath.
Likewise, serological surveys of representative populations (school children under 15) in several regions of northern Peru are a priority, in order to establish the real impact of Trypanosomiasis on the public health of the region.
Very little is known about species of Rhodnius in order to determine their prevalence in Departments of the Peruvian Amazon region. We do not know the role they play in the enzootic and zoonotic transmission of Trypanosoma cruzi and/or T. rangeli, as it has been registered in neighboring countries. What actually happens in localities in the "Selva Alta" and in the Departments of Loreto and Madre de Dios of Peru?
Finally, we should support fundamental research in the morphometry and genetic of triatomine populations and their respective Trypanosomes, as this is the only way to plan a rational and effective combat in the entomological control and vectorial transmission control initiatives.
1.- GUHL F. Chagas disease current epidemiological trends in the Andean Region. IX European Multicolloquium of Parasitology. Symposium Trypanosomes, triatomine and Chagas disease: basic knowledge an applied research. Valencia. 2004. [ Links ]
2.- GALVAO C, CARCAVALLO R, ROCHA D S, JURBERG J. A checklist of the current valid species of the subfamily Triatominae, Jeannel, 1919 (Hemiptera, Reduviidae) and their geographic distribution. Zootaxa 2003; 202: 1-36. [ Links ]
3.- CUBA CUBA C A, ABAD-FRANCH F, ROLDAN J R et al. The triatomines of Northern Peru with emphasis on the ecology and infection by Trypanosomes of Rhodnius ecuadoriensis (Triatominae). Mem Inst Oswaldo Cruz 2002; 97: 175-83. [ Links ]
4. - CUBA CUBA C A, VARGAS F, ROLDAN J, AMPUERO C. Domestic Rhodnius ecuadoriensis (Hemiptera. Reduviidae) infestation in Northern Perú: A comparative trial of detection methods during a six-month follow-up. Rev Inst Med Trop S Paulo 2003; 45: 85-90. [ Links ]
5. - PATTERSON J S, ABAD-FRANCH F, CUBA CUBA C A, MILES M A. Morphometric distinction of domestic and sylvatic populations of Rhodnius ecuadoriensis (Triatominae) from different geographical origins. J Bras Patol 2001; 37: 189. [ Links ]
6.- ABAD-FRANCH F, AGUILAR V H M, PAUCAR C A, et al. Observations on the domestic ecology of Rhodnius ecuadoriensis (Triatominae). Mem Inst Oswaldo Cruz 2002; 97: 199-200. [ Links ]
7.- GRIJALVA M J, PALOMEQUE-RODRÍGUEZ F S, COSTALES J A, et al. High household infestation rate by synanthropic vectors of Chagas disease in Southern Ecuador. J Med Entomol 2005; 42: 68-74. [ Links ]
8.- ABAD-FRANCH F, MONTEIRO F A, PATTERSON J S, et al. Population phenotypic plasticity linked to ecological adaptations in Triatominae. In: XXX Annual Meeting on Basic research in Chagas disease, Caxambu, MG, Brasil. Rev Inst Med Trop S Paulo 2003; 45: 199. [ Links ]
9.- ABAD-FRANCH F, PAUCAR C A, CARPIO C C, et al. Biogeography of Triatominae (Hemiptera, Reduviidae) in Ecuador: implications for the design of control strategies. Mem Inst Oswaldo Cruz 2001; 96: 611-20. [ Links ]
10.- HERRER A, WYGODZINSKY P, NAPÁN N. Presencia de Trypanosoma rangelí Tejera 1920 en el Perú. I El insecto vector Rhodnius ecuadoriensis Lent & León, 1959. Rev Biol Trop 1972; 20: 141-9. [ Links ]
11.- CUBA CUBA C A, MORALES N E, FERNÁNDEZ W. Hallazgo de Rhodnius ecuadoriensis Lent & León, 1958 infectado naturalmente por tripanosomas semejantes a Trypanosoma rangeli Tejera, 1920, en caseríos del distrito de Cascas, Contumazá, Cajamarca-Perú. Rev Inst Med Trop S Paulo 1972; 14: 191-202. [ Links ]
12.- CUBA CUBA C A. Estudo de uma cepa peruana de Trypanosoma rangeli. II Verificação da infecção natural de glándulas salivares em Rhodnius ecuadoriensis. Rev Inst Med Trop S Paulo 1974; 16: 10-8. [ Links ]
13.- CUBA CUBA C A. Estudo de uma cepa peruana de Trypanosoma rangeli IV Observações sobre a evolução e morfogénese do T. rangeli na hemocele e glándulas salivares de Rhodnius ecuadoriensis. Rev Inst Med Trop S Paulo 1975; 17: 284-97. [ Links ]
14.- CUBA CUBA C A. Development of metacyclic forms of triatomid bug's salivary glands ingested by Rhodnius ecuadoriensis. Trans Roy Soc Trop Med Hyg 1979; 66: 944. [ Links ]
15.- CUBA CUBA C A. Revisión de los aspectos biológicos y diagnósticos del Trypanosoma rangeli. Rev Soc Bras Med Trop 1998; 31: 207-20. [ Links ]
16.- KITAJIMA E W, CUBA CUBA C A, BRENER Z. Ultrastructural observations on Trypanosoma (Herpetosoma) rangeli in the salivary glands of Rhodnius ecuadoriensis (Hemiptera, Reduviidae) Parasitol al Día 1998; 22: 65-71. [ Links ]
17.- VALLEJO G R, MACEDO A M, CHIARI E, PENAS D J. Kinetoplast DNA from Trypanosoma rangeli contains two distinct classes of minicircle with different size and molecular organization. Mol Bioch Parasitol 1994; 67: 245-53. [ Links ]
18.- VALLEJO G A, GUHL F, CARRANZA J C, et al. k-DNA markers define two major Trypanosoma rangeli lineages in Latin America. Acta Trópica 2002; 81: 77-82. [ Links ]
19.- URREA D A, CARRANZA J L, CUBA CUBA C A, et al. Molecular characterization of Trypanosoma rangeli strains isolated from Rhodnius ecuadoriensis in Peru R. colombiensis, in Colombia and R. pallescens in Panamá supports a co-evolutionary association between parasites and vectors. Infect Gen Evol 2005; 5: 123-9. [ Links ]
20.- VALLEJO G A, GUHL F, CARRANZA J C, et al. Interaction between Trypanosoma rangeli and Rhodnius sp: A model for molecular epidemiology in American Trypanosomiasis In: IX European Multicolloquium of Parasitology. Medimond 2004; 1: 121-8. [ Links ]
21.- GUILLEN Z, CÁCERES I, ELLIOT A, RAMÍREZ J. Triatominos del Norte Peruano y su importancia como vectores de Trypanosoma spp. Rev Per Entomol 1988; 31: 25-30. [ Links ]
22.- LLANOS Z B. Hallazgo en el Perú del Rhodnius ecuadoriensis Lent & León 1958 naturalmente infectado por el Trypanosoma cruzi. Arch Per Patol Clin 1961; 15: 159-64. [ Links ]
23.- LUMBRERAS H. El problema de la Enfermedad de Chagas en los diferentes Departamentos del Perú. Rev Viernes Med 1972; 23: 43-77. [ Links ]
24.- CROSSAR P,HERNÁNDEZ M,CARACCIO M N, et al. Chromosomal evolution trends of the genus Panstrongylus (Hemiptera, Reduviidae) vectors of Chagas Disease. Infect Gen Evol 2002; 2: 47-56. [ Links ]
25.- MARCILLA A, BARGUES M D, ABAD-FRANCH F et al. Nuclear rDNa ITS-2 sequences reveal polyphyly of Panstrongylus species (Hemiptera: Reduviidae: Triatominae) vectors of Trypanosoma cruzi. Infect Gen Evol 2002; 1: 225-35. [ Links ]
26.- HERRER A, MORALES J. Trypanosomiasis Americana en el Perú. VI Verificación de la Enfermedad de Chagas en la cuenca del Marañón. Rev Med Exp 1955; 9: 83-91. [ Links ]
27.- AMPUERO R C, CUBA CUBA C A, ROLDAN J, VARGAS F. Morphometric of natural domestic and reared populations of Panstrongylus herreri. In: XXXVIII Congresso da Sociedade Brasileira Medicina Tropical, Paraná, Brasil. Rev Soc Bras Med Trop 2002; 35: 186. [ Links ]
28.- CALDERÓN G F, FIGUEROA-KRAP E, NÁQUIRA F. Perú. In: Factores biológicos y ecológicos en la enfermedad de Chagas (Carcavallo R U, Rabinovich J, Tonn R J) OPS/ECO MSAS/SNCh, Buenos Aires, 1985 pp 449-56. [ Links ]
29.- MEJIA G D, VULPE G, BAROT S, et al. Human settling dynamics and estimation of the environmental risk for the American Trypanosomiasis. An example in the active deforestation front in the State of Para Brazil. IX European Multicolloquium of Parasitology. Symposium Trypanosomes, Triatomine and Chagas disease: basic knowledge and applied research, 2004; 4: 179. [ Links ]
30.- TEIXEIRA A R, MONTEIRO P S, REBELO J M, et al. Emerging Chagas Disease: trophic network and cycle of transmission of Trypanosoma cruzi from palm trees in the Amazon. Emer Infect Dis 2001; 71: 100-2. [ Links ]
31.-CARCAVALLO R U, RODRÍGUEZ M E F, SALVATELLA R, et al. Habitats and related fauna. In: Atlas of Chagas Disease vectors in the Americas (Carcavallo R U, Galíndez Girón I, Jurberg J, Lent H), Fiocruz, Rio de Janeiro 1998. pp 561-600. [ Links ]
32.- HERRER A. Observaciones sobre la enfermedad de Chagas en la Provincia de Moyobamba (Departamento de San Martín). Rev Med Per 1956; 10: 59-74. [ Links ]
33.- VEGA J I, YON C, ESCURRA C. Tripanosomiasis Americana en el Distrito de Callayuc, Cajamarca, Perú. J Bras Patol 2001; 37: 267. [ Links ]
34.- VEGA S, NÁQUIRA C, CÁCERES A, et al. Seroprevalencia de la Tripanosomiasis Americana en los Departamentos de Amazonas y Cajamarca- Perú. Parasitol Latinoamer 2005; 60: 220. [ Links ]
35.- CÁCERES A G, TROYES L, GONZALES-PERES A, et al. Enfermedad de Chagas en la región Nororiental del Perú. I Triatominos (Hemiptera, Reduviidae) presentes en Cajamarca y Amazonas. Rev Per Med Exp Salud Públ 2002; 19: 17-23. [ Links ]
36.- LUMBRERAS H, ARRARTE J. La infección natural y experimental del Triatoma carrioni por Tyipanosoma. Arch Per Patol Clin 1956; 10: 107-16. [ Links ]
37.- ARRARTE O J. Nota preliminar acerca de la infección natural del Panstrongylus chinai por Trypanosoma cruzi. Rev Med Per 1955; 26: 247-8. [ Links ]
38.- JARA C A, ESCALANTE H, ROLDAN J, DÍAZ LIMAI E. Distribución y frecuencia de infección por Trypanosoma cruzi de triatominos y Ovisaries en el valle de Chamán, La Libertad, Perú. Sciendo 1998; 1: 23-31. [ Links ]
39.- POLLACK V L, AMPUERO C, ROLDAN J, et al. Morphometric and artificial ecotopes of Panstrongylus chinai (Hemiptera, Reduviidae) in Northern Peru. J Bras Patol 2001; 37: 188. [ Links ]
40.- SALOMÓN D O, RIPOLL C, RIVETTI E, CARCAVALLO R. Presence of Panstrongylus rufotuberculatus (Champion, 1899) (Hemiptera, Triatominae) in Argentina. Mem Inst Oswaldo Cruz 1999; 94: 285-8. [ Links ]
41.-WOLFF M, CASTILLO D. Domiciliation trend of Panstrongylus rufotuberculatus in Colombia. Mem Inst Oswaldo Cruz 2002; 97: 297-300. [ Links ]
42.- HIDALGO R. Trypanosomiasis Americana en el Perú: Observaciones entomológicas en el Departamento de Tumbes. Rev Med Exp 1957; 11: 71-85. [ Links ]
43.- LIZARASO Y. Nota sobre el hallazgo de Triatoma dimidiata y Panstrongylus rufotuberculatus en el Perú. Rev Med Exp 1955; 9: 119-21. [ Links ]
Acknowledgements: The authors express their gratitude to the Division of Epidemiology, Ministry of Health, Peru and the Instituto Nacional de Salud Pública, INS, Ministerio de la Salud del Perú by partial funding of the field research. Special thanks for the valuable assistance received from our Peruvian colleagues: Luis Pollack, Judith Roldan, Franklin Vargas and Edgard Marín, researchers from Universidad Nacional de Trujillo, Perú. Partial financial support from CAPES and CnPq.
Research partly supported by FAP-DF and CAPES.
Cesar Augusto Cuba Cuba