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The abundance of the vector insect, Triatoma dimidiata (Reduviidae) and the ecology of infection with Trypanosoma cruzi

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Title:
The abundance of the vector insect, Triatoma dimidiata (Reduviidae) and the ecology of infection with Trypanosoma cruzi
Translated Title:
La abundancia del insecto vector, Triatoma dimidiata (Reduviidae) y la ecología de la infección con Trypanosoma cruzi ( )
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English
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Vargas, Erica
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Subjects / Keywords:
Parasites   ( lcsh )
Insects   ( lcsh )
Costa Rica--Puntarenas--Monteverde Zone--San Luis   ( lcsh )
Parásitos
Insectos
Costa Rica--Puntarenas--Zona de Monteverde--San Luis
Tropical Ecology Fall 2009
Ecología Tropical Otoño 2009
Genre:
Reports   ( lcsh )
Reports

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Abstract:
A study was conducted in the Monteverde region to determine patterns of infection in Triatoma dimidiata with Trypanosoma cruzi. It was predicted that proximity to domestic animals and looking at the sex ratio would reveal patterns of infection in T. dimidiata. This study was conducted in San Luis, and 12 properties were searched for T. dimidiata. Fourteen individuals were found overall at four sites with two infected individuals. However, the two infected individuals were found in close association with dogs. Fewer nymphs than expected were found this year. Weather patterns of the region could account for the low abundance of T. dimidata. Abundance from past years was also compared to 2002 and 2003. Another long-term study is needed to better understand the dynamics of Chagas disease in the Monteverde area.
Abstract:
Se realizó un estudio en la región de Monteverde para determinar la distribución de la infección en Triatoma dimidiata con Trypanosoma cruzi. Se predijo que la proximidad a los animales domésticos y considerando la proporción de los sexos podría revelar los patrones de infección en T. dimidiata. Este estudio se realizó en San Luis y doce propiedades fueron exploradas en busca de T. dimidiata. Catorce chinches fueron encontrados en general en cuatro sitios con dos chinches infectados. Sin embargo, los chinches infectados fueron encontrados cerca de los perros. Se encontraron menos ninfas de lo esperado para este año. Los patrones climáticos de la región podrían explicar la baja abundancia de T. dimidiata. La abundancia de los años pasados fue comparada con los años 2002 y 2003. Se necesita hacer otro estudio a largo plazo para poder entender mejor las dinámicas de la enfermedad de Chagas en el área de Monteverde.
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Text in English.
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The Abundance of the Vector Insect, Triatoma dimidiata (Reduviidae) and the Ecology of Infection with Trypanosoma cruzi Erica Vargas Department of Biological Sciences, Texas Tech University ABSTRACT A study was conducted in the Monteverde region to de termine patterns of infection in Triatoma dimidiata with Trypanosoma cruzi It was predicted that proximity to domestic animals and looking at the sex ratio would reveal patterns of infection in T. dimidiata This study was conducted in San Luis, and 12 properties were searched for T. dimidiata Fourteen individuals were found overall at four sites with two infected individuals. However, the two infected individuals were found in close association with dogs. Fewer nymphs than expected were found for th is year. Weather patterns of the region could account for the low abundance of T. dimidata Abundance from past years was also compared to 2002 and 2003. Another long term study is needed to better understand the dynamics of Chagas disease in the Montev erde area. RESUMEN Un estudio conducido en la region de Monteverde para determinar la distribucion de infeccion en Triatoma dimidiata con Trypanosoma cruzi Predije que la distancia a los animales domesticos y considerar la proporcin de sexos revelara d istribuciones de infecion en T. dimidiata Este estudio fue conducido en San Luis, y doce propiedades fueron exploradas en busca de T. dimidiata Catorce chinches en total fueron encontrados en cuatro sitos con dos chinches infectados. Pero, los chinche s infectados fueron encontrados cercas de perros. Menos ninfas fueron encontradas de lo esperado para este ao. Es posible que los eventos de tiempo pueden explicar los numeros bajos de T. dimidiata La abundancia de los aos pasados fueron comparados c on las abundancias de los aos 2002 y 2003. Otro estudio de mucho tiempo es necesario para entender ms de las dinmicas de la enfermada de Chagas en la area de Monteverde. INTRODUCTION The ecology of vector borne disease is complex and not well underst ood because it involves the interactions of multiple species. A parasite maintains its population by co existing with a natural reservoir and must complete its life cycle in a vector. This vector transmits the parasite between different hosts perpetuatin g a cycle that is difficult to prevent, unless the vector agent is completely eradicated. Vectors and reservoirs interact with other animals, thus adding more complexity to the system. The vectors and reservoirs are also subject to many abiotic factors a nd this also makes it difficult to predict patterns of infection. However, abiotic and biotic studies are useful because they reveal unusual patterns that may or may not be useful for the prevention of the disease in question. Often, these diseases affec t humans because humans encroach upon forested habitats forcing vectors, reservoirs, and humans to live in the same areas or in overlapping territories (Moore 2008). In addition, some vectors are also able to co exist in the microhabitats that humans crea te (Carcavallo 1999).

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Chagas disease is a vector borne disease that been studied on the molecular and ecological level, but unknown factors still exist. It is a neotropical disease caused by the blood parasite, Trypanosoma cruzi with a distribution from southern United States to Argentina. The insect vectors that transmit Chagas are the assassin bugs from the family Reduviidae with different species associated with specific regions. The protozoan replicates in the alimentary tract of the Reduviidae inse cts and the infective forms pass through the rectum (Brener 1980). The disease is transmitted when the insect takes a blood meal, defecates by the bite wound, and subsequent scratching from the victim According to the Seattle Biomedical Research Institute, the disease affects 16 18 million people in Latin America, with an annual death rate of 20,000 people. The disease occurs in two stages, acute and chronic. The acute stage often has no or mild sympto ms, and the infection goes unnoticed. The infection will usually progress into a chronic form, sometimes exhibiting life threatening symptoms decades after transmission. The parasites commonly infect heart tissue resulting in cardiomyopathy, a deteriorat ion of the heart muscle, which leads to irregular heart rhythm and/or cardiac arrest (Laranja et al. 1956). The parasite can also infect intestinal tissue leading to megacolon, an abnormal dilation of the colon that often requires surgery (Brener 1980). Current anti parasite medications are sometimes not effective even when the disease is caught during the acute stage. Because symptoms sometimes do not appear until years after infection, Chagas can persist in the human population undetected. Heart attac ks caused by Chagas are often misdiagnosed, masking the true threat of the disease in the Americas. Therefore, it is crucial to block transmission of T. cruzi through the insect vector to successfully prevent the disease. Chagas disease is endemic to Cos ta Rica in the regions of Guanacaste, Alajuela, and Puntarenas, and is transmitted by the species, Triatoma dimidiata The insects are sylvatic in origin but are also common around human dwellings (Zeledon et al. 1975). In the wild, the insects are found in tree holes and/or in association with wild rodents and opossums, specifically Didelphis marsupialis (common opossum) (Zeledon et al. 1973). Not surprisingly D. marsupialis has been found to be a natural reservoir, coexisting with the parasite (Kudo 19 66). Near domiciliary areas, the insects are associated with poorly built dwellings or storage areas. They are commonly found in storage areas with woodpiles on dirt floors with a source of blood, such as domestic animals, nearby (Zeledon et al. 2001). For example, past studies have determined that T. dimidiata will feed from dogs, cats, chickens, and Rattus rattus (black rats). There is strong evidence that in certain areas, dogs are becoming the new domestic reservoir (Montenegro et al. 2002). In gen eral, it has been observed that infected individuals are found in close association areas that have domestic animals in close proximity (Lebus 2003). Age correlating to the rate of infection has also been suggested, but this hard to analyze because only r elative age can be determined among nymph stages (Ruth Salas pers. comm). The epidemiology of infection in T. dimidiata in the Monteverde region has been well studied. In addition, the abundance of T. cruzi and its presence in T. dimidiata have also been well documented in the past years. This disease has a medical importance in the community of Monteverde because past studies have shown that T. cruzi is present in the insect vector (Tajrishi 2002, Lebus 2003, Salas, unpublished). Previous studies in the

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area have also revealed that T. dimidiata is more common in San Luis than anywhere else in the Monteverde area and that T. cruzi is present in San Luis. In addition, one study noted that many houses with infected T. dimidiata had domestic animals present in the domiciliary area. It was also determined that between the adults and nymphs, infection was more prevalent among the adults (Lebus 2003). During a long term study in Monteverde from 2006 2008, blood found in the stomachs of T. dimidiata was analyz ed and the most common blood found was rodent (R. Salas pers. comm). Dog and human blood were the third and fourth most common respectively. The presence of opossum blood was detected in 1.5% of insects overall. This supports the fact that rodents are t he main wild reservoir of T. cruzi in the Monteverde region compared to the main reservoir being D. marsupialis in other areas of Costa Rica (Zeledon et al. 1973). This study attempted to reveal patterns of infection in T. dimidiata with T. cruzi in the M onteverde region. Proximity to domestic animals and looking at the sex ratio may have revealed patterns of infection in T. dimidiata I predicted that infected individuals would be closer to domestic animals than non s principle that states populations should have a 1:1 sex ratio, I predicted that there would be no difference in the sex ratio in the population of T. dimidiata The abundance levels from this study were also compared to the numbers obtained from the pas t years, 2002 and 2003. According to data from the Monteverde area, there was less rainfall during the first nine months of 2009 possibly as a result of an El Nio event (Table 1). It was interesting to see if less rainfall had positively affected popula tion numbers since T. dimidiata prefer a dry medium to lay eggs on. I predicted that the abundance levels of both adults and nymphs would be higher than the results found in 2002 and 2003. TABLE 1. Total precipitation in mm, average minimum and maximum temperatures in Celsius for the Monteverde area in 2002, 2003, 2009. Data for 2009 is only up to August 31, 2009. 2002 2003 2009 Precip (mm) 7.7 7.5 6.3 Min (C) 15.3 15.5 15.4 Max (C) 21.1 21.5 21.1 METHODS S AMPLE COLLECTION I sampled twelve properties in San Luis, Monteverde, Puntarenas, Costa Rica from 31 October to 16 November 2009 by searching the bodegas or trojas of each property. I systematically searched the area inside the bodega, and if there was a woodpile present, I focused my eff orts there. To search for additional nymphs, I sifted through dirt using a trowel and strainer (R. Salas pers. comm). D ATA C OLLECTION When I found an insect, I would measure in meters from the point of discovery to the closest domestic animal. All the insects collected were taken to the Estacin Biolgica, Monteverde, Costa Rica. At the station, they were marked and placed in a cage with a mouse in order to feed. After feeding, each T. dimidiata was killed and then sex was determined. Each insect wa s dissected for the extraction of fecal

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matter from the intestine. The fecal material was smeared on a glass slide with a drop of 0.85% saline solution. Then a drop of 10% methylene blue was added with a cover slip on top. The slide was viewed underneat h a compound light microscope at 400 X for the presence of T. cruzi Slides were searched for a maximum of 20 minutes to confirm or negate the presence of T. cruzi S TATISTICAL A NALYSES I performed an ANOVA analysis to determine if infected individuals were found closer to domestic animals (JMP, 2002). I used several chi square tests to determine if the sex ratio of all individuals found was 1:1, to determine if there were more infected individuals found than expected, to determine if there more infecte d males found than expected, and to determine if there were fewer nymphs found than expected. To compare with the data from 2002 and 2003, I performed chi square tests on the adults and nymphs found and on the infected versus non infected individuals foun d for each year. RESULTS Fourteen individuals were found at four different sites in San Luis overall, 5 males, 6 females, and 3 nymphs. Only two individuals were positive for T. cruzi both of them being male (Figure 1). F IGURE 1. Number of total individuals found (N = 14) divided into sex. Number of infected individuals found also included, both male (N = 2). There is no difference between the numbers of males, females, and nymphs found than expected. There was no rela tionship between infected individuals and the distance to the nearest animal (F = 0.1667, df = 6, p = 0.9779). However, it is worth noting that one infected male from one site was found 0 m from a dog and another infected male was found 0.9 m from a dog a s well (Figure 2).

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FIGURE 2. Number of individuals found at each distance measured from site of discovery to the closest animal (N = 14). Infected individuals are also included at 0 m and 0.9 m from the closet animal (N = 2 ). In this study, fewer nymphs than expected were found, and more adults than expected were found. There was no difference between the females, males, and nymphs found than expected meaning that the sex ratio was approximately 1:1. There was also no d ifference between the infected and non infected males found than expected. Fewer infected individuals than expected were found (Table 2). TABLE 2. Chi squared values and p values of four different categories tested. Data is from this study (Fall 2009). Adults / Nymphs Infected / Non infected Females / Males / Nymphs Infected / Non infected Males Results of x2: x2 0.857 0.931 0.436 0.655 df 1 1 1 1 p value 0.033 0.007 0.607 0.418 Comparing the numbers from 2009 to the numbers from 2002 and 2003, it is clear that fewer individuals overall and fewer nymphs were found (Table 3). In 2002, there was no difference between adults and nymphs found than expected (Table 4). In 2003, there were more nymphs found than expected (Table 5). In both 2002 and 2003, there was no difference between infected and non infected individuals found overall than expected (Table 4, 5).

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TABLE 3. Abundance of Triatoma dimidiata in San Luis in three years of data collection. Numbers for adults and nymphs are pres ent for the years of data collection. Percentage of infected individuals are present for each time period. Year 2002 2003 2009 Adults 20 17 11 Nymphs 28 86 3 Total 48 103 14 Positive 19 56 2 % 39.5 54.4 14.3 TABLE 4. Chi squared value s and p values of two different categories tested. Data is from 2002. Adults / Nymphs Infected / Non infected Results of x2: x2 0.618 0.699 df 1 1 p value 0.24 8 0.149 TABLE 5. Chi squared values and p values of two different categories tested Data is from 2003. Adults / Nymphs Infected / Non infected Results of x2: x2 0.999 0.54 df 1 1 p value 1.06 E 11 0.375 DISCUSSION Because the sample size of T. dimidiata was small, it was difficult to see any statistically supported trends. The percentage of infection was low. There was no skewed sex ratio, but the number of nymphs found during this study was abnormally low. The low individual counts and the low nymph numbers could be explained by the high amounts of rain that fell during the weeks of November 1 st and November 8 th due to the influence of Hurricane Ida on the country. The rain made the dirt floors in many sites wet and unfavorable. Since nymphs prefer dry dirt floors for camouflage, it is possible that they moved to an are a that was out of my searchable range. In addition, because adults have

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wings they had the option of migrating to areas of warmer, drier climates during the time period of rain. While there was no difference between proximity to animals and infected vers us non infected individuals, it is worth noting characteristics of specific sites where infected individuals were found. The two infected individuals found 0 m and 0.9 m from a dog respectively probably used them as a constant source of blood. At the two sites where all individuals found were negative, their closest domestic animal was a chicken and, therefore, the most likely source of blood for T. dimidiata This observation implies that dogs are an important link in the web of transmission between rod ents as reservoirs and humans as hosts for T. cruzi This conclusion supports the trend that dogs are becoming the new domestic reservoir in Costa Rica (Montenegro et al. 2002). However, even more information from the Monteverde area is needed. Blood o f dogs from the Monteverde area should be tested for the presence of T. cruzi Rodents should also be trapped in areas around human dwellings and in the forest, and have their blood tested for the presence of the protozoan. It would be interesting to see how the patterns vary from Monteverde compared to the patterns observed in Guanacaste (Zeledon et al. 1973). Future studies should look at the dynamics of rodent populations and infection to see what species are most likely to be carriers. Residents sh ould be aware of T. dimidiata and its importance as a vector of Chagas and its relationship with domestic animals. It may be difficult to prevent transmission of T. cruzi to humans. Prevention of Chagas disease may be best accomplished by complete disrup tion of favorable habitat to discourage further colonization or prevent initial establishment of T. dimidiata (Zeledon et al. 2008). However, it is important to put together as much information about the dynamics of Chagas so that all alternatives can be taken into consideration for the control of the disease. ACKNOWLEDGEMENTS I would like to thank my advisor, Anjali Kumar, for all her guidance and help in designing and modifying a project. I express my gratitude to Ruth Salas for sharing her previous r esearch with me. I thank Moncho Calderon, Pablo Allen, and Yimen Araya for all their extra help. I thank Alan Masters and Frank Joyce for being supportive and providing advice. I thank the Serpentario for providing me with mice when I needed them for th is project. I would to like to thank my fellow classmates for being so amazing and helping each other during these stressful times. I express gratitude to my host family because they made every moment of my homestay worth it. Finally, I would like to th ank the residents of San Luis for letting me search their properties. LITERATURE CITED B RENER Z. 1980. Immunity to Trypanosoma cruzi. In: Lumsden, W., Editor, Advances in Parasitology, Volume 17 Academic Press, Missouri, pp. 247 248. C ARCAVALLO R U. Climatic Factors Related to Chagas Disease Transmission. 1999. Memorias do Instituto Oswaldo Cruz 94(Suppl.1): 367 369. K UDO R. R. 1966. Protozoology Charles C. Thomas Publisher, Illinois, pp. 413 415. L ARANJA F. S., E. D IAS G. N OBREGA AND A. M IRANDA

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Epidemiologic, and Pathologic Study. Circulation 14: 1035 1060. L EBUS D 2003. The role of elevation in the abundance of Triatoma dimidiata and its frequency of infection with the protozoan Trypano soma cruzi in the Monteverde Region. In University of California Education Abroad Program, Fall 2003. M ONTENEGRO V.M., M. J IMENEZ J.C. P INTO D IAS AND R. Z ELEDON 2002. Chagas Disease in Dogs from Endemic Areas of Costa Rica. Memorias do Instituto Oswaldo Cruz 97(4): 491 494. M OORE C.G. 2008. Interdisciplinary research in the ecology of vector borne diseases: Opportunities and needs. Journal of Vector Ecology 33(2): 218 224. T AJRISHI R. 2002. The presence of Chagas bugs ( Triatoma dimidia ta ) and the protozoa responsible for Chagas disease ( Trypanosoma cruzi ) in Monteverde region. In University of California Education Abroad Program, Fall 2002. Z ELEDON R, G. S OLANO A. Z UNIGA AND J.C. S WARTZWELDER 1973. Biology and ethology of Tria toma dimidiata (Latreille, 1811): III. Habitat and blood sources. Journal of Medical Entomology 10(4): 363 370. ----------, R., G. S OLANO L. B URSTIN AND J.C. S WARTZWELDER 1975. Epidemiological pattern of a Rica. The American Journal of Tropical Medicine and Hygiene 24(2): 214 225. ----------, R., V.M. M ONTENEGRO AND O. Z ELEDON 2001. Evidence of Colonization of Man made Ecotopes by Triatoma dimidiata (Latreille, 1811) in Costa Rica. Memorias do Ins tituto Oswaldo Cruz 96(5): 659 660. ----------, R., J.C. R OJAS A. U RBINA M. C ORDERO S.H. G AMBOA E.S. L OROSA AND S. A LFARO 2008. Ecological control of Triatoma dimidiata (Latreille, 1811): five years after a Costa Rican pilot project. Memorias do Instituto Oswalldo Cruz 103(6): 619 621.


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La abundancia del insecto vector, Triatoma dimidiata (Reduviidae) y la ecologa de la infeccin con Trypanosoma cruzi
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A study was conducted in the Monteverde region to determine patterns of infection in Triatoma dimidiata with Trypanosoma cruzi. It was predicted that proximity to domestic animals and looking at the sex ratio would reveal patterns of infection in T. dimidiata. This study was conducted in San Luis, and 12 properties were searched for T. dimidiata. Fourteen individuals were found overall at four sites with two infected
individuals. However, the two infected individuals were found in close association with dogs. Fewer nymphs than expected were found this year. Weather patterns of the region could account for the low abundance of T. dimidata. Abundance from past years was also compared to 2002 and 2003. Another
long-term study is needed to better understand the dynamics of Chagas disease in the Monteverde area.
Se realiz un estudio en la regin de Monteverde para determinar la distribucin de la infeccin en Triatoma dimidiata con Trypanosoma cruzi. Se predijo que la proximidad a los animales domsticos y considerando la proporcin de los sexos podra revelar los patrones de infeccin en T. dimidiata. Este estudio se realiz en San Luis y doce propiedades fueron exploradas en busca de T. dimidiata. Catorce chinches fueron encontrados en general en cuatro sitios con dos chinches infectados. Sin embargo, los chinches infectados fueron encontrados cerca de los perros. Se encontraron menos ninfas de lo esperado para este ao. Los patrones climticos de la regin podran explicar la baja abundancia de T. dimidiata. La abundancia de los aos pasados fue comparada con los aos 2002 y 2003. Se necesita hacer otro estudio a largo plazo para poder entender mejor las dinmicas de la enfermedad de Chagas en el rea de Monteverde.
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