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    Map of Ecuador showing the study area in the Amazon region and the location of the communities found to be seropositive and seronegative for Trypanosoma cruzi. Community labels correspond to the ID number of seropositive communities shown in Table 2.

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    Age (years) distribution of sampled population and individuals seropositive for Trypanosoma cruzi found in four provinces of the Ecuadorian Amazon region.

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SEROPREVALENCE AND RISK FACTORS FOR TRYPANOSOMA CRUZI INFECTION IN THE AMAZON REGION OF ECUADOR

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  • 1 Tropical Disease Institute, College of Osteopathic Medicine, Department of Biomedical Sciences, Ohio University, Athens, Ohio; Instituto Nacional de Higiene Zona Norte, Quito, Ecuador; Escuela de Biologia, Universidad Católica del Ecuador, Quito, Ecuador

Trypanosoma cruzi infection in the Ecuadorian Amazon region has recently been reported. A seroepidemiologic survey conducted in four provinces in this region indicates a seroprevalence rate of 2.4% among the 6,866 samples collected in 162 communities. Among children ≤10 years of age, 1.2% were seropositive. Risk factors for T. cruzi seropositivity were having been born and remaining in the Ecuadorian Amazon provinces, age, living in a house with a thatch roof and open or mixed wall construction, recognizing the vector insects, and reporting being bitten by a triatomine bug. These data suggest active transmission of Chagas’ disease in the Ecuadorian Amazon region is associated with poor housing conditions, and highlight the need for further studies aimed at understanding the biology of the insect vectors, reservoir species, and the clinical impact of T. cruzi infection as the basis for future educational and control programs in this region.

INTRODUCTION

Chagas’ disease has been reported in Ecuador since the1930s.1 Although there have been several studies during the intervening decades documenting the presence of Chagas’ disease in certain areas in the coastal region,1 the current status of the disease in this country is unclear. The latest estimates indicate that there are up to 200,000 people (1.6% of the population of the entire country) infected and approximately three million people (25%) at risk.1

Ecuador is divided from north to south by the Andes Mountains, which constitute a geographic barrier for the movement of the triatomine vectors from the western coastal tropical areas to the Upper Amazon Basin, including the Ecuadorian Amazon region. Since the 1960s, there has been a significant movement of the population to the Amazon region from different regions of the country, including areas considered endemic for Chagas’ disease. This migration has been encouraged by the opportunities offered by oil exploration and the land made accessible by the roads and rivers as part of the government program to colonize the region. It has been proposed that infected migrants brought infectious agents to the Amazon region, including Trypanosoma cruzi, from other regions of the country. Difficult accessibility and limited public health infrastructure could be responsible for the lack of epidemiologic information regarding Chagas’ disease in the Amazon region. However, in 1991, Amunarris and others reported acute cases in this region.2 Chico and others in 1997 reported high seroprevalence in communities located along a portion of the Napo River in the Orellana Province,3 formerly part of Napo Province. Finally, Abad-Franch and others in 2001 reported the presence of nine different species of triatomine insects in the Amazon region.4 These studies, combined with sporadic new case information provided by the Ministry of Health of Ecuador, suggest the presence of active Chagas’ disease transmission in the Amazon region.

This study expands prior seroprevalence studies in the Amazon region and describes some of the risk factors favoring disease transmission in the area. Our results confirm and extend previous findings of high prevalence and support the hypothesis of active Chagas’ disease transmission in the Amazon region.

MATERIALS AND METHODS

Study area and population.

This study was conducted in the Ecuadorian Amazon region provinces of Sucumbios, Napo, Orellana, and Pastaza (Figure 1). The altitude ranges from approximately 1,200 meters above sea level on the eastern slopes of the Andes Mountains to 350 meters above sea level near the borders with Peru and Colombia. The climate in this region is tropical and comprises ecologic areas of montane forest and tropical humid forest. The northwestern portion of this region is accessible via two roads that originate in the northern and central highlands and traverse the foothills of the eastern slopes of the Andes Mountains from north to south. The western portion of these provinces is accessible via a road system created to serve the oil exploration industry in the northern province of Sucumbios with branches into Orellana Province; some of the most remote communities have airstrips that allow access via small planes. However, most of the area is accessible only via the extensive pluvial system that constitutes the upper Amazon River basin. The population is a mixture of indigenous and colono (migrants from other regions of the country) populations. The population is concentrated in towns, villages, and small, disseminated family unit compounds (farms) located near the rivers or roads.

Sampling.

Systematic sampling was performed from 1997 to 1999 in four Amazon region provinces according to the accessibility of the communities. Most of the sampling was conducted in communities along rivers or roads. Samples were collected from every third house in the community until the desired sample size was reached. This was based on the previously estimated number of inhabitants and an expected 2% prevalence and 3% worst expected result (EpiInfo version 6.0; Centers for Disease Control and Prevention, Atlanta, GA). Informed consent was obtained from all human adult participants and from the parents or legal guardians of minors taking part in the study, in accordance with Ohio University Institutional Review Board policies and procedures. Participants ≥10 years of age were asked to respond to an epidemiologic questionnaire related to housing conditions, previous residence location, and risk factors. Questionnaires were administered in Spanish by trained field technicians.

Blood sampling.

Blood collection was performed by finger prick using disposable lancets (Fisher Scientific, Pittsburgh, PA) onto filter paper (Whatman #1; Fisher Scientific). Pieces of filter paper were lightly impregnated with 0.01% thymerosal (Sigma, St. Louis, MO) in talcum powder prior to sample collection to prevent fungal and bacterial growth. Enough blood was collected to completely saturate six circles (6-mm diameter) printed in the filter paper. Filter paper with samples were placed in individual plastic bags along with the questionnaire and kept at ambient temperature until the team returned to a facility equipped with refrigeration, where the samples were stored at 4°C until use.

Serologic analysis.

For the elution of antibodies from filter paper, a 5-mm diameter punch was obtained from every sample and incubated for two hours at room temperature in 200 μL of 0.5% Tween 20 (Sigma) in phosphate-buffered saline (PBS) (137 mM NaCl, 2.7 mM KCl, 4.3 mM Na2HPO4, 1.4 mM KH2PO4, pH 7.3) using 96-well polystyrene plates (Falcon 3912 Microtest III; Fisher Scientific). Simultaneously, other 96-well polystyrene plates were coated with 0.5 μg/well of detergent-extracted T. cruzi Brazil strain epimastigote antigen5,6 and blocked with 5% non-fat dry milk (Carnation; Nestle USA, Solon, OH) and 0.05% anti-foam A (Sigma) in PBS. The eluate was then diluted 1:2 with PBS-5% milk and 100 μL per well were added to the antigen-coated plate and incubated for 90 minutes at room temperature. Plates were then washed five times in 0.05% Tween-20-PBS and incubated for one hour at room temperature in a 1:2,000 dilution of horseradish peroxidase-conjugated goat anti-human immunoglubulin (AHI0704; Biosource, Camarillo, CA) in PBS-5% milk. The plates were then washed as above, developed, and the absorbance was measured as previously described.6 Each plate contained positive, negative, and blocking controls. All samples and controls were assayed in duplicate. Cut-off points were calculated individually for each plate using the positive and negative control values as a reference (positive cut-off value =negative control plus 2.5 standard deviations of the average negative control mean). Samples were classified as positive, negative, and doubtful. Both positive and doubtful samples, as well as a number of randomly chosen negative samples, were assayed two more times. Samples that were positive at least two times were considered positive.

Collection of blood onto filter paper for serologic analysis has been successfully used in previous serologic studies.7–9 The logistical difficulty in reaching the population in this area, combined with the local resistance to venous blood sampling, makes blood collection onto filter paper using a finger prick a convenient methodology. Acceptance by the population and sample stability at room temperature are key features of this approach. However, it is important to note that filter paper collection, rather than serum collection, has some limitations, which includes lower antibody concentration, reduction of titer over time, and limited sample availability for confirmatory testing.10 Nevertheless, our experience indicates an acceptable degree of correlation between the results obtained from filter paper and serum samples under carefully monitored testing conditions (Grijalva MJ, unpublished results).

Infection of humans with T. rangeli has been reported in the Amazonic region of Colombia,11 Peru,12 and Brazil,13 but not in Ecuador. It is possible that some of the seropositivity found in this and previous studies2,3 could be due to the known cross-reactivity between T. cruzi and T. rangeli.14 Further studies are required to test this hypothesis.

Data management and analysis.

Epidemiologic data was coded and entered into a database along with the serologic results. Statistical analyses were performed using SAS (Cary, NC) software package version 8.1. Descriptive statistics were computed for all variables of interest for comparison purposes and to examine distributions for fit to statistical assumptions. Univariate analyses were performed between T. cruzi seropositivity and all other variables. Chi-square or Fisher’s exact tests, as appropriate, were used to examine nominal level variable comparisons. Odds ratios (ORs) and 95% confidence intervals were estimated using the Mantel-Haenszel method. An alpha level of 0.05 was used for determination of statistical significance. Household construction, age, and migration variables were analyzed using multivariate logistic regression models to test their independent relationships with T. cruzi seropositivity.

Geographic information.

Maps were purchased from the Insituto Geográfico Militar and the Instituto Nacional de Estadística y Censo (INEC), (Quito, Ecuador). Geographic T. cruzi seropositivity maps were generated using MapInfo version 6.0 (MapInfo, New York, NY).

RESULTS

A total of 6,866 samples were collected within the four provinces studied. The overall demographics and household characteristics are presented in Table 1. The age and sex distribution of the sample conforms to the estimated distribution of the country and the region, according to the latest census15 (Figure 2). The serologic results (Table 2) showed a general seroprevalence of 2.4% and ranged from 1.4% in Sucumbios Province to 3.4% in Orellana Province.

Forty-seven of the 162 sampled communities (29%) had individuals seropositive for T. cruzi in the sampled population (Table 2). The seroprevalence in the communities ranged from 0% to 13.6%. The geographic distribution of the seropositive and seronegative communities for which geographic information was found in the reference maps is shown in Figure 1.

Univariate analysis demonstrated an association between age and T. cruzi seropositivity that was also statistically significant in the multivariate model. Thirty-three (1.2%) of 2,663 children ≤10 years old were seropositive for T. cruzi. The youngest seropositive child was two years old and the average age of the seropositive children was 6.6 years. The results also show an association between no migration or migration within communities in the same province and T. cruzi seropositivity (Tables 3 and 4). However, it is worth noting that several seropositive individuals reported moving from the provinces of Loja (4) and El Oro (1), which are considered endemic for Chagas’ disease, and from Pichincha (1) and Chimborazo (1) provinces, which are not considered endemic.

Living in a house with walls of open or mixed type construction and made of materials such as bamboo cane and wood boards, when compared with closed type walls (cement, brick, or cinderblock), was strongly associated with T. cruzi seropositivity in the univariate analysis. However, only walls of mixed construction retained a statistically significant association with seropositivity in the multivariate analysis (Table 3 and 5). Conversely, an open type of roof (thatched) was associated with increased risk for T. cruzi seropositivity when compared with a closed type of roof (cement, tiled, or zinc plate) in both the univariate and multivariate analyses (Table 3 and 5).

Recognition of triatomine bugs by participants ≥10 years old was assessed. Sixty-three percent of responders recognized one or more species of kissing bugs. Of these, 71% reported having seen the insects inside their domicile. Thirty-seven percent of the respondents reported having been bitten by a triatomine bug. In addition, 59% reported having had their house sprayed with insecticide in the past (Table 1). Interestingly, recognition of the insects and reporting being bitten were associated with seropositivity (ORs =1.81 and 1.79, respectively) while intra-domiciliary insecticide spraying did not show a statistically significant relationship to being seropositive for T. cruzi (Table 3). Other factors such as sex, number of inhabitants per house, and reporting constipation or having being diagnosed with heart problems were not significantly associated with seropositivity.

DISCUSSION

The present study represents a collaborative effort to update the status of Chagas’ disease in Ecuador by examining the seroprevalence for T. cruzi and by analyzing for possible risk factors among samples collected in four provinces in the Ecuadorian Amazon region. Ecuador has been considered endemic for Chagas’ disease since the 1930s.1 Multiple reports on the presence of the disease in the coastal areas16–20 and in blood banks have been published.6,21–23 However, it was generally believed that endemicity was restricted to the coastal region of the country. The first reports of Chagas’ disease in the Amazon region by Amunarriz and others in 19912 were followed by other studies that found high seroprevalence in the area3 and reports of the existence several triatomine species in this region.4

Demographically, the population is composed of two segments: indigenous and colono. Agriculture is the main economic activity. The oil industry typically brings in personnel from other regions of the county or from other countries. In contrast to the varieties of simple house construction used by the indigenous and colono population, the oil workers are usually housed in quarters with air conditioning, screened windows, and other factors that minimize exposure to vectors, requiring special epidemiologic consideration that is beyond the scope of this study. Sampling was concentrated on both indigenous and colono communities accessible by boat or road. Some of the communities sampled consist of only a few houses spread over a large area. In others, there is a larger number of houses clumped together near the rivers or roads with a few dispersed in the immediate vicinity. All efforts were made to maintain the sampling scheme outlined in the Materials and Methods. However, in some instances, the absence of people at the time of the visit was a barrier to obtaining an adequate community sample size. In some communities, not enough individuals were available to ensure the statistical probability of representing the population of that specific area. These small populations provided data useful for analysis at the regional level, but less so at the community level.

A total of 6,866 samples were collected from 162 communities. Seropositive samples were found in 29% of these communities. Although some clustering in the geographic distribution of these communities was observed, it is difficult to speculate as to the reason. It is possible that a larger sample would yield a more homogeneous distribution of seropositive communities. Alternatively, it could be hypothesized that people that brought the disease from other regions and infected the local triatomines could have immigrated to certain communities but not others. In addition, it is possible that in certain areas T. cruzi could have been present in vector populations before human populations were established.

Ecuador’s age pyramid is typical of a developing nation with a large population of children and a sharp decrease in the population with age.15 Indeed, the high proportion of infants is related to lack of appropriate health care and sanitation, high infant mortality rates, and other factors that affect the population of the Amazon region. The fact that the sex ratio of the sampled population is balanced and consistent with population estimates for these provinces in Ecuador suggests that the sample is representative of the general population of the area. Sex was not found to be associated with seropositivity, suggesting that the different sex roles do not have an effect on transmission. Conversely, age was found to be associated with seropositivity, which is expected for a chronic, life-long infection, because increased time of exposure would increase the risk of being infected with T. cruzi.

Our data show that 1.2% of the children ≤10 years old were seropositive for T. cruzi and suggest that Chagas’ disease is actively transmitted in the Amazon region. In addition, univariate and multivariate analysis of reported migration patterns suggests that being born and remaining in this region (no migration/migration within province) constitutes a risk factor for seropositivity for T. cruzi when compared with migration from other provinces or regions. Our data also suggest that the population is exposed to active transmission in some communities. The migratory movement of the population from other regions cannot be dismissed as a contributing factor to Chagas’ disease in the Amazon region. In fact, seropositive individuals were found that reported previous residence in Loja and El Oro Provinces, which are considered endemic, and from Chimborazo and Pichinca, which are not considered endemic, but have tropical and subtropical areas where the prevalence of Chagas’ disease has not yet been determined.

The risk for being seropositive for T. cruzi was also higher among populations that live in dwellings that have an open and mixed type of wall construction and thatched roofs. This is consistent with the well-known fact that the prevalence of Chagas’ disease is higher among the poorest population living in crudely constructed houses that do not constitute a barrier for sylvatic haematophagus triatomine bugs and may provide a habitat for the domiciliation of triatomine colonies.24 Differences in house construction and economic status of the population could account for the differences in seroprevalence among communities that are located geographically close to each other. However, as noted, sample size could also play a role in this distribution.

Interestingly, an individual’s ability to recognize triatomine insect species, which indicates familiarity with them, was associated with being seropositive for T. cruzi. It was not possible to determine if those responding affirmatively to recognition of triatomine insect species were able to differentiate triatomine bugs from non-hematophagous reduviid bugs or other insects present in the region that resemble triatomines. Reporting being bitten by a kissing bug was associated with increase risk of T. cruzi seropositivity. Although T. cruzi transmission occurs via the feces of infected triatomine insects, reporting being bitten indicates close contact with these bugs. Interestingly, reporting intra-domiciliary insecticide spraying was not found to be associated with seropositivity. However, the questionnaire did not allow for discrimination of when or how often the insecticide application took place. Therefore, the effectiveness of this method of vector control remains to be investigated.

Our results indicate that there is active transmission of Chagas’ disease in the Ecuadorian Amazon region and stresses the need for a Chagas’ disease control program to be implemented in the area. However, more studies are required to understand the biology of the vectors and mammalian reservoirs occurring in the area, the association between being seropositive for T. cruzi and clinical disease, and the genetic relationships between the T. cruzi strains circulating in this region and other regions of Ecuador.

Table 1

Overall demographics, household characteristics, and individual responses to entomologic questions of the population surveyed

No.%
* Based on the number of participants that reported previous residence data. Endemic provinces outside of the region include those in the Costal region and Loja Province.
† Open walls include bamboo cane, wood, or adobe; closed walls include brick, cinderblock, or cement; mixed walls include combinations of materials used in open and closed wall construction.
‡ Open roof includes thatch, bamboo, ardex, wood, mixed, or other materials; closed roof includes zinc, ceramic, or cement.
Sex
    Male3,495/6,86950.9
    Female3,374/6,86949.1
Age, years, mean (range)19.4 (0.1–98)
Number of people in household
    Mean (range)7.0 (1–20)
Migration*
    None/within province of current residency735/1,94137.9
    Outside province/within Amazon region313/1,94116.1
    Outside region from non-endemic province410/1,94121.1
    Outside region from endemic province483/1,94124.9
Type of walls†
    Open4,133/5,31877.7
    Closed347/5,3186.5
    Mixed838/5,31815.8
Type of roof‡
    Open2,204/5,31441.5
    Closed3,110/5,31458.5
House sprayed with insecticide
    Yes3,173/5,37159.1
    No2,198/5,37140.9
Recognition of triatomine insects
    Yes3,865/6,12463.1
    No2,259/6,12436.9
Been bitten by a triatomine insect
    Yes1,720/4,57437.6
    No2,854/4,57462.4
Table 2

Trypanosoma cruzi seroprevalence by province, county, and in seropositive communities in the Ecuadorian Amazon region

Province/county/community*/ID†No.‡Province/county/community*/ID†No.‡
*Data shown only for seropositive communities (42 of 162 sampled).
†ID number correlates with community labels in Figure 1. Communities with no ID number did not appear in the maps available for reference.
‡Number seropositive/total sampled.
§The overall seroprevalence for the 6,866 samples collected was 2.4%.
¶Sample size smaller than required based on a priori estimates.
Napo Province40/1,7302.3Pastaza Province8/4751.7
    El Chaco County0/500    Arajuno County0/160
    Quijos County0/400    Mera County0/120
    Tena County40/1,6402.4Santa Clara County0/80
        1 Ahuano1/2970.3    Pastaza County8/4321.9
        2 Campana2/219.5        11 Alto Corrientes1/11¶9.1
        3 Chontapunta1/1240.8        12 Bobonaza2/326.3
        4 Cruz Chigta1/1001.0        13 El Inca1/661.5
            Escupolo1/442.27            Las Palmas3/358.6
        5 Misahuallí1/1160.9        14 Nuevo Corrientes1/12¶8.3
        6 Pano2/484.2
        7 Peurto Loja12/1418.5Orellana Province84/2,5043.4
        9 Shandia5/806.3    Joya de los Sachas County0/1850
        10 Santa Rosa (Tena)14/2615.4    Loreto County0/1350
    Orellana County8/4411.8
Sucumbios Province31/2,1571.4        26 Amarún Meza2/277.4
    Lago Agrio County2/5460.4        27 El Edén3/903.3
        15 Lago Agrio2/2880.7        28 García Moreno1/11¶9.1
            Turupunta2/2010.0
    Putumayo County24/1,2611.9    Aguarico County76/1,7434.4
        Bs 552/812.5
        16 Lorocachi6/1264.8        Chiroisla9/1755.1
        17 Palma Roja3/674.5        Fronteras Del Ecuador5/3912.8
        18 Puerto El Carmen2/1381.4        29 Huiririma4/449.1
        19 San Miguel4/1422.8            Limonyacu3/387.9
        20 Santa Rosa1/323.1            Martinica1/591.7
        21 Silvayacu2/593.4        30 Nueva Armenia2/494.1
        22 Tase3/2213.6        31 Nuevo Rocafuerte11/3103.5
        23 Tigre Playa1/531.9        32 Pandochicta2/405.0
        33 Puerto Miranda4/458.9
    Shushufindi County5/3501.4
        24 Panacocha1/821.2        Puerto Quinche2/842.4
        25 Pompeya4/1882.1        34 Samona2/375.4
            San Vicente9/1396.5
            Santa Rosa (Miranda)4/894.5
        35 Santa Teresita7/1893.7
        36 Sinchichigta9/6913.0
        37 Tiputini2/2500.8
Table 3

Univariate associations between Trypanosoma cruzi seropositivity and select variables*

VariableSeropositive no. (%)Seronegative no. (%)OR (95% CI)P
*OR =odds ratio; CI =confidence interval.
†Open roof includes thatch, bamboo, ardex, wood, mixed, or other materials; closed roof includes zinc, ceramic, or cement.
‡Open walls include bamboo cane, wood, or adobe; mixed walls include combinations of materials used in open and closed wall construction; closed walls include brick, cinderblock, or cement.
Age, years, mean29.219.1<0.0001
Age, years (categorized)
    ≤50127 (78.4)6,310 (94.7)1
    >5035 (21.6)354 (5.3)4.91 (3.33, 7.25)<0.0001
Number of people in household
    Mean7.16.90.4000
Sex
    Male85 (52.2)3,407 (50.8)1.05 (0.77, 1.44)0.7392
    Female78 (47.9)3,296 (49.2)1
Migration (new categorization)
    None/within province297063.93 (1.51, 10.21)0.0026
    Outside province/within region43091.23 (0.33, 4.64)0.7518
    Outside region from non-endemic province24080.47 (0.09, 2.43)0.3556
    Outside region from endemic province54781
House fumigated
    Yes70 (54.3)3,103 (59.2)0.82 (0.56, 1.16)0.2583
    No59 (45.7)2,137 (40.8)1
Type of roof†
    Open85 (63.0)2,119 (40.9)2.45 (1.72, 3.49)<0.0001
    Closed50 (37.0)3,057 (59.1)1
Type of walls‡
    Open88 (64.7)4,045 (78.1)3.75 (0.92, 15.31)0.0477
    Mixed46 (33.8)792 (15.3)10.02 (2.42, 41.51)<0.0001
    Closed2 (1.5)345 (6.7)1
Recognized triatomine
    Yes116 (75.3)3,748 (62.8)1.81 (1.25, 2.62)0.0015
    No38 (24.7)2,219 (37.2)1
Report been bitten by triatomine
    Yes68 (51.1)1,652 (37.2)1.79 (1.25, 2.49)0.0011
    No65 (48.9)2,787 (62.8)1
Table 4

Multivariable model for associations between Trypanosoma cruzi seropositivity and age and migration *

VariableOR (95% CI)P
* OR =odds ratio; CI =confidence interval.
Age >50 years7.52 (3.74, 15.10)<0.0001
Migration
    None/within province3.99 (1.52, 10.48)0.0049
    Outside province/within region0.8 (0.23, 3.41)0.8666
    Outside Amazon region from non-endemic province0.39 (0.07, 2.02)0.2587
    Outside Amazon region from endemic province1
Table 5

Multivariate model for associations between Trypanosoma cruzi seropositivity and wall and roof construction materials*

VariableOR (95% CI)P
*OR =odds ratio; CI =confidence interval.
† Open walls include bamboo cane, wood, or adobe; mixed walls include combinations of materials used in open and closed wall construction; closed walls include brick, cinderblock, or cement.
‡ Open roof includes thatch, bamboo, ardex, wood, mixed, or other materials; closed roof includes zinc, ceramic, or cement.
Type of walls†
    Open2.84 (0.69, 11.69)0.1493
    Mixed6.03 (1.41, 25.75)0.0153
    Closed1
Type of roof‡
    Open1.89 (1.30, 2.76)0.0010
    Closed1
Figure 1.
Figure 1.

Map of Ecuador showing the study area in the Amazon region and the location of the communities found to be seropositive and seronegative for Trypanosoma cruzi. Community labels correspond to the ID number of seropositive communities shown in Table 2.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 69, 4; 10.4269/ajtmh.2003.69.380

Figure 2.
Figure 2.

Age (years) distribution of sampled population and individuals seropositive for Trypanosoma cruzi found in four provinces of the Ecuadorian Amazon region.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 69, 4; 10.4269/ajtmh.2003.69.380

Authors’ addresses: Mario J. Grijalva, Jaime A. Costales, and Edwin C. Rowland, Tropical Disease Institute, College of Osteopathic Medicine, Department of Biomedical Sciences, Ohio University, 333 Irvine Hall, Athens, OH 45701, Telephone: 740-593-2192, Fax: 740-597-2778, E-mail: Grijalva@ohiou.edu. Luis Escalante, H. Marcelo Aguilar, and Jose Racines, Instituto Nacional de Higiene Zona Norte, Iquique 2045 y Yaguachi, Quito, Ecuador. Rodrigo A. Paredes, Alberto Padilla, Escuela de Biologia, Universidad Católica del Ecuador, Ave. 12 de Octubre y Roca, Quito, Ecuador.

Acknowledgments: We thank the Servicio Nacional para el Control de Malaria and the Ecuadorian Army for logistical support, and Dr. Richard Seed and Carla Black (Department of Epidemiology, School of Public Health, University of North Carolina, Chapel Hill, NC) for assistance in the preparation of the manuscript.

Financial support: This research project was supported by TDR/World Health organization grants 970285 and A000209 and by Ohio University.

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