• View in gallery
    Figure 1.

    Location of the three rural communities in the northeastern Peruvian Amazon from where samples were collected: Nueva Esperanza (04°19′53″ S; 71°57′33″ W) in the Yavari-Mirin basin, Sol Naciente (03°38′26″ S, 73°12′57″ W) near the Amazon river, and Diamante/7 de Julio (04°36′43″ S, 72°46′12″ W) in the Tamshiyacu–Tahuayo Regional Conservation Area.

  • View in gallery
    Figure 2.

    Identification of trypanosomatids and Trypanosoma cruzi by nested polymerase chain reaction in 14 wild mammals only for illustration purposes. (A) PCR for the identification of trypanosomatids (225–265 bp). Lane 1: negative control (water). Lane 2: positive control #1 (Trypanosoma cruzi, Y strain – 265 bp). Lane 3: positive control #2 (Trypanosoma cruzi, Tulahuen strain – 250 bp). Lane 4: + control (Leishmania (V.) braziliensis – 225 bp). Lane 5, 7–16, 18: positive samples (double bands in lanes 7 and 14 may depict multiple infections with trypanosomatids). Lane 6, 17: negative samples. (B) Nested-PCR for the identification of Trypanosoma cruzi (110–125 bp). Lane 1: negative control (water). Lane 2: positive control #1 (Trypanosoma cruzi, Y strain – 125 bp). Lane 3: positive control #2 (Trypanosoma cruzi, Tulahuen strain – 110 bp). Lane 4: negative control (Leishmania (V.) braziliensis). Lane 7, 9, 10: positive samples. Lane 5, 6, 8, 11–18: negative samples.

  • 1.

    Pan American Health Organization (PAHO), 2012. Enfermedad de Chagas (Trypanosomiasis Americana). Available at: http://www.paho.org/hq/index.php?option=com_topics&view=article&id=10&Itemid=40743. Accessed January 8, 2017.

  • 2.

    Coura JR, Junqueira AC, 2012. Risks of endemicity, morbidity and perspectives regarding the control of Chagas disease in the Amazon region. Mem Inst Oswaldo Cruz 107: 145154.

    • Search Google Scholar
    • Export Citation
  • 3.

    Coura JR, 2013. Chagas disease: control, elimination and eradication. Is it possible? Mem Inst Oswaldo Cruz 108: 962967.

  • 4.

    Naquira C, Cabrera R, 2009. Short review of Chagas disease history after a century of its discovery and the current situation in Peru. Rev Peru Med Exp Salud Publica 26: 494504.

    • Search Google Scholar
    • Export Citation
  • 5.

    Carlos N, Solis HM, 2015. Wild reservoirs of Trypanosoma cruzi in four locations of Amazon and Loreto regions. Theorema. 2: 6373.

  • 6.

    Shikanai-Yasuda MA, Carvalho NB, 2012. Oral transmission of Chagas disease. Clin Infect Dis 54: 845852.

  • 7.

    Alarcon B, Diaz-Bello Z, Colmenares C, Ruiz-Guevara R, Mauriello L, Muñoz-Calderon A, Noya O, 2015. Update on oral Chagas disease outbreaks in Venezuela: epidemiological, clinical and diagnostic approaches. Mem Inst Oswaldo Cruz 110: 377386.

    • Search Google Scholar
    • Export Citation
  • 8.

    Toso MA, Vial UF, Galanti N, 2011. Oral transmission of Chagas’ disease. Rev Med Chil 139: 258266.

  • 9.

    Pan American Health Organization (PAHO), 2009. Guide for Surveillance, Prevention, Control and Clinical Management of Acute Chagas Disease Transmitted by Food. Rio de Janeiro, Brazil: PANAFTOSA-VP/OPAS/OMS, 92.

  • 10.

    Souto RP, Vargas N, Zingales B, 1999. Trypanosoma rangeli: discrimination from Trypanosoma cruzi based on a variable domain from the large subunit ribosomal RNA gene. Exp Parasitol 91: 306314.

    • Search Google Scholar
    • Export Citation
  • 11.

    Alves FM, Olifiers N, de Cassia Bianchi R, Duarte AC, Cotias PMT, D’Andrea PS, Gomper ME, Mourao GM, Herrera HM, Jansen AM, 2010. Modulating variables of Trypanosoma cruzi and Trypanosoma evansi transmission in free-ranging Coati (Nasua nasua) from the Brazilian Pantanal region. Vector Borne Zoonotic Dis 11: 835841.

    • Search Google Scholar
    • Export Citation
  • 12.

    Herrera HM, Lisboa CV, Pinho AP, Olifiers N, Bianchi RC, Rocha FL, Mourao GM, Jansen AM, 2008. The coati (Nasua nasua, Carnivora, Procyonidae) as a reservoir host for the main lineages of Trypanosoma cruzi in the Pantanal region, Brazil. Trans R Soc Trop Med Hyg 102: 11331139.

    • Search Google Scholar
    • Export Citation
  • 13.

    Raccurt CP, 1996. Trypanosoma cruzi in French Guinea: review of accumulated data since 1940. Med Trop (Mars) 56: 7987.

  • 14.

    Tenorio MS, Oliveira e Sousa L, Alves-Martin MF, Paixão MS, Rodrigues MV, Starke-Buzetti WA, Araújo JP Jr, Lucheis SB, 2014. Molecular identification of trypanosomatids in wild animals. Vet Parasitol 203: 203206.

    • Search Google Scholar
    • Export Citation
  • 15.

    Xavier SC, Roque AL, Lima Vdos S, Monteiro KJ, Otaviano JC, Ferreira da Silva LF, Jansen AM, 2012. Lower richness of small wild mammal species and chagas disease risk. PLoS Negl Trop Dis 6: e1647.

    • Search Google Scholar
    • Export Citation
  • 16.

    Herrera L, Xavier SCC, Viegas C, Martinez C, Cotias PM, Carrasco H, Urdaneta-Morales S, Jansen AM, 2004. Trypanosoma cruzi in a caviomorph rodent: parasitological and pathological features of the experimental infection of Trichomys apereoides (Rodentia, Echimyidae). Exp Parasitol 107: 7888.

    • Search Google Scholar
    • Export Citation
  • 17.

    de Lima H, Carrero J, Rodríguez A, de Guglielmo Z, Rodriguez N, 2006. Trypanosomatidae of public health importance occurring in wild and synanthropic animals of rural Venezuela. Biomedica 26: 4250.

    • Search Google Scholar
    • Export Citation
  • 18.

    Roque ALR, Xavier SCC, Gerhardt M, Silva MFO, Lima V, D’Andrea PS, Jansen AM, 2012. Trypanosoma cruzi among wild and domestic mammals in different areas of the Abaetetuba municipality (Pará State, Brazil), an endemic Chagas disease transmission area. Vet Parasitol 193: 7177.

    • Search Google Scholar
    • Export Citation
  • 19.

    Bodmer RE, Lozano EP, 2001. Rural development and sustainable wildlife use in Peru. Conserv Biol 15: 11631170.

  • 20.

    Ministerio de Salud del Peru (MINSA) – Dirección General de Epidemiologia, 2015. Sala Situacional Para el Análisis de Situación de Salud. Lima, Peru: MINSA. Available at: http://www.dge.gob.pe/portal/index.php?option=com_content&view=article&id=14&Itemid=121. Accessed January 8, 2017.

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Prevalence of Trypanosoma cruzi and Other Trypanosomatids in Frequently-Hunted Wild Mammals from the Peruvian Amazon

E. Angelo MoralesUniversidad Nacional Mayor de San Marcos, Lima, Peru;

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Pedro MayorUniversitat Autònoma de Barcelona, Barcelona, Spain;
Programa de Pós-Graduação em Saúde e Produção Animal na Amazônia, Universidade Federal Rural da Amazônia, Belém, Brazil;

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Mark BowlerSan Diego Zoo Global Institute for Conservation Research, Escondido, California;

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Esar AysanoaUniversidad Nacional Mayor de San Marcos, Lima, Peru;

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Erika S. Pérez-VelezUS Naval Medical Research Unit No. 6, Callao, Peru;

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Jocelyn PérezUniversity of Prince Edward Island, Charlottetown, Prince Edward Island, Canada;

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Julio A. VentocillaUS Naval Medical Research Unit No. 6, Callao, Peru;

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G. Christian BaldevianoUS Naval Medical Research Unit No. 6, Callao, Peru;

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Andrés G. LescanoUS Naval Medical Research Unit No. 6, Callao, Peru;
Emerge, Emerging Diseases and Climate Change Research Unit, Universidad Peruana Cayetano Heredia, Lima, Peru

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To better understand the ecology of Trypanosoma cruzi in the northeastern Peruvian Amazon, we evaluated the prevalence of T. cruzi and other trypanosomatids in four orders of wild mammals hunted and consumed by inhabitants of three remote indigenous communities in the Peruvian Amazon. Of 300 wild mammals sampled, 115 (38.3%) were infected with trypanosomatids and 15 (5.0%) with T. cruzi. The prevalence of T. cruzi within each species was as follows: large rodents (Cuniculus paca, 5.5%; Dasyprocta spp., 2.6%), edentates (Dasypus novemcinctus, 4.2%), and carnivores with higher prevalence (Nasua nasua, 18.8%). The high prevalence of T. cruzi and other trypanosomatids in frequently hunted wild mammals suggests a sizeable T. cruzi sylvatic reservoir in remote Amazonian locations.

Because of its high prevalence, and occurrence in 21 countries, Chagas disease is one of the most important, neglected tropical diseases in Latin America.1 It is estimated that between 6 and 8 million people are infected in Latin America, of whom 12,000 die of the disease each year.1 The Amazon Basin, inhabited by 30 million people, is the largest tropical biome in which both animal reservoirs and multiple species of triatomine vectors of Trypanosoma cruzi coexist, representing a major threat to human populations.2

About 33 species in six mammalian genera act as reservoirs for T. cruzi in the Amazon, including marsupials, bats, rodents, edentates, carnivores, and primates.3 However, the challenges of studying wildlife populations in remote areas have limited the identification of natural hosts of T. cruzi in the Peruvian Amazon, and only three are previously documented: Saimiri boliviensis, Saguinus nigricollis and Didelphis paraguayensis pernigra,4 whereas more are described from regions of the Brazilian Amazon.2,5

Chagas disease is mainly transmitted by contact with feces from infected triatomine insects.4 Oral transmission through food and beverages contaminated with such vector feces has also been documented and may be more important than previously considered, accounting for up to 70% of acute cases in the Brazilian Amazon.6 Oral transmission through the consumption of undercooked meat may also occur, but has not been conclusively confirmed.79 As hunting is one of the main subsistence activities in the Amazon Basin, local villagers might be at the risk of infection during excursions into the forest. This study evaluated the prevalence of T. cruzi and other trypanosomatids in blood samples from four taxonomic orders of wild mammals hunted and consumed by the inhabitants of rural communities in the Peruvian Amazon.

We studied a sample of 300 wild mammals from 13 species and four taxonomical orders that had been hunted for subsistence and household income by local villagers in three remote indigenous communities in the Peruvian Amazon from 2009 to 2011 (Table 1, Figure 1). No sampled animals were killed exclusively for this study. Blood samples were directly spotted onto Whatman paper during butchering by trained local villagers, preserved on silica gel desiccant, transported to the US Naval Medical Research Unit No. 6 in Lima, and stored at −80°C. The research protocol was approved by the Dirección General de Flora y Fauna Silvestre (0350-2012-AG-DGFFS-DGEFFS) of Peru.

Table 1

Prevalence of Trypanosoma cruzi and trypanosomatids in four orders and 13 animal species from three rural communities of the Peruvian Amazon, 2009–2011

OrderSpeciesNTrypanosomatids*Trypanosoma cruzi
Positives*%95% CIPositives%95% CI
RodentiaCuniculus paca1287558.649.6–67.275.52.2–10.9
Dasyprocta spp.38410.52.9–24.812.60.00–13.8
Sciurus igniventris100.00.0–97.500.00.0–97.5
Subtotal1677947.339.5–55.284.82.1–9.2
ArtiodactylaTapirus terrestris9555.621.2–86.300.00.0–33.6
Tayassu pecari4250.06.8–93.200.00.0–60.2
Mazama americana15640.016.3–67.700.00.0–21.8
Tayassu tajacu441022.711.5–37.800.00.0–8.0
Mazama gouazoubira200.00.0–84.200.00.0–84.2
Subtotal742331.120.8–42.900.00.0–4.9
CarnivoraNasua nasua32928.113.7–46.7618.87.2–36.4
Puma concolor100.00.0–97.500.00.0–97.5
Leopardus pardalis100.00.0–97.500.00.0–97.5
Subtotal34926.512.9–44.4617.66.8–34.5
Edentata (Xenarthra)Dasypus novemcinctus24416.74.7–37.414.20.1–21.1
Priodontes maximus100.00.0–97.500.00.0–97.5
Subtotal25416.04.5–36.114.00.1–20.4
Total30011538.332.8–44.1155.02.8–8.1

There were statistically significant differences between the four orders studied in the prevalence of T. cruzi (P = 0.003) and trypanosomatids (P = 0.002).

Trypanosomatids including T. cruzi.

95% confidence interval was computed using the binomial test.

Figure 1.
Figure 1.

Location of the three rural communities in the northeastern Peruvian Amazon from where samples were collected: Nueva Esperanza (04°19′53″ S; 71°57′33″ W) in the Yavari-Mirin basin, Sol Naciente (03°38′26″ S, 73°12′57″ W) near the Amazon river, and Diamante/7 de Julio (04°36′43″ S, 72°46′12″ W) in the Tamshiyacu–Tahuayo Regional Conservation Area.

Citation: The American Journal of Tropical Medicine and Hygiene 97, 5; 10.4269/ajtmh.17-0028

We isolated DNA from samples using the QIAamp DNA mini kit (QIAGEN, Valencia, CA). DNA concentrations were quantified using the NanoDrop-1000 spectrophotometer (Thermo Scientific, Somerset, NJ). We conducted a polymerase chain reaction (PCR) (Applied Biosystems) targeting the 24S alpha subunit rRNA gene of trypanosomatids overall using primers D75 and D76. Subsequently, a nested-PCR targeted an internal T. cruzi–specific region of the same gene using primers D71 and D72.10 Ultrapure water, Leishmania (V.) brasiliensis and T. cruzi (Y and Tulahuen strains) were used as controls (Figure 2). Between 2009 and 2011, hunting records of eight out of 60 families from Nueva Esperanza were used to estimate the annual number of species hunted and consumed by local inhabitants and assess the potential consumption of T. cruzi–infected mammals in these communities. The prevalence of T. cruzi and trypanosomatids between orders and communities were compared using χ2 test and Fisher’s exact test according to the sample size. Confidence intervals of 95% were also estimated accordingly using RStudio version 0.98.1091 (The R Foundation for Statistical Computing, Vienna, Austria).

Figure 2.
Figure 2.

Identification of trypanosomatids and Trypanosoma cruzi by nested polymerase chain reaction in 14 wild mammals only for illustration purposes. (A) PCR for the identification of trypanosomatids (225–265 bp). Lane 1: negative control (water). Lane 2: positive control #1 (Trypanosoma cruzi, Y strain – 265 bp). Lane 3: positive control #2 (Trypanosoma cruzi, Tulahuen strain – 250 bp). Lane 4: + control (Leishmania (V.) braziliensis – 225 bp). Lane 5, 7–16, 18: positive samples (double bands in lanes 7 and 14 may depict multiple infections with trypanosomatids). Lane 6, 17: negative samples. (B) Nested-PCR for the identification of Trypanosoma cruzi (110–125 bp). Lane 1: negative control (water). Lane 2: positive control #1 (Trypanosoma cruzi, Y strain – 125 bp). Lane 3: positive control #2 (Trypanosoma cruzi, Tulahuen strain – 110 bp). Lane 4: negative control (Leishmania (V.) braziliensis). Lane 7, 9, 10: positive samples. Lane 5, 6, 8, 11–18: negative samples.

Citation: The American Journal of Tropical Medicine and Hygiene 97, 5; 10.4269/ajtmh.17-0028

Of 300 sampled mammals, 115 (38.3%; 95% CI = 32.8–44.1) were infected with trypanosomatids and 15 (5.0%; 95% CI = 2.8–8.1) of the latter with T. cruzi (Table 1). Trypanosomatids were identified at all sampling sites with different prevalence (P = 0.013): Nueva Esperanza (41.1%, 109/265), Diamante/7 de Julio (27.3%; 3/11), and Sol Naciente (12.5%; 3/24), whereas all T. cruzi–positive samples came exclusively from Nueva Esperanza (5.7%; 15/265).

The order Rodentia showed the highest prevalence of trypanosomatids (79/167; 47.3%), followed by Artiodactyla (23/74; 31.1%), Carnivora (9/34; 26.5%), and Edentata (4/25; 16.0%). Trypanosoma cruzi was found in all taxonomic orders except Artiodactyla, with the rodent Cuniculus paca (7/128; 5.5%) and the carnivore Nasua nasua (6/32; 18.8%) accounting for 46.7% and 40.0% of cases, respectively. The small number of C. paca (N = 11) and N. nasua (N = 1) sampled in Diamante/7 de Julio and Sol Naciente may explain the absence of T. cruzi in these communities.

Eight families from Nueva Esperanza reported hunting 739 animals over 3 years. We estimated a yearly harvest of 31 animals per family, and 1,847 animals for the whole community of approximately 307 inhabitants in 60 families. Considering only species that were T. cruzi–positive in our study, we estimated that 45 infected animals might be consumed annually in the community: C. paca (N = 24), N. nasua (N = 17), Dasypus novemcinctus (N = 2), and Dasyprocta spp. (N = 2).

Trypanosoma cruzi was found in all sampled orders (Rodentia, Carnivora, and Edentata), except Artiodactyla, and in four of seven species with five or more specimens tested, suggesting a high prevalence of T. cruzi in frequently hunted mammals. Coatis (N. nasua) showed the highest prevalence of T. cruzi, confirming the important role of this carnivore in the sylvatic cycle of Chagas disease in the Peruvian Amazon and consistent with evidence from Brazil.11,12 It has been proposed that coatis may become infected through oral transmission rather than vectorial transmission by ingesting contaminated triatomines and feeding on small mammals.12 We also found T. cruzi (4.2%) in armadillos (Dasypus novemcinctus), which are well-known reservoirs of T. cruzi in both peridomestic and sylvatic cycles.13 Finally, we found T. cruzi naturally infecting large rodents (C. paca, 5.5%, and Dasyprocta spp., 2.6%), which is also consistent with the findings in the Brazilian Amazon.14,15 Although epidemiological studies on large rodents are limited, they are considered ancient hosts of T. cruzi, and may be effective reservoirs.16 The large rodents C. paca and Dasyprocta spp. are unlikely to be predated by coatis, but are predated by larger carnivores (e.g., felines), which in turn could possibly become infected. The peccaries Tayassu tajacu and Tajassu pecari have also been suggested as reservoirs of T. cruzi in a previous study,12 however, we found no peccary infected. Our study in remote and isolated communities shows a 5.0% prevalence of T. cruzi in four species of large rodents, carnivores, and edentates. Although the high natural prevalence of T. cruzi infections in frequently hunted wild mammals might suggest a large T. cruzi sylvatic reservoir in the Peruvian Amazon, we cannot rule out the possibility that the disease could make these mammals more vulnerable to be hunted, and thus the reported prevalence might be overestimating the true prevalence in the Amazon.

The high prevalence of trypanosomatids (38.3%) found in all sampled mammalian orders suggests that several parasites of this family in remote Amazonian regions may be widely distributed across different mammalian groups rather than being confined to specific hosts. We cannot exclude that preinfection with other trypanosomatids might increase the susceptibility to T. cruzi infection in these mammals as previously suggested for Trypanosoma lewisi and Leishmania chagasi.17

Dogs may also play an important role in the peridomestic cycle of Chagas disease as potential reservoirs and may be accurate sentinels for identifying areas of active T. cruzi transmission.6,18 Although we did not sample domestic dogs in this study, they may help to establish a link between the peridomestic and sylvatic cycles of T. cruzi in rural communities as dogs usually accompany hunters on foot during excursions into the forest and can be vectorially infected. In addition, dogs in these communities are often fed raw viscera and oral transmission cannot be ruled out.

Evidence of oral transmission of T. cruzi through consumption of undercooked meat is currently inconclusive, but its occurrence in the Amazon basin is suspected,8 and to our knowledge, no study has rejected this hypothesis. The consumption of bushmeat in our sampled communities was typical of bushmeat consumption across Amazon rural communities, in which wild meat represents an important animal protein source. An estimated 113,000 wild animals are hunted annually in the department of Loreto.19 We estimated that the study community annually hunts and eats 45 animals infected with T. cruzi, translating to 0.75 infected animals typically consumed by a large extended family per year, not accounting for sharing of meat between families, suggesting recurring opportunities of infection.18 Further studies addressing a relationship between wild meat consumption and Chagas disease are required to better understand the risk of infection in Amazonian communities.

In Peru, 830 human cases of T. cruzi were reported from 2004 to 2015,20 most of them (81.3%) in the Peruvian southern highlands, in the department of Arequipa. Only 23 cases were documented in Loreto, Peruvian Amazon’s largest department in urban and rural population, which probably greatly underestimates the burden of T. cruzi infection, because of the absence of routine diagnosis and limited access to healthcare in remote indigenous communities.

Acknowledgments:

We thank the residents of Nueva Esperanza (Yavari-Mirín River), Sol Naciente (Amazon River), and Diamante/7 de Julio (Tamshiyacu–Tahuayo Community Reserve) who actively participated in sample collection.

REFERENCES

  • 1.

    Pan American Health Organization (PAHO), 2012. Enfermedad de Chagas (Trypanosomiasis Americana). Available at: http://www.paho.org/hq/index.php?option=com_topics&view=article&id=10&Itemid=40743. Accessed January 8, 2017.

  • 2.

    Coura JR, Junqueira AC, 2012. Risks of endemicity, morbidity and perspectives regarding the control of Chagas disease in the Amazon region. Mem Inst Oswaldo Cruz 107: 145154.

    • Search Google Scholar
    • Export Citation
  • 3.

    Coura JR, 2013. Chagas disease: control, elimination and eradication. Is it possible? Mem Inst Oswaldo Cruz 108: 962967.

  • 4.

    Naquira C, Cabrera R, 2009. Short review of Chagas disease history after a century of its discovery and the current situation in Peru. Rev Peru Med Exp Salud Publica 26: 494504.

    • Search Google Scholar
    • Export Citation
  • 5.

    Carlos N, Solis HM, 2015. Wild reservoirs of Trypanosoma cruzi in four locations of Amazon and Loreto regions. Theorema. 2: 6373.

  • 6.

    Shikanai-Yasuda MA, Carvalho NB, 2012. Oral transmission of Chagas disease. Clin Infect Dis 54: 845852.

  • 7.

    Alarcon B, Diaz-Bello Z, Colmenares C, Ruiz-Guevara R, Mauriello L, Muñoz-Calderon A, Noya O, 2015. Update on oral Chagas disease outbreaks in Venezuela: epidemiological, clinical and diagnostic approaches. Mem Inst Oswaldo Cruz 110: 377386.

    • Search Google Scholar
    • Export Citation
  • 8.

    Toso MA, Vial UF, Galanti N, 2011. Oral transmission of Chagas’ disease. Rev Med Chil 139: 258266.

  • 9.

    Pan American Health Organization (PAHO), 2009. Guide for Surveillance, Prevention, Control and Clinical Management of Acute Chagas Disease Transmitted by Food. Rio de Janeiro, Brazil: PANAFTOSA-VP/OPAS/OMS, 92.

  • 10.

    Souto RP, Vargas N, Zingales B, 1999. Trypanosoma rangeli: discrimination from Trypanosoma cruzi based on a variable domain from the large subunit ribosomal RNA gene. Exp Parasitol 91: 306314.

    • Search Google Scholar
    • Export Citation
  • 11.

    Alves FM, Olifiers N, de Cassia Bianchi R, Duarte AC, Cotias PMT, D’Andrea PS, Gomper ME, Mourao GM, Herrera HM, Jansen AM, 2010. Modulating variables of Trypanosoma cruzi and Trypanosoma evansi transmission in free-ranging Coati (Nasua nasua) from the Brazilian Pantanal region. Vector Borne Zoonotic Dis 11: 835841.

    • Search Google Scholar
    • Export Citation
  • 12.

    Herrera HM, Lisboa CV, Pinho AP, Olifiers N, Bianchi RC, Rocha FL, Mourao GM, Jansen AM, 2008. The coati (Nasua nasua, Carnivora, Procyonidae) as a reservoir host for the main lineages of Trypanosoma cruzi in the Pantanal region, Brazil. Trans R Soc Trop Med Hyg 102: 11331139.

    • Search Google Scholar
    • Export Citation
  • 13.

    Raccurt CP, 1996. Trypanosoma cruzi in French Guinea: review of accumulated data since 1940. Med Trop (Mars) 56: 7987.

  • 14.

    Tenorio MS, Oliveira e Sousa L, Alves-Martin MF, Paixão MS, Rodrigues MV, Starke-Buzetti WA, Araújo JP Jr, Lucheis SB, 2014. Molecular identification of trypanosomatids in wild animals. Vet Parasitol 203: 203206.

    • Search Google Scholar
    • Export Citation
  • 15.

    Xavier SC, Roque AL, Lima Vdos S, Monteiro KJ, Otaviano JC, Ferreira da Silva LF, Jansen AM, 2012. Lower richness of small wild mammal species and chagas disease risk. PLoS Negl Trop Dis 6: e1647.

    • Search Google Scholar
    • Export Citation
  • 16.

    Herrera L, Xavier SCC, Viegas C, Martinez C, Cotias PM, Carrasco H, Urdaneta-Morales S, Jansen AM, 2004. Trypanosoma cruzi in a caviomorph rodent: parasitological and pathological features of the experimental infection of Trichomys apereoides (Rodentia, Echimyidae). Exp Parasitol 107: 7888.

    • Search Google Scholar
    • Export Citation
  • 17.

    de Lima H, Carrero J, Rodríguez A, de Guglielmo Z, Rodriguez N, 2006. Trypanosomatidae of public health importance occurring in wild and synanthropic animals of rural Venezuela. Biomedica 26: 4250.

    • Search Google Scholar
    • Export Citation
  • 18.

    Roque ALR, Xavier SCC, Gerhardt M, Silva MFO, Lima V, D’Andrea PS, Jansen AM, 2012. Trypanosoma cruzi among wild and domestic mammals in different areas of the Abaetetuba municipality (Pará State, Brazil), an endemic Chagas disease transmission area. Vet Parasitol 193: 7177.

    • Search Google Scholar
    • Export Citation
  • 19.

    Bodmer RE, Lozano EP, 2001. Rural development and sustainable wildlife use in Peru. Conserv Biol 15: 11631170.

  • 20.

    Ministerio de Salud del Peru (MINSA) – Dirección General de Epidemiologia, 2015. Sala Situacional Para el Análisis de Situación de Salud. Lima, Peru: MINSA. Available at: http://www.dge.gob.pe/portal/index.php?option=com_content&view=article&id=14&Itemid=121. Accessed January 8, 2017.

Author Notes

Address correspondence to Andrés G. Lescano, Emerge, Emerging Diseases and Climate Change Research Unit, School of Public Health and Administration, Universidad Peruana Cayetano Heredia, Av. Honorio Delgado 430. San Martin de Porres Lima 31, Peru. E-mail: andres.lescano.g@upch.pe

Financial support: This work was been supported by LA Zoo, and the training grant 2D43 TW007393 awarded to AGL by the Fogarty International Center of the U.S. National Institutes of Health; and the Earthwatch Institute. The sponsors had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Copyright statement: Some authors of this manuscript are employees of the U.S. Government. This work was prepared as part of their duties. Title 17 U.S.C. § 105 provides that “Copyright protection under this title is not available for any work of the United States Government.” Title 17 U.S.C. § 101 defines a U.S. Government work as a work prepared by an employee of the U.S. Government as part of that person’s official duties.

Authors’ addresses: E. Angelo Morales and Esar Aysanoa, Universidad Nacional Mayor de San Marcos, Department of Microbiology and Parasitology, Lima, Peru, E-mails: eangelo.morales@gmail.com and eaysanoa@yahoo.com. Pedro Mayor, Universitat Autonoma de Barcelona, Animal Health and Anatomy, Bellaterra, Catalunya, Spain, E-mail: mayorpedro@hotmail.com. Mark Bowler, Zoological Society of San Diego, Institute for Conservation Research, San Diego, CA, E-mail: mark@markbowler.com. Erika S. Pérez-Velez, Naval Medical Research Unit No. 6, Department of Parasitology, Bellavista, Callao, Peru, and Universidad Nacional Mayor de San Marcos, Facultad de Ciencias Biologicas, Lima, Peru, E-mail: erikasofiaperez@gmail.com. Jocelyn Pérez, University of Prince Edward Island, Pathology and Microbiology, Charlottetown, Prince Edward Island, Canada, E-mail: jocelynginette@gmail.com. Julio A. Ventocilla, Naval Medical Research Unit No. 6, Department of Parasitology, Bellavista, Callao, Peru, E-mail: julio.a.ventocilla.fn@mail.mil. G. Christian Baldeviano, United States Naval Medical Research Unit – Six (NAMRU-6), Parasitology, Lima, Callao, Peru, E-mail: geralc.baldeviano.fn@mail.mil. Andrés G. Lescano, Universidad Peruana Cayetano Heredia, School of Public Health and Management, Urb. Ingenieria, San Martin de Porres, Lima, Peru, E-mail: andres.lescano.g@upch.pe.

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