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Low Prevalence of Chagas Parasite Infection in a Nonhuman Primate Colony in Louisiana
Authors:Patricia L Dorn  Megan E Daigle  Crescent L Combe  Ashley H Tate  Lori Stevens  Kathrine M Phillippi-Falkenstein
Affiliation:1Loyola University New Orleans, New Orleans and;2Tulane National Primate Research Center, Covington, Louisiana;3University of Vermont, Burlington, Vermont
Abstract:Chagas disease, an important cause of heart disease in Latin America, is caused by the parasite Trypanosoma cruzi, which typically is transmitted to humans by triatomine insects. Although autochthonous transmission of the Chagas parasite to humans is rare in the United States, triatomines are common, and more than 20 species of mammals are infected with the Chagas parasite in the southern United States. Chagas disease has also been detected in colonies of nonhuman primates (NHP) in Georgia and Texas, and heart abnormalities consistent with Chagas disease have occurred at our NHP center in Louisiana. To determine the level of T. cruzi infection, we serologically tested 2157 of the approximately 4200 NHP at the center; 34 of 2157 primates (1.6%) tested positive. Presence of the T. cruzi parasite was confirmed by hemoculture in 4 NHP and PCR of the cultured parasites. These results strongly suggest local transmission of T. cruzi, because most of the infected NHP were born and raised at this site. All 3 species of NHP tested yielded infected animals, with significantly higher infection prevalence in pig-tailed macaques, suggesting possible exploration of this species as a model organism. The local T. cruzi strain isolated during this study would enhance such investigations. The NHP at this center are bred for use in scientific research, and the effects of the Chagas parasite on infected primates could confuse the interpretation of other studies.Abbreviation: NHP, nonhuman primate; TNPRC, Tulane National Primate Research CenterMost nonhuman primates (NHP) used in research in the United States are now raised at 1 of 8 National Primate Research Centers or other institutions in the United States and are shipped as needed for studies, thereby avoiding the importation of pathogens from their native countries. However, knowledge about the infection status of these research animals within colonies in the United States is important with regard to colony health, the outcome of the scientific studies that use these NHP, and the safety of caregivers and laboratory workers.Infection with the hemoflagellate parasitic pathogen Trypanosoma cruzi, the causative agent of Chagas disease, has been reported sporadically in NHP colonies in the United States (33 Of the approximately 8 million people infected,26 20% to 30% will develop chronic disease; most of these persons will die of heart disease (70% to 85%), digestive disorders (15% to 30%), or neurologic disease (less than 5%). Most (80%) transmission occurs through insect vectors, specifically through contact of parasite-containing feces (which are deposited while the insect is taking a blood meal) with mammalian mucous membranes or through a break in the skin. In addition, approximately 1% to 12% of offspring of infected mothers will acquire the parasite by congenital transmission.7 Insect-vector-mediated autochthonous transmission to humans is rare in the United States, with only 7 documented cases.11,18 However, a robust sylvan cycle exists in the United States, including T. cruzi-infected triatomine insects and a variety of mammals.31,36

Table 1.

Reports of T. cruziinfection in nonhuman primates in the United States
SpeciesNo. of NHP infected/ no. testedState where infection identified (and likely acquired)Evidence (method of detection)Reference
Pileated gibbon (Hylobates pileatus)1/1LouisianaAmastigotes in myocardium at necropsy30
Rhesus macaque (Macaca mulatta)1/1Maryland (Texas or Georgia)Blood culture after inadvertently transferred to immunosuppressed NHP; recipient confirmed by blood smears, serology, and xenodiagnosis9
Rhesus macaque20/236 (8.5%)TexasIndex case: amastigotes observed at necropsy; 19 additional by serology17
Squirrel monkey (Saimiri sciureus)2/2LouisianaMicroscopy, hemoculture, and xenodiagnosis12
Yellow baboon (Papio cynocephalus)1/1TexasAmastigotes noted at necropsy13
Crested black macaque (Macaca nigra)1/1Oregon (Texas)Flagellates observed in spinal fluid; amastigotes in brain at necropsy; serology25
Lion-tailed macaque (Macaca silenus)7/11 (64%)GeorgiaHemoculture and PCR27
Ring-tailed lemur (Lemur catta)1/19 (5%)GeorgiaHemoculture and PCR27
Pig-tailed macaque (Macaca nemestrina)1/1Washington (Louisiana)Hemoculture, PCR, and serology29
Ring-tailed lemur (Lemur catta)21/41 (51%)GeorgiaHemoculture, PCR, and serology14
Black-eyed lemur (Eulemur macaco flavifrons)1/5 (20%)GeorgiaSerology14
Black and white ruffed lemur (Varecia variegata variegata)3/4 (75%)GeorgiaSerology14
Chimpanzee (Pan troglodytes)1TexasAmastigotes on necropsy, PCR, and immunohistochemistry5
Open in a separate windowT. cruzi was first identified in the United States in 1916 in the triatomine insect vector Triatoma protracta.19 Eleven species of triatomine insects live in the southern two-thirds of the United States, where they are commonly known as ‘kissing bugs’ (because as night feeders, they often feed on the face) or ‘cone-nosed bugs.’ T. sanguisuga is the species reported most commonly in Louisiana.10 On average, the prevalence of infection in the insect vectors is 25%,36 although much higher prevalence is reported in some areas, including Louisiana (56%).10T. cruzi has been identified in more than 20 mammalian species across the southern United States; the most important of these mammals are rodents, raccoons, opossums, and armadillos.6,16 Recent studies showed that the highest prevalence of antibodies against T. cruzi occurred in raccoons (0% to 68%, range depends on state) and opossums (17% to 52%).6The first case of T. cruzi in a NHP in the United States occurred at the Delta Regional Primate Research Center (Covington, LA; now called the Tulane National Primate Research Center [TNPRC]), where a gibbon (Hylobates pileatus) from Malaysia died of symptoms of Chagas disease30. This case suggested local transmission because Chagas is endemic only to the Americas (
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