Exclusion of Horizontal and Vertical Transmission as Major Sources of Trypanosoma Cruzi Infections in a Breeding Colony of Rhesus Macaques (Macaca Mulatta)

Abstract

The vector-borne protozoal parasite Trypanosoma cruzi causes Chagas disease in humans and animals. This parasite is endemic to the southern United States where outdoor-housed NHP at biomedical facilities are at risk of infection. In addi- tion to the direct morbidity caused by T. cruzi, infected animals are of limited biomedical research use because infections can produce confounding pathophysiologic changes even in animals with no clinical disease. In part due to concerns for direct T. cruzi transmission between animals, infected NHP at some institutions have been culled, removed, or otherwise isolated from uninfected animal populations. However, data that document horizontal or vertical transmission in captive NHP in the United States are not available. To evaluate the potential for inter-animal transmission and to identify environmental factors that affect the distribution of new infections in NHPs, we conducted a retrospective epidemiologic study of a rhesus macaque ( Macaca mulatta ) breeding colony in south Texas. We used archived biologic samples and husbandry records to identify the time and location of macaque seroconversion. These data were used to perform a spatial analysis of how geographic location and animal associations affected the spread of disease and to infer the importance of horizontal or vertical routes of transmission. The majority of T. cruzi infections were spatially clustered, suggesting that environmental factors promoted vector exposure in various areas of the facility. Although we cannot not rule out horizontal transmission, our data suggest that horizontal transmission was not a critical route for spread for the disease. Vertical transmission was not a contributing factor in this colony. In conclusion, our findings suggest that local triatome vectors were the major source of T. cruzi infections in captive macaques in our colony. Therefore, limiting contact with vectors, rather than segregation of infected macaques, is a key strategy for disease prevention at institutions that house macaques outdoors in the southern United States.

Figure 1.

Satellite image (2018) of a portion of the facility, illustrating the 2 rhesus macaque colony compounds, with animal building numbers labeled in red. The main rhesus compound (lower image) contains Buildings 1 through 8, the 8 corncrib structures (collectively referred to as ‘Building 9’), a veterinary clinic, an administrative office, and a laundry–locker facility. The north rhesus compound (upper image) contains Buildings 10 and 11. Yellow circles denote the center of each corncrib structure and the individual rooms in each animal building. Red stars indicate the locations of 4 elevated storage sheds north of Buildings 1 and 2. The summer storage site for the fiberglass winterizing panels between 2011 and 2018 is denoted by the green box directly west of Building 1. The previous location of a planter box of interest is denoted by the blue box in the northeast corner of the main rhesus compound. The fenced boundary of each compound is denoted with dashed orange lines. Photo credit: Map data © 2020 Google, Maxar Technologies.

Figure 2.

Flow diagram of criteria used for determining whether horizontal transmission remained a potential route of transmission for individual seropositive animals.

Figure 3.

Previously acquired PCR results and DTU typing determinations for seropositive animals.

Figure 4.

Spatial hot-spot analysis for T. cruzi seroconversion in the main rhesus compound. (A) Data obtained from analysis of animals that became infected during 1999 through 2010. (B) Data obtained from analysis of animals that became infected during 2012 through 2017. Each colored dot represents an individual room or corncrib structure. Red and orange dots represent animal housing sites with a significantly higher incidence of T. cruzi seroconversion than the colony in general. Blue and gray dots represent animal housing sites with a significantly lower incidence of T. cruzi seroconversion than the colony in general. Yellow dots represent animal housing with an incidence of T. cruzi considered similar to that of the colony overall. The yellow stars on the lower portion of each figure highlight the wooded area that underwent intensive fire mitigation efforts in 2011–2012. Photo credit: Map data © 2014 Google image edited to remove red cars in parking lots.

Figure 5.

Cumulative shed power values assigned to rooms in Buildings 1 and 2 in the main rhesus compound. The 4 black boxes at the top of the image represent the 4 sheds. The 2, 12-room buildings are represented in the bottom half of the illustration. The illustration provides the approximate size and location of each shed relative to the 2 animal buildings. The number located in each of the building rooms is the cumulative shed power value assigned to each room. The 5 rooms with the largest cumulative shed power values are highlighted in red.