White-tailed deer (Odocoileus virginianus) are a major reservoir of a diversity of Toxoplasma gondii strains in the USA and pose a risk to consumers of venison

Authors: Dubey, Jitender; CERQUEIRA-CÉZAR, C - US Department Of Agriculture (USDA); Murata, Anthony; VERMA, S - US Department Of Agriculture (USDA); Kwok, Oliver; PEDERSEN, K - Animal And Plant Health Inspection Service (APHIS); Rosenthal, Benjamin; SU, C - University Of Tennessee

Submitted to: Parasitology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/1/2020
Publication Date: 3/17/2020
Citation: Dubey, J.P., Cerqueira-Cézar, C.K., Murata, A.A., Verma, S.K., Kwok, O.C., Pedersen, K., Rosenthal, B.M., Su, C. 2020. White-tailed deer (Odocoileus virginianus) are a major reservoir of a diversity of Toxoplasma gondii strains in the USA and pose a risk to consumers of venison. Parasitology. 147(7):1-19. https://doi.org/10.1017/S0031182020000451.
DOI: https://doi.org/10.1017/S0031182020000451

Interpretive Summary: Among these zoonotic pathogens, the protozoan parasite T. gondii is perhaps the most ubiquitous, having been identified in the tissues of a variety of animal hosts, including both mammalian and avian species. Toxoplasma gondii is estimated to chronically infect one third of the world’s human population, causing ocular toxoplasmosis in immunocompetent individuals and often-fatal encephalitis in the immunocompromised, as well as birth defects and mortality following vertical transmission to developing fetuses. Humans become infected postnatally by eating undercooked meat infected with T. gondii tissue cysts or by ingesting oocysts from the environment. Cats (domestic and wild) are the main reservoir of infection because they are the only hosts that can excrete the environmentally resistant stage, the oocyst. Oocysts are highly infectious for people and animals. The presence of T. gondii in white-tailed deer is considered a good indicator of contamination in the environment because they are herbivores, and become infected both by ingesting oocysts while grazing. In the present study, antibodies to T. gondii were found in 36 % of 914 deer across the USA and viable T. gondii was isolated from tissues of 36. Genetic typing of T. gondii isolates revealed moderate genetic diversity. The results will be of interest to biologists, parasitologists, public health workers, and hunters.

Technical Abstract: To assess the role of white-tailed deer (WTD) in the epidemiology of toxoplasmosis, we conducted a national survey of WTD across the USA for Toxoplasma gondii infection. To do this, we paired serological samples with parasite isolation to evaluate the prevalence and genetic diversity of these parasites. From October 2012-March 2019, serum and tissues were collected from 914 WTD across the USA. Serum samples were initially screened for antibodies to T. gondii, and then the tissues of seropositive WTD were bioassayed in mice. Antibodies were detected in 36 % of WTD tested by the modified agglutination test (MAT, 1:25 or higher). Adults (42.1% of 668) were more likely to be antibody positive than juveniles (19.2% of 239). Viable T. gondii was isolated from the heart of 36 WTD from 11 states. Three of the 36 isolates were pathogenic but not highly virulent to outbred Swiss Webster mice and 36 isolates could be propagated further in cell culture and were genotyped. For genotyping, DNA extracted from cell culture-derived tachyzoites was characterized by PCR restriction fragment length polymorphism (PCR-RFLP) using the genetic markers SAG1, SAG2, SAG3, BTUB, GRA6, c22-8, c29-2, L358, PK1 and Apico. Genotyping revealed 7 ToxoDB PCR-RFLP genotypes, including 24 isolates for genotype #5 (haplogroup 12), 4 isolates for #2 (type III, haplogroup 3), 3 isolates for genotypes #1 (type II, haplogroup 2), 2 isolates for genotypes #3 (type II, haplogroup 2), 1 isolate each for #39, #221, and #224. Genotype #5 was the most frequently isolated, accounting for 66.6% (24 of 35) of the isolates. Combining the 36 isolates from this study with previously reported 69 isolates from WTD, 15 genotypes are identified. Among these, 50.4% (53/105) isolates belongs to genotype #5. Taken together, dominance of genotype #5 is a signature of sylvatic transmission of T. gondii in wildlife in the mainland United States. Our results indicate moderate genetic diversity of T. gondii in WTD, with genotype #5 (haplogroup 12), the most common type in sylvatic transmission cycle, dominates across the continental USA.