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

Published online by Cambridge University Press:  17 March 2020

J. P. Dubey Open the ORCID record for J. P. Dubey [Opens in a new window] ,
C. K. Cerqueira-Cézar ,
F. H. A. Murata ,
S. K. Verma ,
O. C. H. Kwok ,
K. Pedersen ,
B. M. Rosenthal  and
C. Su
J. P. Dubey*
Affiliation:
United States Department of Agriculture, Agricultural Research Service, Animal Parasitic Diseases Laboratory, Beltsville Agricultural Research Center, Building 1001, Beltsville, MD20705-2350, USA
C. K. Cerqueira-Cézar
Affiliation:
United States Department of Agriculture, Agricultural Research Service, Animal Parasitic Diseases Laboratory, Beltsville Agricultural Research Center, Building 1001, Beltsville, MD20705-2350, USA
F. H. A. Murata
Affiliation:
United States Department of Agriculture, Agricultural Research Service, Animal Parasitic Diseases Laboratory, Beltsville Agricultural Research Center, Building 1001, Beltsville, MD20705-2350, USA
S. K. Verma
Affiliation:
United States Department of Agriculture, Agricultural Research Service, Animal Parasitic Diseases Laboratory, Beltsville Agricultural Research Center, Building 1001, Beltsville, MD20705-2350, USA
O. C. H. Kwok
Affiliation:
United States Department of Agriculture, Agricultural Research Service, Animal Parasitic Diseases Laboratory, Beltsville Agricultural Research Center, Building 1001, Beltsville, MD20705-2350, USA
K. Pedersen
Affiliation:
United States Department of Agriculture, Animal and Plant Health Inspection Service, Wildlife Services, 920 Main Campus Drive, Suite 200 Raleigh, NC, 27606, USA
B. M. Rosenthal
Affiliation:
United States Department of Agriculture, Agricultural Research Service, Animal Parasitic Diseases Laboratory, Beltsville Agricultural Research Center, Building 1001, Beltsville, MD20705-2350, USA
C. Su
Affiliation:
Department of Microbiology, University of Tennessee, Knoxville, TN37996-0845, USA
*
Author for correspondence: J. P. Dubey, E-mail: Jitender.dubey@ars.usda.gov
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Abstract

To assess the role of white-tailed deer (Odocoileus virginianus, WTD) in the epidemiology of toxoplasmosis, we conducted a national survey of WTD across the USA for Toxoplasma gondii infection. To do this, we combined serology with parasite isolation to evaluate the prevalence and genetic diversity of T. gondii in this game species. From October 2012 to March 2019, serum and tissues were collected from 914 WTD across the USA. Serum samples were screened for antibodies to T. gondii, and then the tissues of seropositive WTD were bioassayed in mice. Antibodies were detected in 329 (36%) of 914 WTD tested by the modified agglutination test (positive reaction at 1:25 or higher). 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 all 36 isolates could be propagated further in cell culture and were genotyped. For genotyping, DNA extracted from cell culture-derived tachyzoites was characterized by polymerase chain reaction-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 seven ToxoDB PCR-RFLP genotypes, including 24 isolates for genotype #5 (haplogroup 12), four isolates for #2 (type III, haplogroup 3), three isolates for genotypes #1 (type II, haplogroup 2), two isolates for genotypes #3 (type II, haplogroup 2) and one isolate each for #39, #221 and #224. Genotype #5 was the most frequently isolated, accounting for 66.6% (24 of 36) of the isolates. Combining the 36 isolates from this study with previously reported 69 isolates from WTD, 15 genotypes have been identified. Among these, 50.4% (53/105) isolates belong to genotype #5. Our results indicate moderate genetic diversity of T. gondii in WTD. The results also indicate that undercooked venison should not be consumed by humans or fed to cats.

Keywords

IsolationToxoplasma gondiitoxoplasmosisUSAwhite-tailed deer (Odocoileus virginianus)
Type
Research Article
Information
Parasitology , Volume 147 , Issue 7 , June 2020 , pp. 775 - 781
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Copyright
Copyright © The Author(s) 2020. Published by Cambridge University Press

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References

Adams, K and Ross, M (2013) QDMA's WhitetailReport 2013. An annual report on the status of white-tailed deer, the foundation of the hunting industry in North America. 1–67.Google Scholar
Ajzenberg, D, Bañuls, AL, Su, C, Dumètre, A, Demar, M, Carme, B and Dardé, ML (2004) Genetic diversity, clonality and sexuality in Toxoplasma gondii. International Journal for Parasitology 34, 1185–1196.CrossRefGoogle ScholarPubMed
Aubert, D, Ajzenberg, D, Richomme, C, Gilot-Fromont, E, Terrier, ME, de Gevigney, C, Game, Y, Maillard, D, Gibert, P, Dardé, ML and Villena, I (2010) Molecular and biological characteristics of Toxoplasma gondii isolates from wildlife in France. Veterinary Parasitology 171, 346–349.CrossRefGoogle ScholarPubMed
Ballash, GA, Dubey, JP, Kwok, OCH, Shoben, AB, Robison, TL, Kraft, TJ and Dennis, PM (2015) Seroprevalence of Toxoplasma gondii in white-tailed deer (Odocoileus virginianus) and free-roaming cats (Felis catus) across a suburban to urban gradient in northeastern Ohio. EcoHealth 12, 359–367.CrossRefGoogle ScholarPubMed
Crouch, EEV, Mittel, LD, Southard, TL, Cerqueira-Cézar, CK, Murata, FHA, Kwok, OCH, Su, C and Dubey, JP (2019) Littermate cats rescued from a shelter succumbed to acute, primary toxoplasmosis associated with TOXO DB genotype #4, generally circulating in wildlife. Parasitology International 72, 101942.CrossRefGoogle Scholar
Demar, M, Ajzenberg, D, Maubon, D, Djossou, F, Panchoe, D, Punwasi, W, Valery, N, Peneau, C, Daigre, JL, Aznar, C, Cottrelle, B, Terzan, L, Dardé, ML and Carme, B (2007) Fatal outbreak of human toxoplasmosis along the Maroni River: epidemiological, clinical, and parasitological aspects. Clinical Infectious Diseases 45, e88–e95.CrossRefGoogle ScholarPubMed
Dubey, JP (2010) Toxoplasmosis of Animals and Humans, 2nd Edn. Boca Raton, FL: CRC Press.Google Scholar
Dubey, JP and Desmonts, G (1987) Serological responses of equids fed Toxoplasma gondii oocysts. Equine Veterinary Journal 19, 337–339.CrossRefGoogle ScholarPubMed
Dubey, JP and Prowell, M (2013) Ante-mortem diagnosis, diarrhea, oocyst shedding, treatment, isolation, and genetic typing of Toxoplasma gondii associated with clinical toxoplasmosis in a naturally infected cat. Journal of Parasitology 99, 158–160.CrossRefGoogle Scholar
Dubey, JP, Thulliez, P and Powell, EC (1995) Toxoplasma gondii in Iowa sows: comparison of antibody titers to isolation of T. gondii by bioassays in mice and cats. Journal of Parasitology 81, 48–53.CrossRefGoogle Scholar
Dubey, JP, Graham, DH, de Young, RW, Dahl, E, Eberhard, ML, Nace, EK, Won, K, Bishop, H, Punkosdy, G, Sreekumar, C, Vianna, MCB, Shen, SK, Kwok, OCH, Sumners, JA, Demarais, S, Humphreys, JG and Lehmann, T (2004) Molecular and biologic characteristics of Toxoplasma gondii isolates from wildlife in the United States. Journal of Parasitology 90, 67–71.CrossRefGoogle ScholarPubMed
Dubey, JP, Velmurugan, GV, Ulrich, V, Gill, J, Carstensen, M, Sundar, N, Kwok, OCH, Thulliez, P, Majumdar, D and Su, C (2008) Transplacental toxoplasmosis in naturally-infected white-tailed deer: isolation and genetic characterisation of Toxoplasma gondii from foetuses of different gestational ages. International Journal for Parasitology 38, 1057–1063.CrossRefGoogle ScholarPubMed
Dubey, JP, Jenkins, MC, Kwok, OCH, Zink, RL, Michalski, ML, Ulrich, V, Gill, J, Carstensen, M and Thulliez, P (2009) Seroprevalence of Neospora caninum and Toxoplasma gondii antibodies in white-tailed deer (Odocoileus virginianus) from Iowa and Minnesota using four serologic tests. Veterinary Parasitology 161, 330–334.CrossRefGoogle ScholarPubMed
Dubey, JP, Randall, AR, Choudhary, S, Ferreira, LR, Verma, SK, Oliveira, S, Kwok, OCH and Su, C (2013 a) Occurrence, isolation, and genetic characterization of Toxoplasma gondii from white-tailed deer (Odocoileus virginianus) in New Jersey. Journal of Parasitology 99, 763–769.CrossRefGoogle Scholar
Dubey, JP, Tiwari, K, Chikweto, A, DeAllie, C, Sharma, R, Thomas, D, Choudhary, S, Ferreira, LR, Oliveira, S, Verma, SK, Kwok, OCH and Su, C (2013 b) Isolation and RFLP genotyping of Toxoplasma gondii from the domestic dogs (Canis familiaris) from Grenada, West Indies revealed high genetic variability. Veterinary Parasitology 197, 623–626.CrossRefGoogle ScholarPubMed
Dubey, JP, Dennis, PM, Verma, SK, Choudhary, S, Ferreira, LR, Oliveira, S, Kwok, OCH, Butler, E, Carstensen, M and Su, C (2014 a) Epidemiology of toxoplasmosis in white tailed deer (Odocoileus virginianus): occurrence, congenital transmission, correlates of infection, isolation, and genetic characterization of Toxoplasma gondii. Veterinary Parasitology 202, 270–275.CrossRefGoogle ScholarPubMed
Dubey, JP, Van Why, K, Verma, SK, Choudhary, S, Kwok, OCH, Khan, A, Behinke, MS, Sibley, LD, Ferreira, LR, Oliveira, S, Weaver, M, Stewart, R and Su, C (2014 b) Genotyping Toxoplasma gondii from wildlife in Pennsylvania and identification of natural recombinants virulent to mice. Veterinary Parasitology 200, 74–84.Google ScholarPubMed
Dubey, JP, Cerqueira-Cézar, CK, Murata, FHA, Verma, SK, Kwok, OCH, Pedersen, K, Rosenthal, BM and Su, C (2020) Genotyping of viable Toxoplasma gondii from the first national survey of feral swine revealed evidence for sylvatic transmission cycle, and presence of highly virulent parasite genotypes. Parasitology 147, 295–302. doi: 10.1017/S0031182019001586CrossRefGoogle ScholarPubMed
Elbez-Rubinstein, A, Ajzenberg, D, Dardé, ML, Cohen, R, Dumètre, A, Yera, H, Gondon, E, Janaud, JC and Thulliez, P (2009) Congenital toxoplasmosis and reinfection during pregnancy: case report, strain characterization, experimental model of reinfection, and review. Journal of Infectious Diseases 199, 280–285.CrossRefGoogle ScholarPubMed
Gaulin, C, Ramsay, D, Thivierge, K, Tataryn, J, Courville, A, Martin, C, Cunningham, P, Désilets, J, Morin, D and Dion, R (2020) Acute toxoplasmosis among Canadian deer hunters associated with consumption of undercooked deer meat hunted in the United States. Emerging Infectious Diseases 26, 199–205.CrossRefGoogle ScholarPubMed
Gerhold, RW, Saraf, P, Chapman, A, Zou, X, Hickling, G, Stiver, WH, Houston, A, Souza, M and Su, C (2017) Toxoplasma gondii seroprevalence and genotype diversity in select wildlife species from the southeastern United States. Parasites & Vectors 10, 508.CrossRefGoogle ScholarPubMed
Grigg, ME and Sundar, N (2009) Sexual recombination punctuated by outbreaks and clonal expansions predicts Toxoplasma gondii population genetics. International Journal for Parasitology 39, 925–933.CrossRefGoogle ScholarPubMed
Hollis-Etter, KM, Anchor, CL, Chelsvig, JE, Dubey, JP and Warner, RE (2019) Suburban white-tailed deer seropositive for Toxoplasma gondii from Chicago, Illinois. Parasitology Research 118, 2271–2276.CrossRefGoogle ScholarPubMed
Howe, DK and Sibley, LD (1995) Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotype with human disease. Journal of Infectious Diseases 172, 1561–1566.CrossRefGoogle ScholarPubMed
Humphreys, JG, Stewart, RL and Dubey, JP (1995) Prevalence of Toxoplasma gondii antibodies in sera of hunter-killed white-tailed deer in Pennsylvania. American Journal of Veterinary Research 56, 172–173.Google ScholarPubMed
Jiang, T, Shwab, EK, Martin, RM, Gerhold, RW, Rosenthal, BM, Dubey, JP and Su, C (2018) A partition of Toxoplasma gondii genotypes across spatial gradients and among host species, and decreased parasite diversity towards areas of human settlement in North America. International Journal for Parasitology 48, 611–619.CrossRefGoogle ScholarPubMed
Jokelainen, P, Näreaho, A, Knaapi, S, Oksanen, A, Rikula, U and Sukura, A (2010) Toxoplasma gondii in wild cervids and sheep in Finland: north-south gradient in seroprevalence. Veterinary Parasitology 171, 331–336.CrossRefGoogle ScholarPubMed
Jokelainen, P, Murat, JB and Nielsen, HV (2018) Direct genetic characterization of Toxoplasma gondii from clinical samples from Denmark: not only genotypes II and III. European Journal of Clinical Microbiology and Infectious Diseases 37, 579–586.CrossRefGoogle ScholarPubMed
Lindsay, DS, Blagburn, BL, Dubey, JP and Mason, WH (1991) Prevalence and isolation of Toxoplasma gondii from white-tailed deer in Alabama. Journal of Parasitology 77, 62–64.CrossRefGoogle ScholarPubMed
Lindsay, DS, Sundermann, CA, Dubey, JP and Blagburn, BL (1997) Update on Toxoplasma gondii infections in wildlife and exotic animals from Alabama. Journal of the Alabama Academy of Science 68, 246–254.Google Scholar
Lorenzi, H, Khan, A, Behnke, MS, Namasivayam, S, Swapna, LS, Hadjithomas, M, Karamycheva, S, Pinney, D, Brunk, BP, Ajioka, JW, Ajzenberg, D, Boothroyd, JC, Boyle, JP, Dardé, ML, Diaz-Miranda, MA, Dubey, JP, Fritz, HM, Gennari, SM, Gregory, BD, Kim, K, Saeij, JPJ, Su, C, White, MW, Zhu, XQ, Howe, DK, Rosenthal, BM, Grigg, ME, Parkinson, J, Liu, L, Kissinger, JC, Roos, DS and Sibley, LD (2016) Local admixture of amplified and diversified secreted pathogenesis determinants shapes mosaic Toxoplasma gondii genomes. Nature Communications 7, 10147.CrossRefGoogle ScholarPubMed
Pomares, C, Devillard, S, Holmes, TH, Olariu, TR, Press, CJ, Ramirez, R, Talucod, J, Estran, R, Su, C, Dubey, JP, Ajzenberg, D and Montoya, JG (2018) Genetic characterization of Toxoplasma gondii DNA samples isolated from humans living in North America: an unexpected high prevalence of atypical genotypes. Journal of Infectious Diseases 218, 1783–1791.CrossRefGoogle ScholarPubMed
Ross, RD, Stec, LA, Werner, JC, Blumenkranz, MS, Glazer, L and Williams, GA (2001) Presumed acquired ocular toxoplasmosis in deer hunters. Retina 21, 226–229.CrossRefGoogle ScholarPubMed
Sacks, JJ, Delgado, DG, Lobel, HO and Parker, RL (1983) Toxoplasmosis infection associated with eating undercooked venison. American Journal of Epidemiology 118, 832–838.CrossRefGoogle ScholarPubMed
Schumacher, A, Kazmierczak, J, Moldenhauer, E, Hanhly, T, Montoya, J, Press, C, Letzer, L, Elbadawi, S, Smiley, S and Davis, J (2018) Toxoplasmosis associated with venison consumption during a retreat – Wisconsin, September–October 2017. Presented at 67th Annual Epidemic Intelligence Service (EIS) Conference, 16–19 April 2018, Atlanta, Georgia, USA.Google Scholar
Shwab, EK, Saraf, P, Zhu, XQ, Zhou, DH, McFerrin, BM, Ajzenberg, D, Schares, G, Hammond-Aryee, K, van Helden, P, Higgins, SA, Gerhold, RW, Rosenthal, BM, Zhao, X, Dubey, JP and Su, C (2018) Human impact on the diversity and virulence of the ubiquitous zoonotic parasite Toxoplasma gondii. Proceedings of the National Academy of Sciences of the United States of America 115, E6956–E6963.CrossRefGoogle ScholarPubMed
Sibley, LD and Ajioka, JW (2008) Population structure of Toxoplasma gondii: clonal expansion driven by infrequent recombination and selective sweeps. Annual Review of Microbiology 62, 329–351.CrossRefGoogle ScholarPubMed
Su, C and Dubey, JP (2020) Isolation and genotyping of Toxoplasma gondii strains. Methods in Molecular Biology 2071, 49–80.CrossRefGoogle ScholarPubMed
Su, C, Shwab, EK, Zhou, P, Zhu, XQ and Dubey, JP (2010) Moving towards an integrated approach to molecular detection and identification of Toxoplasma gondii. Parasitology 137, 1–11.CrossRefGoogle ScholarPubMed
Vanek, JA, Dubey, JP, Thulliez, P, Riggs, MR and Stromberg, BE (1996) Prevalence of Toxoplasma gondii antibodies in hunter-killed white-tailed deer (Odocoileus virginianus) in four regions of Minnesota. Journal of Parasitology 82, 41–44.Google ScholarPubMed
VanWormer, E, Miller, MA, Conrad, PA, Grigg, ME, Rejmanek, D, Carpenter, TE and Mazet, JAK (2014) Using molecular epidemiology to track Toxoplasma gondii from terrestrial carnivores to marine hosts: implications for public health and conservation. PLoS Neglected Tropical Diseases 8, e2852.CrossRefGoogle ScholarPubMed
Verma, SK, Sweeny, AR, Lovallo, MJ, Calero-Bernal, R, Kwok, OC, Jiang, T, Su, C, Grigg, ME and Dubey, JP (2017) Seroprevalence, isolation, and co-infection of multiple Toxoplasma gondii strains in individual bobcats (Lynx rufus) from Mississippi, USA. International Journal for Parasitology 47, 297–303.CrossRefGoogle ScholarPubMed
Yu, L, Shen, J, Su, C and Sundermann, CA (2013) Genetic characterization of Toxoplasma gondii in wildlife from Alabama, USA. Parasitology Research 112, 1333–1336.CrossRefGoogle ScholarPubMed
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