Isolation and characterization of new genetic types of Toxoplasma gondii and prevalence of Trichinella murrelli from black bear (Ursus americanus)

Veterinary Parasitology

Volumn 196, Issue 1-2, 2013, Pages 24-30

  Dubey, J P ^a   Hill, D ^a   Zarlenga, D ^a   Choudhary, S ^a   Ferreira, L R ^a   Oliveira, S ^a   Verma, S K ^a   Kwok, O C H ^a   Driscoll, C P ^b   Spiker, H ^b   Su, C ^c  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

^b MARYLAND DEPARTMENT OF NATURAL RESOURCES   (United States)

^c UNIVERSITY OF TENNESSEE   (United States)

Author keywords

Black bear (Ursus americanus); Toxoplasma gondii; Trichinella murrelli; USA

Indexed keywords

CHLORIDE; PEPSIN A;

AGGLUTINATION TEST; ANIMAL TISSUE; ARTICLE; BLACK BEAR; FEMALE; GENOTYPE; LARVA; MALE; MOUSE; NONHUMAN; PARASITE ISOLATION; PARASITE VIABILITY; PARASITE VIRULENCE; POLYMERASE CHAIN REACTION; PREVALENCE; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; TACHYZOITE; TONGUE; TOXOPLASMA GONDII; TOXOPLASMOSIS; TRICHINELLA; TRICHINELLA MURRELLI; TRICHINOSIS; UNITED STATES; WILDLIFE;

MUS; TOXOPLASMA GONDII; TRICHINELLA; TRICHINELLA MURRELLI; URSUS AMERICANUS;

EID: 84880734719     PISSN: 03044017     EISSN: 18732550     Source Type: Journal    
DOI: 10.1016/j.vetpar.2013.02.007     Document Type: Article

References (53)

1. Ajzenberg D., Bañuls A.L., Tibayrenc M., Dardé M.L. Microsatellite analysis of Toxoplasma gondii shows considerable polymorphism structured into two main clonal groups. Int. J. Parasitol. 2002, 32:27-38.
2. Ajzenberg D., Cogné N., Paris L., Bessières M.H., Thulliez P., Filisetti D., Pelloux H., Marty P., Dardé M.L. Genotype of 86 Toxoplasma gondii isolates associated with human congenital toxoplasmosis, and correlation with clinical findings. J. Infect. Dis. 2002, 186:684-689.
3. Ajzenberg D., Bañuls A.L., Su C., Dumètre A., Demar M., Carme B., Dardé M.L. Genetic diversity, clonality and sexuality in Toxoplasma gondii. Int. J. Parasitol. 2004, 34:1185-1196.
4. Ancelle T. History of trichinellosis outbreaks linked to horse meat consumption 1975-1998. Euro. Surveill. 1998, 3:86-89.
5. Aubert D., Ajzenberg D., Richomme C., Gilot-Fromont E., Terrier M.E., de Gevigney C., Game Y., Maillard D., Gibert P., Dardé M.L., Villena I. Molecular and biological characteristics of Toxoplasma gondii isolates from wildlife in France. Vet. Parasitol. 2010, 171:346-349.
6. Briscoe N., Humphreys J.G., Dubey J.P. Prevalence of Toxoplasma gondii infections in Pennsylvania black bears, Ursus americanus. J. Wildl. Dis. 1993, 29:599-601.
7. Burke R., Masuoka P., Murrell K.D. Swine Trichinella infection and geographic information system tools. Emerg. Infect. Dis. 2008, 14:1109-1111.
8. Centers for Disease Control and Prevention (CDC) Trichinellosis associated with bear meat-New York and Tennessee. MMWR Morb. Mortal. Wkly. Rep. 2003, 53:606-610.
9. Chomel B.B., Zarnke R.L., Kasten R.W., Kass P.H., Mendes E. Serologic survey of Toxoplasma gondii in grizzly bears (Ursus arctos) and black bears (Ursus americanus), from Alaska, 1988 to 1991. J. Wildl. Dis. 1995, 31:472-479.
10. Chambers D.L., Ulrey W.A., Guthrie J.M., Kwok O.C.H., Cox J.J., Maehr D.S., Dubey J.P. Seroprevalence of Toxoplasma gondii from free-ranging black bears (Ulsus americanus) from Florida. J. Parasitol. 2012, 98:674-675.
11. Dardé M.L., Bouteille B., Perstreal M. Isoenzyme analysis of 35 Toxoplasma gondii isolates and the biological and epidemiologic implications. J. Parasitol. 1992, 78:909-912.
12. Demar M., Ajzenberg D., Maubon D., Djossou F., Panchoe D., Punwasi W., Valery N., Peneau C., Daigre J.L., Aznar C., Cottrelle B., Terzan L., Dardé M.L., Carme B. Fatal outbreak of human toxoplasmosis along the Maroni River: epidemiological, clinical, and parasitological aspects. Clin. Infect. Dis. 2007, 45:e88-e95.
13. Dubey J.P., Desmonts G. Serological responses of equids fed Toxoplasma gondii oocysts. Equine Vet. J. 1987, 19:337-339.
14. Dubey J.P., Briscoe N., Gamble R., Zarlenga D., Humphreys J.G., Thulliez P. Characterization of Toxoplasma and Trichinella isolates from muscles of black bears in Pennsylvania. Am. J. Vet. Res. 1994, 55:815-819.
15. Dubey J.P., Humphreys J.G., Thulliez P. Prevalence of viable Toxoplasma gondii tissue cysts and antibodies to T. gondii by various serologic tests in black bears (Ursus americanus) from Pennsylvania. J. Parasitol. 1995, 81:109-112.
16. Dubey J.P., Graham D.H., de Young R.W., Dahl E., Eberhard M.L., Nace E.K., Won K., Bishop H., Punkosdy G., Sreekumar C., Vianna M.C.B., Shen S.K., Kwok O.C.H., Sumners J.A., Demarais S., Humphreys J.G., Lehmann T. Molecular and biologic characteristics of Toxoplasma gondii isolates from wildlife in the United States. J. Parasitol. 2004, 90:67-71.
17. Dubey J.P., Jones J.L. Toxoplasma gondii infection in humans and animals in the United States. Int. J. Parasitol. 2008, 38:1257-1278.
18. Dubey J.P. Toxoplasmosis of Animals and Humans 2010, CRC Press, Boca Raton, FL, pp. 1-313. 2nd ed.
19. Dubey J.P., Rajendran C., Ferreira L.R., Kwok O.C.H., Sinnett D., Majumdar D., Su C. A new atypical highly mouse virulent Toxoplasma gondii genotype isolated from a wild black bear in Alaska. J. Parasitol. 2010, 96:713-716.
20. Dubey J.P., Rajendran C., Ferreira L.R., Martins J., Kwok O.C.H., Hill D.E., Villena I., Zhou H., Su C., Jones J.L. High prevalence and genotypes of Toxoplasma gondii isolated from goats from a retail meat store destined for human consumption in the USA. Int. J. Parasitol. 2011, 41:827-833.
21. Dubey J.P., Velmurugan G.V., Rajendran C., Yabsley M., Thomas N.J., Beckman K.B., Sinnett D., Ruid D., Paul W., Hart J., Fair P.A., McFee W.E., Shearn-Bochsler V., Kwok O.C.H., Ferreira L., Choudhary S., Faria E.B., Zhou H., Felix T.A., Su C. Genetic characterization of Toxoplasma gondii in wildlife from North America revealed widespread and high prevalence of the fourth clonal type. Int. J. Parasitol. 2011, 41:1139-1147.
22. Dubey, J.P., Choudhary, S., Kwok, O.C.H., Ferreira, L.R., Solange, S., Verma, S.K., Marks, D.R., Pedersen, K., Mickley, R.M., Randall, A.R., Arsnoe, D., Su. C. Isolation and genetic characterization of Toxoplasma gondii from mute swan (Cygnus olor) from the USA. Vet. Parasitol., in press. doi:10.1016/j.vetpar.2012.12.051.
23. Dunbar M.R., Cunningham M.W., Roof J.C. Seroprevalence of selected disease agents from free-ranging black bears in Florida. J. Wildl. Dis. 1998, 34:612-619.
24. Elbez-Rubinstein A., Ajzenberg D., Dardé M.L., Cohen R., Dumètre A., Yera H., Gondon E., Janaud J.C., Thulliez P. Congenital toxoplasmosis and reinfection during pregnancy: case report, strain characterization, experimental model of reinfection, and review. J. Infect. Dis. 2009, 199:280-285.
25. Grigg M.E., Sundar N. Sexual recombination punctuated by outbreaks and clonal expansions predicts Toxoplasma gondii population genetics. Int. J. Parasitol. 2009, 39:925-933.
26. Hall R.L., Lindsay A., Hammond C., Montgomery S.P., Wilkins P.P., da Silva A.J., McAuliffe I., de Almeida M., Bishop H., Mathison B., Sun B., Largusa R., Jones J.L. Outbreak of human trichinellosis in Northern California caused by Trichinella murrelli. Am. J. Trop. Med. Hyg. 2012, 87:297-302.
27. Hill D.E., Gamble H.R., Zarlenga D.S., Coss C., Finnigan J. Trichinella nativa in a black bear from Plymouth, New Hampshire. Vet. Parasitol. 2005, 132:143-146.
28. Hill D.E., Samuel M.D., Nolden C.A., Sundar N., Zarlenga D.S., Dubey J.P. Trichinella murrelli in scavenging mammals from south-central Wisconsin, USA. J. Wildl. Dis. 2008, 44:629-635.
29. Hill D.E., Pierce V., Murrell K.D., Ratliffe N., Rupp B., Fournet V.M., Zarlenga D.S., Rosenthal B.M., Gamble H.R., Kelly K., Dulin M. Cessation of Trichinella spiralis transmission among scavenging mammals after the removal of infected pigs from a poorly managed farm: implications for trichinae transmission in the U.S. Zoo. Public Health 2010, 57:e116-e123. 10.1111/j.1863-2378.2009.01296.x.
30. Howe D.K., Sibley L.D. Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotype with human disease. J. Infect. Dis. 1995, 172:1561-1566.
31. Jordan G.W., Theis J., Fuller C.M., Hoeprich P.D. Bear meat trichinosis with a concomitant serologic response to Toxoplasma gondii. Am. J. Med. Sci. 1975, 269:251-257.
32. Khan A., Dubey J.P., Su C., Ajioka J.W., Rosenthal B., Sibley L.D. Genetic analyses of atypical Toxoplasma gondii strains reveals a fourth clonal lineage in North America. Int. J. Parasitol. 2011, 41:645-655.
33. McLeod R., Boyer K.M., Lee D., Mui E., Wroblewski K., Karrison T., Noble A.G., Withers S., Swisher C.N., Heydemann P.T., Sautter M., Babiarz J., Rabiah P., Meier P., Grigg M.E., The Toxoplasmosis Study Group Prematurity and severity are associated with Toxoplasma gondii alleles (NCCCTS, 1981-2009). Clin. Infect. Dis. 2012, 54:1595-1605.
34. Nutter F.B., Levine J.F., Stoskopf M.K., Gamble H.R., Dubey J.P. Seroprevalence of Toxoplasma gondii and Trichinella spiralis in North Carolina black bears (Ursus americanus). J. Parasitol. 1998, 84:1048-1050.
35. Pozio E., La Rosa G., Murrell K.D., Lichtenfels J.R. Taxonomic revision of the genus Trichinella. J. Parasitol. 1992, 78:654-659.
36. Pozio E., La Rosa G. Trichinella murrellin sp.: etiological agent of sylvatic trichinellosis in temperate areas of North America. J. Parasitol. 2000, 86:134-139.
37. Pozio E., Pence D.B., La Rosa G., Casulli A., Henke S.E. Trichinella infection in wildlife of the southwestern United States. J. Parasitol. 2001, 87(5):1208-1210.
38. Pozio E., Zarlenga D.S. Recent advances on the taxonomy, systematics and epidemiology of Trichinella. Int. J. Parasitol. 2005, 35:1191-1204.
39. Rogers L.L. Parasites of black bears of the Lake Superior region. J. Wildl. Dis. 1975, 11:189-192.
40. Rosenthal B.M., La Rosa G., Zarlenga D., Dunams D., Chunyu Y., Mingyuan L., Pozio E. Human dispersal of Trichinella spiralis in domesticated pigs. Infect. Gen. Evol. 2008, 6:799-805.
41. Ruppanner R., Jessup D.A., Ohishi I., Behymer D.E., Franti C.E. Serologic survey for certain zoonotic diseases in black bears in California. J. Am. Vet. Med. Assoc. 1982, 181:1288-1291.
42. Schad G.A., Leiby D.A., Duffy C.H., Murrell K.D., Alt G.L. Trichinella spiralis in the black bear (Ursus americanus) of Pennsylvania: distribution, prevalence and intensity of infection. J. Wildl. Dis. 1986, 22(1):36-41.
43. Snyder D.E., Zarlenga D.S., La Rosa G., Pozio E. Biochemical, biological, and genetic characterization of a sylvatic isolate of Trichinella. J. Parasitol. 1993, 79:347-352.
44. Su C., Shwab E.K., Zhou P., Zhu X.Q., Dubey J.P. Moving towards an integrated approach to molecular detection and identification of Toxoplasma gondii. Parasitology 2010, 137:1-11.
45. Su C., Khan A., Zhou P., Majumdar D., Ajzenberg D., Dardé M.L., Zhu X.Q., Ajioka J.W., Rosenthal B.M., Dubey J.P., Sibley L.D. Globally diverse Toxoplasma gondii isolates comprise six major clades originating from a small number of distinct ancestral lineages. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:5844-5849.
46. Vaudaux J.D., Muccioli C., James E.R., Silveira C., Magargal S.L., Jung C., Dubey J.P., Jones J.L., Doymaz M.Z., Bruckner D.A., Belfort R., Holland G.N., Grigg M.E. Identification of an atypical strain of Toxoplasma gondii as the cause of a waterborne outbreak of toxoplasmosis in Santa Isabel do Ivai Brazil. J. Infect. Dis. 2010, 202:1226-1233.
47. Velmurugan G.V., Su C., Dubey J.P. Isolate designation and characterization of Toxoplasma gondii isolates from pigs in the United States. J. Parasitol. 2009, 95:95-99.
48. Wendte J.M., Miller M.A., Lambourn D.M., Magargal S.L., Jessup D.A., Grigg M.E. Self-mating in the definitive host potentiates clonal outbreaks of the apicomplexan parasites Sarcocystis neurona and Toxoplasma gondii. PLoS Genet. 2010, 6(12):e1001261.
49. Wilson D., Ruff S. The Smithsonian Book of North American Mammals 1999, The Smithsonian Institution Press, Washington, D.C, pp. 1-750.
50. Zarlenga D.S., Chute M.B., Martin A., Kapel C.M. A multiplex PCR for unequivocal differentiation of all encapsulated and non-encapsulated genotypes of Trichinella. Int. J. Parasitol. 1999, 29:1859-1867.
51. Zarlenga D.S., Al-Yaman F., Minchella D.J., La Rosa G. A repetitive DNA probe specific for a North American sylvatic genotype of Trichinella. Mol. Biochem. Parasitol. 1991, 48:131-137.
52. Zarnke R.L., Dubey J.P., Kwok O.C.H., Ver Hoef J.M. Serologic survey for Toxoplasma gondii in selected wildlife species from Alaska. J. Wildl. Dis. 2000, 36:219-224.
53. Zimmermann W.J. Trichinosis in bears of western and northcentral United States. Am. J. Epidemiol. 1977, 106:167-171.