Advertisement

Toxoplasma

  • Gastón Moré
  • Maria Cecilia Venturini
  • Lais Pardini
  • Juan Manuel Unzaga
Chapter

Abstract

Toxoplasmosis is a zoonotic infection caused by the protozoon Toxoplasma gondii affecting animals worldwide. T. gondii has a facultative heteroxenous life cycle with felids as definitive hosts and a wide range of mammalian and avian species as intermediate hosts. Infectious stages are oocysts present in felid feces, bradyzoites forming tissue cysts, and tachyzoites. While two major clonal lineages (type II and III) dominate clinical and natural isolates in Europe and North America, other parts of the world, like Brazil and Argentina, are dominated by non-clonal or other clonal T. gondii lineages, representing a greater genetic diversity. Different animal species show a variable degree of susceptibility to T. gondii infection and to the development of clinical signs. Humans are considered susceptible, and about one third of the human population in the world is estimated to be infected. Toxoplasmosis is an important abortive disease in small ruminants. It is mainly asymptomatic in cattle and chicken, but the latter is an epidemiological sentinel, and isolation of viable parasites from this source is frequent. Infected pigs can show reproductive failure, and, in addition, their tissues are considered, together with infected small ruminant tissues, a relevant source of human infection. Cats and dogs can show neuromuscular disease mainly associated with other immunosuppressive conditions, such as viral infections. Some species like New World monkeys, lemurs, Pallas’ cats, slender-tailed meerkats, and some Australian marsupials are highly susceptible to fatal generalized toxoplasmosis. General control measures are presented, focusing on the prevention of human toxoplasmosis.

Keywords

Toxoplasma gondii Zoonosis Intermediate and definitive hosts Acute toxoplasmosis Genotypes 

References

  1. Adkesson MJ, Gorman ME, Hsiao V, Whittington JK, Langan JN. Toxoplasma gondii inclusions in peripheral blood leukocytes of a red-necked wallaby (Macropus rufogriseus). Vet Clin Pathol. 2007;36:97–100.CrossRefGoogle Scholar
  2. Ajzenberg D. 1995-2015: it is time to celebrate 20 years of (intensive) genotyping of Toxoplasma gondii strains. Future Microbiol. 2015;10:689–91.  https://doi.org/10.2217/fmb.15.23.CrossRefPubMedGoogle Scholar
  3. Ajzenberg D, Banuls AL, Su C, Dumetre A, Demar M, Carme B, Darde ML. Genetic diversity, clonality and sexuality in Toxoplasma gondii. Int J Parasitol. 2004;34:1185–96.  https://doi.org/10.1016/j.ijpara.2004.06.007.CrossRefPubMedGoogle Scholar
  4. Ali CN, Harris JA, Watkins JD, Adesiyun AA. Seroepidemiology of Toxoplasma gondii in dogs in Trinidad and Tobago. Vet Parasitol. 2003;113:179–87.CrossRefGoogle Scholar
  5. Basso W, Edelhofer R, Zenker W, Mostl K, Kubber-Heiss A, Prosl H. Toxoplasmosis in Pallas’ cats (Otocolobus manul) raised in captivity. Parasitology. 2005;130:293–9.CrossRefGoogle Scholar
  6. Basso W, Venturini MC, More G, Quiroga A, Bacigalupe D, Unzaga JM, Larsen A, Laplace R, Venturini L. Toxoplasmosis in captive Bennett’s wallabies (Macropus rufogriseus) in Argentina. Vet Parasitol. 2007;144:157–61.  https://doi.org/10.1016/j.vetpar.2006.09.030.CrossRefPubMedGoogle Scholar
  7. Basso W, et al. Isolation and molecular characterization of Toxoplasma gondii from captive slender-tailed meerkats (Suricata suricatta) with fatal toxoplasmosis in Argentina. Vet Parasitol. 2009;161:201–6.  https://doi.org/10.1016/j.vetpar.2009.01.006.CrossRefPubMedGoogle Scholar
  8. Basso W, Handke M, Sydler T, Borel N, Grimm F, Sidler X, Deplazes P. Involvement of Toxoplasma gondii in reproductive disorders in Swiss pig farms. Parasitol Int. 2015;64:157–60.  https://doi.org/10.1016/j.parint.2014.11.017.CrossRefPubMedGoogle Scholar
  9. Beck HP, et al. Molecular approaches to diversity of populations of apicomplexan parasites. Int J Parasitol. 2009;39:175–89.  https://doi.org/10.1016/j.ijpara.2008.10.001.CrossRefPubMedGoogle Scholar
  10. Bermudez R, Failde LD, Losada AP, Nieto JM, Quiroga MI. Toxoplasmosis in Bennett’s wallabies (Macropus rufogriseus) in Spain. Vet Parasitol. 2009;160:155–8.  https://doi.org/10.1016/j.vetpar.2008.10.082.CrossRefPubMedGoogle Scholar
  11. Blader IJ, Saeij JP. Communication between Toxoplasma gondii and its host: impact on parasite growth, development, immune evasion, and virulence. APMIS. 2009;117:458–76.  https://doi.org/10.1111/j.1600-0463.2009.02453.x.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Buxton D, Thomson K, Maley S, Wright S, Bos HJ. Vaccination of sheep with a live incomplete strain (S48) of Toxoplasma gondii and their immunity to challenge when pregnant. Vet Rec. 1991;129:89–93.CrossRefGoogle Scholar
  13. Canada N, Meireles CS, Rocha A, da Costa JM, Erickson MW, Dubey JP. Isolation of viable Toxoplasma gondii from naturally infected aborted bovine fetuses. J Parasitol. 2002;88:1247–8.  https://doi.org/10.1645/0022-3395(2002)088[1247:IOVTGF]2.0.CO;2.CrossRefPubMedGoogle Scholar
  14. Carme B, Demar M, Ajzenberg D, Darde ML. Severe acquired toxoplasmosis caused by wild cycle of Toxoplasma gondii, French Guiana. Emerg Infect Dis. 2009;15:656–8.  https://doi.org/10.3201/eid1504.081306.CrossRefPubMedPubMedCentralGoogle Scholar
  15. Deng H, Dam-Deisz C, Luttikholt S, Maas M, Nielen M, Swart A, Vellema P, van der Giessen J, Opsteegh M. Risk factors related to Toxoplasma gondii seroprevalence in indoor-housed Dutch dairy goats. Prev Vet Med. 2016;124:45–51.  https://doi.org/10.1016/j.prevetmed.2015.12.014.CrossRefPubMedGoogle Scholar
  16. Dietz HH, Henriksen P, Bille-Hansen V, Henriksen SA. Toxoplasmosis in a colony of new world monkeys. Vet Parasitol. 1997;68:299–304.CrossRefGoogle Scholar
  17. Dubey JP. Distribution of cysts and tachyzoites in calves and pregnant cows inoculated with Toxoplasma gondii oocysts. Vet Parasitol. 1983;13:199–211.CrossRefGoogle Scholar
  18. Dubey JP. A review of toxoplasmosis in pigs. Vet Parasitol. 1986;19:181–223.CrossRefGoogle Scholar
  19. Dubey JP. Strategies to reduce transmission of Toxoplasma gondii to animals and humans. Vet Parasitol. 1996;64:65–70.CrossRefGoogle Scholar
  20. Dubey JP. Advances in the life cycle of Toxoplasma gondii. Int J Parasitol. 1998a;28:1019–24.CrossRefGoogle Scholar
  21. Dubey JP. Toxoplasma gondii oocyst survival under defined temperatures. J Parasitol. 1998b;84:862–5.CrossRefGoogle Scholar
  22. Dubey JP. A review of toxoplasmosis in wild birds. Vet Parasitol. 2002;106:121–53.CrossRefGoogle Scholar
  23. Dubey JP. Toxoplasma gondii infections in chickens (Gallus domesticus): prevalence, clinical disease, diagnosis and public health significance. Zoonoses Public Health. 2010a;57:60–73.  https://doi.org/10.1111/j.1863-2378.2009.01274.x.CrossRefPubMedGoogle Scholar
  24. Dubey JP. Toxoplasmosis of animals and humans. 2nd ed. Boca Raton, FL: CRC Press; 2010b.Google Scholar
  25. Dubey JP, Carpenter JL. Histologically confirmed clinical toxoplasmosis in cats: 100 cases (1952-1990). J Am Vet Med Assoc. 1993;203:1556–66.PubMedGoogle Scholar
  26. Dubey JP, Crutchley C. Toxoplasmosis in wallabies (Macropus rufogriseus and Macropus eugenii): blindness, treatment with atovaquone, and isolation of Toxoplasma gondii. J Parasitol. 2008;94:929–33.  https://doi.org/10.1645/GE-1448.1.CrossRefPubMedGoogle Scholar
  27. Dubey JP, Emond JP, Desmonts G, Anderson WR. Serodiagnosis of postnatally and prenatally induced toxoplasmosis in sheep. Am J Vet Res. 1987;48:1239–43.PubMedGoogle Scholar
  28. Dubey JP, Carpenter JL, Speer CA, Topper MJ, Uggla A. Newly recognized fatal protozoan disease of dogs. J Am Vet Med Assoc. 1988a;192:1269–85.PubMedGoogle Scholar
  29. Dubey JP, Ott-Joslin J, Torgerson RW, Topper MJ, Sundberg JP. Toxoplasmosis in black-faced kangaroos (Macropus fuliginosus melanops). Vet Parasitol. 1988b;30:97–105.CrossRefGoogle Scholar
  30. Dubey JP, Lindsay DS, Speer CA. Structures of Toxoplasma gondii tachyzoites, bradyzoites, and sporozoites and biology and development of tissue cysts. Clin Microbiol Rev. 1998;11:267–99.PubMedPubMedCentralGoogle Scholar
  31. Dubey JP, et al. Prevalence of viable Toxoplasma gondii in beef, chicken, and pork from retail meat stores in the United States: risk assessment to consumers. J Parasitol. 2005;91:1082–93.  https://doi.org/10.1645/GE-683.1.CrossRefPubMedGoogle Scholar
  32. Dubey JP, Webb DM, Sundar N, Velmurugan GV, Bandini LA, Kwok OC, Su C. Endemic avian toxoplasmosis on a farm in Illinois: clinical disease, diagnosis, biologic and genetic characteristics of Toxoplasma gondii isolates from chickens (Gallus domesticus), and a goose (Anser Anser). Vet Parasitol. 2007;148:207–12.CrossRefGoogle Scholar
  33. Dubey JP, Pas A, Rajendran C, Kwok OC, Ferreira LR, Martins J, Hebel C, Hammer S, Su C. Toxoplasmosis in sand cats (Felis margarita) and other animals in the breeding Centre for Endangered Arabian Wildlife in the United Arab Emirates and al Wabra wildlife preservation, the State of Qatar. Vet Parasitol. 2010;172:195–203.  https://doi.org/10.1016/j.vetpar.2010.05.013.CrossRefPubMedGoogle Scholar
  34. Epe C, Ising-Volmer S, Stoye M. Parasitological fecal studies of equids, dogs, cats and hedgehogs during the years 1984-1991. Dtsch Tierarztl Wochenschr. 1993;100:426–8.PubMedGoogle Scholar
  35. Faria EB, Gennari SM, Pena HF, Athayde AC, Silva ML, Azevedo SS. Prevalence of anti-Toxoplasma gondii and anti-Neospora caninum antibodies in goats slaughtered in the public slaughterhouse of Patos city, Paraiba state, northeast region of Brazil. Vet Parasitol. 2007;149:126–9.  https://doi.org/10.1016/j.vetpar.2007.07.009.CrossRefPubMedGoogle Scholar
  36. Fentress SJ, et al. Phosphorylation of immunity-related GTPases by a Toxoplasma gondii-secreted kinase promotes macrophage survival and virulence. Cell Host Microbe. 2010;8:484–95.  https://doi.org/10.1016/j.chom.2010.11.005.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Fleckenstein MC, Reese ML, Konen-Waisman S, Boothroyd JC, Howard JC, Steinfeldt T. A Toxoplasma gondii pseudokinase inhibits host IRG resistance proteins. PLoS Biol. 2012;10:e1001358.  https://doi.org/10.1371/journal.pbio.1001358.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Gamble HR, Brady RC, Dubey JP. Prevalence of Toxoplasma gondii infection in domestic pigs in the New England states. Vet Parasitol. 1999;82:129–36.CrossRefGoogle Scholar
  39. Garcia-Bocanegra I, Cabezon O, Hernandez E, Martinez-Cruz MS, Martinez-Moreno A, Martinez-Moreno J. Toxoplasma gondii in ruminant species (cattle, sheep, and goats) from southern Spain. J Parasitol. 2013;99:438–40.  https://doi.org/10.1645/12-27.1.CrossRefPubMedGoogle Scholar
  40. Gottstein B, Hentrich B, Wyss R, Thur B, Busato A, Stark KD, Muller N. Molecular and immunodiagnostic investigations on bovine neosporosis in Switzerland. Int J Parasitol. 1998;28:679–91.CrossRefGoogle Scholar
  41. Gyimesi ZS, Lappin MR, Dubey JP. Application of assays for the diagnosis of toxoplasmosis in a colony of woolly monkeys (Lagothrix lagotricha). J Zoo Wildl Med. 2006;37:276–80.  https://doi.org/10.1638/05-018.1.CrossRefPubMedGoogle Scholar
  42. Hide G. Role of vertical transmission of Toxoplasma gondii in prevalence of infection. Expert Rev Anti Infect Ther. 2016;14:335–44.  https://doi.org/10.1586/14787210.2016.1146131.CrossRefPubMedGoogle Scholar
  43. Howe DK, Sibley LD. Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotype with human disease. J Infect Dis. 1995;172:1561–6.CrossRefGoogle Scholar
  44. Howe DK, Honore S, Derouin F, Sibley LD. Determination of genotypes of Toxoplasma gondii strains isolated from patients with toxoplasmosis. J Clin Microbiol. 1997;35:1411–4.PubMedPubMedCentralGoogle Scholar
  45. Iovu A, Gyorke A, Mircean V, Gavrea R, Cozma V. Seroprevalence of Toxoplasma gondii and Neospora caninum in dairy goats from Romania. Vet Parasitol. 2012;186:470–4.  https://doi.org/10.1016/j.vetpar.2011.11.062.CrossRefPubMedGoogle Scholar
  46. Jones JL, Kruszon-Moran D, Wilson M, McQuillan G, Navin T, McAuley JB. Toxoplasma gondii infection in the United States: seroprevalence and risk factors. Am J Epidemiol. 2001a;154:357–65.CrossRefGoogle Scholar
  47. Jones JL, Lopez A, Wilson M, Schulkin J, Gibbs R. Congenital toxoplasmosis: a review. Obstet Gynecol Surv. 2001b;56:296–305.CrossRefGoogle Scholar
  48. Karsten V, Qi H, Beckers CJ, Reddy A, Dubremetz JF, Webster P, Joiner KA. The protozoan parasite Toxoplasma gondii targets proteins to dense granules and the vacuolar space using both conserved and unusual mechanisms. J Cell Biol. 1998;141:1323–33.CrossRefGoogle Scholar
  49. Labalette P, Delhaes L, Margaron F, Fortier B, Rouland JF. Ocular toxoplasmosis after the fifth decade. Am J Ophthalmol. 2002;133:506–15.CrossRefGoogle Scholar
  50. Lang C, Gross U, Luder CG. Subversion of innate and adaptive immune responses by Toxoplasma gondii. Parasitol Res. 2007;100:191–203.  https://doi.org/10.1007/s00436-006-0306-9.CrossRefPubMedGoogle Scholar
  51. Lin MH, Chen TC, Kuo TT, Tseng CC, Tseng CP. Real-time PCR for quantitative detection of Toxoplasma gondii. J Clin Microbiol. 2000;38:4121–5.PubMedPubMedCentralGoogle Scholar
  52. Lindsay DS, Dubey JP. Toxoplasma gondii: the changing paradigm of congenital toxoplasmosis. Parasitology. 2011;138:1829–31.  https://doi.org/10.1017/S0031182011001478.CrossRefPubMedGoogle Scholar
  53. Lopes AP, Dubey JP, Neto F, Rodrigues A, Martins T, Rodrigues M, Cardoso L. Seroprevalence of Toxoplasma gondii infection in cattle, sheep, goats and pigs from the north of Portugal for human consumption. Vet Parasitol. 2013;193:266–9.  https://doi.org/10.1016/j.vetpar.2012.12.001.CrossRefPubMedGoogle Scholar
  54. Mancianti F, Nardoni S, D'Ascenzi C, Pedonese F, Mugnaini L, Franco F, Papini R. Seroprevalence, detection of DNA in blood and milk, and genotyping of Toxoplasma gondii in a goat population in Italy. Biomed Res Int. 2013;2013:905326.  https://doi.org/10.1155/2013/905326.CrossRefPubMedPubMedCentralGoogle Scholar
  55. McAllister MM, McGuire AM, Jolley WR, Lindsay DS, Trees AJ, Stobart RH. Experimental neosporosis in pregnant ewes and their offspring. Vet Pathol. 1996;33:647–55.CrossRefGoogle Scholar
  56. Melo MB, Jensen KD, Saeij JP. Toxoplasma gondii effectors are master regulators of the inflammatory response. Trends Parasitol. 2011;27:487–95.  https://doi.org/10.1016/j.pt.2011.08.001.CrossRefPubMedPubMedCentralGoogle Scholar
  57. Miller CM, Boulter NR, Ikin RJ, Smith NC. The immunobiology of the innate response to Toxoplasma gondii. Int J Parasitol. 2009;39:23–39.  https://doi.org/10.1016/j.ijpara.2008.08.002.CrossRefPubMedGoogle Scholar
  58. Moré G, Basso W, Bacigalupe D, Venturini MC, Venturini L. Diagnosis of Sarcocystis cruzi, Neospora caninum, and Toxoplasma gondii infections in cattle. Parasitol Res. 2008;102:671–5.  https://doi.org/10.1007/s00436-007-0810-6.CrossRefPubMedGoogle Scholar
  59. Moré G, Pardini L, Basso W, Machuca M, Bacigalupe D, Villanueva MC, Schares G, Venturini MC, Venturini L. Toxoplasmosis and genotyping of Toxoplasma gondii in Macropus rufus and Macropus giganteus in Argentina. Vet Parasitol. 2010;169:57–61.  https://doi.org/10.1016/j.vetpar.2009.12.004.CrossRefPubMedGoogle Scholar
  60. Moré G, et al. Toxoplasma gondii infection in sentinel and free-range chickens from Argentina. Vet Parasitol. 2012;184:116–21.  https://doi.org/10.1016/j.vetpar.2011.09.012.CrossRefPubMedGoogle Scholar
  61. Ortega-Mora L, Gottstein B, Conraths F, Buxton D. Protozoal abortificients in farm ruminants. Guidelines for diagnosis and control. Wallingford: CABI; 2007.Google Scholar
  62. Pardini L, et al. Evaluation of an in-house TgSAG1 (P30) IgG ELISA for diagnosis of naturally acquired Toxoplasma gondii infection in pigs. Vet Parasitol. 2012;189:204–10.  https://doi.org/10.1016/j.vetpar.2012.04.014.CrossRefPubMedGoogle Scholar
  63. Pardini L, et al. Isolation and molecular characterization of Toxoplasma gondii in a colony of captive black-capped squirrel monkeys (Saimiri boliviensis). Parasitol Int. 2015;64:587–90.  https://doi.org/10.1016/j.parint.2015.08.009.CrossRefPubMedGoogle Scholar
  64. Pardini L, Moré G, Rudzinski M, Gos ML, Campero LM, Meyer A, Bernstein M, Unzaga JM, Venturini MC. Toxoplasma gondii isolates from chickens in an area with human toxoplasmic retinochoroiditis. Exp Parasitol. 2016;166:16–20.  https://doi.org/10.1016/j.exppara.2016.03.006.CrossRefPubMedGoogle Scholar
  65. Pena HF, Gennari SM, Dubey JP, Su C. Population structure and mouse-virulence of Toxoplasma gondii in Brazil. Int J Parasitol. 2008;38:561–9.  https://doi.org/10.1016/j.ijpara.2007.09.004.CrossRefPubMedGoogle Scholar
  66. Pollard AM, Onatolu KN, Hiller L, Haldar K, Knoll LJ. Highly polymorphic family of glycosylphosphatidylinositol-anchored surface antigens with evidence of developmental regulation in Toxoplasma gondii. Infect Immun. 2008;76:103–10.  https://doi.org/10.1128/IAI.01170-07.CrossRefPubMedGoogle Scholar
  67. Saadatnia G, Haj Ghani H, Khoo BY, Maimunah A, Rahmah N. Optimization of Toxoplasma gondii cultivation in VERO cell line. Trop Biomed. 2010;27:125–30.PubMedGoogle Scholar
  68. Saeij JP, Boyle JP, Coller S, Taylor S, Sibley LD, Brooke-Powell ET, Ajioka JW, Boothroyd JC. Polymorphic secreted kinases are key virulence factors in toxoplasmosis. Science. 2006;314:1780–3.  https://doi.org/10.1126/science.1133690.CrossRefPubMedPubMedCentralGoogle Scholar
  69. Schares G, Vrhovec MG, Pantchev N, Herrmann DC, Conraths FJ. Occurrence of Toxoplasma gondii and Hammondia hammondi oocysts in the faeces of cats from Germany and other European countries. Vet Parasitol. 2008;152:34–45.  https://doi.org/10.1016/j.vetpar.2007.12.004.CrossRefPubMedGoogle Scholar
  70. Schares G, Herrmann DC, Maksimov P, Matzkeit B, Conraths FJ, Moré G, Preisinger R, Weigend S. Chicken line-dependent mortality after experimental infection with three type IIxIII recombinant Toxoplasma gondii clones. Exp Parasitol. 2016;180:101–11.  https://doi.org/10.1016/j.exppara.2016.11.004.CrossRefPubMedGoogle Scholar
  71. Shwab EK, Zhu XQ, Majumdar D, Pena HF, Gennari SM, Dubey JP, Su C. Geographical patterns of Toxoplasma gondii genetic diversity revealed by multilocus PCR-RFLP genotyping. Parasitology. 2014;141:453–61.  https://doi.org/10.1017/S0031182013001844.CrossRefPubMedGoogle Scholar
  72. Sibley LD, Boothroyd JC. Virulent strains of Toxoplasma gondii comprise a single clonal lineage. Nature. 1992;359:82–5.  https://doi.org/10.1038/359082a0.CrossRefPubMedGoogle Scholar
  73. Spencer JA, Joiner KS, Hilton CD, Dubey JP, Toivio-Kinnucan M, Minc JK, Blagburn BL. Disseminated toxoplasmosis in a captive ring-tailed lemur (Lemur catta). J Parasitol. 2004;90:904–6.  https://doi.org/10.1645/GE-249R.CrossRefPubMedGoogle Scholar
  74. Stormoen M, Tharaldsen J, Hopp P. Seroprevalence of Toxoplasma gondii infection in Norwegian dairy goats. Acta Vet Scand. 2012;54:75.  https://doi.org/10.1186/1751-0147-54-75.CrossRefPubMedPubMedCentralGoogle Scholar
  75. Su C, Zhang X, Dubey JP. Genotyping of Toxoplasma gondii by multilocus PCR-RFLP markers: a high resolution and simple method for identification of parasites. Int J Parasitol. 2006;36:841–8.  https://doi.org/10.1016/j.ijpara.2006.03.003.CrossRefPubMedGoogle Scholar
  76. Su C, Shwab EK, Zhou P, Zhu XQ, Dubey JP. Moving towards an integrated approach to molecular detection and identification of Toxoplasma gondii. Parasitology. 2010;137:1–11.  https://doi.org/10.1017/S0031182009991065.CrossRefPubMedGoogle Scholar
  77. Su C, et al. 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;109:5844–9.  https://doi.org/10.1073/pnas.1203190109.CrossRefPubMedPubMedCentralGoogle Scholar
  78. Tait ED, Hunter CA. Advances in understanding immunity to Toxoplasma gondii. Mem Inst Oswaldo Cruz. 2009;104:201–10.CrossRefGoogle Scholar
  79. Tenter AM, Heckeroth AR, Weiss LM. Toxoplasma gondii: from animals to humans. Int J Parasitol. 2000;30:1217–58.CrossRefGoogle Scholar
  80. Tizard IR. Veterinary immunology and introduction. 8th ed. Barcelona: Elsevier; 2009.Google Scholar
  81. Tzanidakis N, Maksimov P, Conraths FJ, Kiossis E, Brozos C, Sotiraki S, Schares G. Toxoplasma gondii in sheep and goats: seroprevalence and potential risk factors under dairy husbandry practices. Vet Parasitol. 2012;190:340–8.  https://doi.org/10.1016/j.vetpar.2012.07.020.CrossRefPubMedGoogle Scholar
  82. Uggla A, Sjoland L, Dubey JP. Immunohistochemical diagnosis of toxoplasmosis in fetuses and fetal membranes of sheep. Am J Vet Res. 1987;48:348–51.PubMedGoogle Scholar
  83. Unzaga JM, Moré G, Bacigalupe D, Rambeaud M, Pardini L, Dellarupe A, De Felice L, Gos ML, Venturini MC. Toxoplasma gondii and Neospora caninum infections in goat abortions from Argentina. Parasitol Int. 2014;63:865–7.  https://doi.org/10.1016/j.parint.2014.07.009.CrossRefPubMedGoogle Scholar
  84. VanWormer E, Miller MA, Conrad PA, Grigg ME, Rejmanek D, Carpenter TE, Mazet JA. Using molecular epidemiology to track Toxoplasma gondii from terrestrial carnivores to marine hosts: implications for public health and conservation. PLoS Negl Trop Dis. 2014;8:e2852.  https://doi.org/10.1371/journal.pntd.0002852.CrossRefPubMedPubMedCentralGoogle Scholar
  85. Verma R, Khanna P. Development of Toxoplasma gondii vaccine: a global challenge. Hum Vaccin Immunother. 2013;9:291–3.CrossRefGoogle Scholar
  86. Wingstrand A, Lind P, Haugegaard J, Henriksen SA, Bille-Hansen V, Sorensen V. Clinical observations, pathology, bioassay in mice and serological response at slaughter in pigs experimentally infected with Toxoplasma gondii. Vet Parasitol. 1997;72:129–40.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Gastón Moré
    • 1
    • 2
  • Maria Cecilia Venturini
    • 1
  • Lais Pardini
    • 1
    • 2
  • Juan Manuel Unzaga
    • 1
  1. 1.Laboratory of Immunoparasitology (LAINPA), School of Veterinary SciencesNational University of La PlataLa PlataArgentina
  2. 2.National Council of Scientific and Technological Research (CONICET), CABABuenos AiresArgentina

Personalised recommendations