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Medicine » Infectious Diseases » "Toxoplasmosis - Recent Advances", book edited by Olgica Djurković Djaković, ISBN 978-953-51-0746-0, Published: September 12, 2012 under CC BY 3.0 license. © The Author(s).

Chapter 1

The Life Cycle of Toxoplasma gondii in the Natural Environment

By Emmanuelle Gilot-Fromont, Maud Lélu, Marie-Laure Dardé, Céline Richomme, Dominique Aubert, Eve Afonso, Aurélien Mercier, Cécile Gotteland and Isabelle Villena
DOI: 10.5772/48233

  1. Dubey JP (2010) Toxoplasmosis of animals and humans, second edition. Boca Raton: CRC Press. 313 p.

  2. Tenter AM, Heckeroth AR, Weiss LM (2000) Toxoplasma gondii: from animals to humans. Int. j. parasitol. 30: 1217-1258.

  3. Miller MA, Miller WA, Conrad PA, James ER, Melli AC, Leutenegger CM, Dabritz HA, Packham AE, Paradies D, Harris M, Ames J, Jessup DA, Worcester K, Grigg ME (2008) Type X Toxoplasma gondii in a wild mussel and terrestrial carnivores from coastal California: new linkages between terrestrial mammals, runoff and toxoplamosis of sea otters. Int. j. parasitol 58: 928-937.

  4. Deplazes P, Hegglin D, Gloor S, Romig T (2004) Wilderness in the city: the urbanization of Echinococcus multilocularis. Trends parasitol 20 : 77-84.

  5. House PK, Vyas A, Sapolsky R (2011) Predator cat odors activate sexual arousal pathways in brains of Toxoplasma gondii infected rats. PLoS ONE 6: e23277.

  6. Dass SAH, Vasudevan A, Dutta D, Soh LJT, Salposky RM, Vyas A (2011) Protozoan parasite Toxoplasma gondii manipulates mate choice in rats by enhancing attractiveness of males. PLoS ONE 6: e27229.

  7. Cook AJC, Gilbert RE, Buffolano W, Zufferey J, Petersen E, Jenum PA, Foulon W, Semprini AE, Dunn DT (2000) Sources of Toxoplasma infection in pregnant women: European multicentre case-control study. Br. med. j. 321: 142-147.

  8. Beverly JKA (1959) Congenital transmission of toxoplasmosis through successive generations of mice. Nature 183: 1348-1349.

  9. Dubey JP (2006) Comparative infectivity of oocysts and bradyzoites of Toxoplasma gondii for intermediate (mice) and definitive (cats) hosts. Vet. parasitol. 140: 69-75.

  10. Lélu M, Langlais M, Poulle ML, Gilot-Fromont E (2010) Transmission dynamics of Toxoplasma gondii along an urban-rural gradient. Theor. popul. biol. 78: 139–147.

  11. Berenreiterova M, Flegr J, Kubena AA, Nemec P (2011) The Distribution of Toxoplasma gondii Cysts in the Brain of a Mouse with Latent Toxoplasmosis: Implications for the Behavioral Manipulation Hypothesis. PLoS One 6: e28925.

  12. Pappas G, Roussos N, Falagas ME (2009) Toxoplasmosis snapshots: Global status of Toxoplasma gondii seroprevalence and implications for pregnancy and congenital toxoplasmosis. Int. j. parasitol. 39: 1385-1394.

  13. Berger F, Goulet V, Le Strat Y, Desenclos JC (2008) Toxoplasmose chez les femmes enceintes en France : évolution de la séroprévalence et de l’incidence et facteurs associés, 1995-2003. Bulletin Epidemiologique Hebdomadaire 14-15: 117-121.

  14. Gilot-Fromont E, Riche B, Rabilloud M (2009) Seroprevalence of Toxoplasma gondii in a rural population in France: detection of a household effect. BMC infect. dis. 9: 76.

  15. Haydon DT, Cleaveland S, Taylor LH, Laurenson K (2002) Identifying Reservoirs of Infection: A Conceptual and Practical Challenge. Emerg. infect. dis. 8: 1468-1473.

  16. Turner DC, Bateson PB (2000) The Domestic cat: the biology of its behaviour. Cambridge University Press.

  17. Macdonald DW (1983) The ecology of carnivore social behaviour. Nature 301: 379-384.

  18. Page RJC, Ross J, Bennett DH (1993) Home ranges of feral cats at Avonmouth Docks (United Kingdom). Rev. sci. tech. OIE 12: 23-26.

  19. Calhoon RE, Haspel C (1989) Urban cat populations compared by season, subhabitat and supplemental feeding. J. anim. ecol. 58: 321-328.

  20. Liberg O (1980) Spacing pattern in a population of rural free-roaming domestic cats. Oikos 35: 336-349.

  21. Pontier D, Rioux N, Heizmann A (1995) Evidence of selection on the orange allele in the domestic cat Felis catus: the role of social structure. Oikos 73: 299-308.

  22. Fromont E, Artois M, Pontier D (1998) Epidemiology of feline leukemia virus (FeLV) and structure of domestic cat populations. J. wildl. manage. 62: 978-988.

  23. Liberg O (1981) Predation and social behaviour in a population of domestic cats. An evolutionary perspective. Ph. D. Thesis, Univ. Lund (Sweden), 135 p.

  24. Liberg O (1984) Food habits and prey impact by feral and house-based domestic cats in a rural area in southern Sweden. J. mammal. 65: 424-432.

  25. Say L, Gaillard JM, Pontier D. (2002) Spatiotemporal variation in cat population density in a sub-Antarctic environment. Polar biol. 25: 90–95.

  26. Say L, Devillard S, Natoli E, Pontier D (2002) The mating system of feral cats (Felis catus L.) in a sub-Antarctic environment. Polar biol. 25: 838–842.

  27. Le Louarn H, Quéré JP (2003) Les Rongeurs de France. Faunistique et biologie. INRA éditions, Paris, 256pp.

  28. Dickman CR, Doncaster CP (1987) The Ecology of Small Mammals in Urban Habitats. I. Populations in a Patchy Environment. J. anim. ecol. 56: 629-640.

  29. Baker PJ, Ansell RJ, Dodds PAA, Webber CE, Harris S (2003) Factors affecting the distribution of small mammals in an urban area. Mammal rev. 33: 95-100.

  30. Dubey JP, Saville WJA, Stanek J, Reed SM (2002) Prevalence of Toxoplasma gondii antibodies in domestic cats From rural Ohio. J. parasitol. 88: 802-803.

  31. Miró G, Montoya A, Jimenez S, Frisuelos C, Mateo M, Fuentes I (2004) Prevalence of antibodies to Toxoplasma gondii and intestinal parasites in stray, farm and household cats in Spain. Vet. parasitol. 126: 249-255.

  32. Afonso E, Thulliez P, Gilot-Fromont E (2010) Local meteorological conditions, dynamics of seroconversion to Toxoplasma gondii in cats (Felis catus) and oocyst burden in a rural environment. Epidemiol. infect. 138: 1105–1113.

  33. Wu SM, Zhu XQ, Zhou DH, Fu BQ, Chen J, Yang JF, Song HQ, Weng YB, Ye DH (2011) Seroprevalence of Toxoplasma gondii infection in household and stray cats in Lanzhou, northwest China. Parasites & Vectors 4: 214-218.

  34. Zhang H, Zhou DH, Zhou P, Lun ZR, Chen XG, Lin RQ, Yuan ZG, Zhu XQ (2009) Seroprevalence of Toxoplasma gondii infection in stray and household cats in Guangzhou, China. Zoonoses public health 56: 502-505.

  35. Barratt DG (1998) Predation by house cats, Felis catus (L.), in Canberra, Australia. II. Factors affecting the amount of prey caught and estimates of the impact on wildlife. Wildlife res. 25: 475-487.

  36. Baker PJ, Bentley AJ, Ansell RJ, Harris S (2005) Impact of predation by domestic cats Felis catus in an urban area. Mammal rev. 35: 302-312.

  37. Woods M, McDonald RA, Harris S (2003) Predation of wildlife by domestic cats Felis catus in Great Britain. Mammal rev. 33: 174–188.

  38. Gillies C, Clout M (2003) The prey of domestic cats (Felis catus) in two suburbs of Auckland City, New Zealand J. zool. 259: 309-315.

  39. Kays RW, DeWan AA (2004) Ecological impact of inside/outside house cats around a suburban nature reserve. Anim. conserv. 7: 273-283.

  40. Rosenthal BM (2009) How has agriculture influenced the geography and genetics of animal parasites? Trends parasitol. 25: 67-70.

  41. Afonso E, Thulliez P, Gilot-Fromont E (2006) Transmission of Toxoplasma gondii in an urban population of domestic cats (Felis catus). Int. j. parasitol. 36: 1373-1382.

  42. Hornok S, Edelhofer R, Joachim A, Farkas R, Berta K, Repasi A, Lakatos B (2008) Seroprevalence of Toxoplasma gondii and Neospora caninum infection of cats in Hungary. Acta vet. hung. 56: 81-88.

  43. Lee SE, Kim NH, Chae HS, Cho SH, Nam HW, Lee WJ, Kim SH, Lee JH (2011) Prevalence of Toxoplasma gondii infection in feral cats in Seoul, Korea. J. parasitol. 97, 153-155.

  44. Dubey JP, Weigel RM, Siegel AM, Thuilliez P, Kitron UD, Mitchell MA, Mannelli A, Mateus-Pinilla NE, Shen SK, Kwok OCH, Todd KS (1995) Sources and reservoirs of Toxoplasma gondii infection on 47 swine farms in Illinois. J. parasitol. 81: 723-729.

  45. Cavalcante GT, Aguiar DM, Chiebao D, Dubey JP, Ruiz VLA, Dias RA, Camargo LMA, Labruna MB, Gennari SM (2006) Seroprevalence of Toxoplasma gondii antibodies in cats and pigs from rural Western Amazon, Brazil. J. parasitol. 92: 863-864.

  46. Afonso E, Thulliez P, Pontier D, Gilot-Fromont E (2007) Toxoplasmosis in prey species and consequences for prevalence in feral cats: not all prey species are equal. Parasitology 134: 1963-1971.

  47. Dabritz HA, Miller MA, Gadner IA, Packham AE, Atwill ER, Conrad PA (2008) Risk factors for Toxoplasma gondii infection in wild rodents from central coastal California and a review of T. gondii prevalence in rodents. J. parasitol. 94: 675–683.

  48. Genchi G, Polidori GA, Zaghini L, Lanfranchi P (1991) Aspetti epidemiologici della toxoplasmosi nell’allevamento intensivo del suino. Arch. vet. ital. 42, 105–111.

  49. Marshall PA, Hughes JM, Williams RH, Smith JE, Murphy RG, Hide G (2004) Detection of high levels of congenital transmission of Toxoplasma gondii in natural urban populations of Mus domesticus. Parasitology 128: 39-42.

  50. Afonso E, Lemoine M, Poulle ML, Ravat MC, Romand S, Thulliez P, Villena I, Aubert D, Riche B, Rabilloud M, Gilot-Fromont E (2008) Spatial distribution of soil contamination by Toxoplasma gondii in relation to cat defecation behaviour in an urban area. Int. j. parasitol. 38: 1017-1023.

  51. Dabritz HA, Miller, Atwill ER, Gardner IA, Leutenegger CM, Melli AC, Conrad PA (2007) Detection of Toxoplasma gondii-like oocysts in cat feces and estimates of the environmental oocyst burden. J. am. vet. med. assoc. 231: 1676–1684.

  52. Dabritz HA, Atwill ER, Gardner IA, Miller MA, Conrad PA (2006) Outdoor fecal deposition by free-roaming cats and attitudes of cat owners and nonowners toward stray pets, wildlife, and water pollution. J. am. vet. med. assoc. 229: 74-81.

  53. Forman RTT, Godron M (1986) Landscape ecology. Wiley and Sons, New York, USA.

  54. McKinney ML (2002) Urbanization, biodiversity, and conservation. BioScience 52: 883-890.

  55. Bradley CA, Altizer S (2007) Urbanization and the ecology of wildlife diseases. Trends ecol. evol. 22: 95-102.

  56. Zaunbrecher KI, Smith RE (1993) Neutering of feral cats as an alternative to eradication programs. J. am. vet. med. assoc. 203: 449-452.

  57. Neville PF, Remfry J (1984) Effect of neutering on two groups of feral cats. Vet. rec. 114: 447-450.

  58. Natoli E (1985) Spacing pattern in a colony of urban stray cats (Felis catus L.) in the historic centre of Rome. Appl. anim. behav. sci. 14: 289-304.

  59. Haspel C, Calhoon RE (1989) Home ranges of free ranging cats (Felis catus) in Brooklyn, New York. Can. j. zool. 67: 178-181.

  60. Salant H, Spira DT (2004) A cross-sectional survey of anti-Toxoplasma gondii antibodies in Jerusalem cats. Vet. parasitol. 124: 167-177.

  61. Jittapalapong S, Nimsupan B, Pinyopanuwat N., Chimnoi W, Kabeya H, Maruyama S (2006) Seroprevalence of Toxoplasma gondii antibodies in stray cats and dogs in the Bangkok metropolitan area, Thailand. Vet. parasitol. 145: 138-141.

  62. Pena HJF, Soares RM, Amaku M, Dubey JP, Gennari SM (2006) Toxoplasma gondii infection in cats from Saõ Paulo state, Brazil: seroprevalence, oocyst shedding, isolation in mice, and biologic and molecular characterization. Res. vet. sci. 81: 58-67.

  63. Gauss CBL, Almeria S, Ortuno A, Garcia F, Dubey JP (2003) Seroprevalence of Toxoplasma gondii Antibodies in Domestic Cats from Barcelona, Spain. J. parasitol. 89: 1067-1068.

  64. Dorny P, Speybroeck N, Verstraete S, Baeke M, De Becker A, Berkvens D, Vercruysse J (2002) Serological survey of Toxoplasma gondii, feline immunodeficiency virus and feline leukaemia virus in urban stray cats in Belgium. Vet. rec. 151: 626-629.

  65. Corbett LK (1979) Feeding ecology and social organization of wildcats (Felis silvetris) and domestic cats (Felis catus) in Scotland. Scotland: University of Aberdeen.

  66. Uga S, Minami T, Nagata K (1996) Defecation habits of cats and dogs and contamination by Toxocara eggs in public park sandpits. Am. j. trop. med. hyg. 54: 122-126.

  67. Lass A, Pietkiewicz H, Modzelewska E, Dumètre A, Szostakowska B, Myjak P (2009) Detection of Toxoplasma gondii oocysts in environmental soil samples using molecular methods. Eur. j. clin. microbiol. Infect. dis. 28: 599-605.

  68. Du F, Feng HL, Nie H, Tu P, Zhang QL, Hu M, Zhou YQ, Zhao JL (2012) Survey on the contamination of Toxoplasma gondii oocysts in the soil of public parks of Wuhan, China. Vet. parasitol. 184: 141-146.

  69. Bobić B, Jevremović I, Marinković J, Šibalić D, Djurković-Djaković O (1998) Risk factors for Toxoplasma infection in a reproductive age female population in the area of Belgrade, Yugoslavia. Eur. j. epidemiol. 14: 605-610.

  70. Kortbeek LM, De Melker HE, Veldhuijzen IK, Conyn-Van Spaendonck MAE (2004) Population-based Toxoplasma seroprevalence study in the Netherlands. Epidemiol. infect. 132: 839-845.

  71. Frenkel JK, Hassanein KL, Hassanein RS, Brown E, Thulliez P, Quintero-Nunez R (1995) Transmission of Toxoplasma gondii in Panama city, Panama: A five-year prospective cohort study of children, cats, rodents, birds, and soil. Am. j. trop. med. hyg. 53: 458-468.

  72. Lehmann T, Graham DH, Dahl E, Sreekumar C, Launer F, Corn JL, Gamble HR, Dubey JP (2003) Transmission dynamics of Toxoplasma gondii on a pig farm. Infect. genet. evol. 3: 135–141.

  73. Gauss CB, Dubey JP, Vidal D, Cabezon O, Ruiz-Fons F, Vicente J, Marco I, Lavin S, Gortazar C, Almería S (2006) Prevalence of Toxoplasma gondii antibodies in red deer (Cervus elaphus) and other wild ruminants from Spain. Vet. parasitol. 136: 193-200.

  74. Malmsten J, Jakubek EB, Bjorkman C (2011) Prevalence of antibodies against Toxoplasma gondii and Neospora caninum in moose (Alces alces) and roe deer (Capreolus capreolus) in Sweden. Vet. parasitol. 177: 275-280.

  75. Williamson JMW, Williams H (1980) Toxoplasmosis in farmed red deer (Cervus elaphus) in Scotland. Res. vet. sci. 29: 36–40.

  76. Simon A, Chambellant M, Ward BJ, Simard M, Proulx JF, Levesque B, Bigras-Poulin M, Rousseau AN, Ogden NH (2011) Spatio-temporal variations and age effect on Toxoplasma gondii seroprevalence in seals from the Canadian Arctic. Parasitology 138: 1-7.

  77. Tizard IR, Fish NA, Quinn JP (1976) Some observations on the epidemiology of toxoplasmosis in Canada. J. hyg. Camb. 77: 11–21.

  78. Gotteland C, Aubert A, Gilbert P, Moinet M, Klein F, Villena I, Game Y, Gilot-Fromont E (submitted) Toxoplasma gondii in natural populations of Ungulates in France : prevalence and spatio-temporal variations.

  79. Dumètre A, Dardé ML (2003) How to detect Toxoplasma gondii oocysts in environmental samples? FEMS microbiol. rev. 27: 651-661.

  80. Davies, CM, Altavilla N, Krogh M, Ferguson CM, Deere DA, Ashbolt NJ (2005) Environmental inactivation of Cryptosporidium oocysts in catchment soils. J. appl. microbiol. 98: 308-317.

  81. Langkjær M, Roepstorff A (2008) Survival of Isospora suis oocysts under controlled environmental conditions. Vet. parasitol. 152: 186-193.

  82. Frenkel JK, Ruiz A, Chinchilla M (1975) Soil survival of Toxoplasma oocysts in Kansas and Costa Rica. Am. j. trop. med. hyg. 24: 439–443.

  83. Lélu M, Villena I, Dardé ML, Aubert D, Geers R, Dupuis E, Marnef F, Poulle ML, Gotteland C, Dumètre A, Gilot-Fromont E (2012) Quantitative assessment of the survival of Toxoplasma gondii oocysts in soil. Appl. env. microbiol. doi: 10.1128/AEM.00246-12.

  84. Stenseth NC,Viljugrein H, Jedrejewski W, Mysterud A, Pucek Z (2002) Population dynamics of Clethrionomys glareolus and Apodemus flavicollis : seasonal components of density dependence and density independence. Acta theriol. 47 (Suppl. 1): 39–67.

  85. Tizard R, Harmeson J, Lai CH (1978) The Prevalence of Serum Antibodies to Toxoplasma gondii in Ontario Mammals. Can. j. comp. med. 42: 177-183.

  86. Bobić B, Klun I, Nikolić A, Nikolić A, Vujanić M, Zivković T, Ivović V, Djurković-Djakovic O (2010) Seasonal variations in human Toxoplasma infection in Serbia. Vector borne zoonotic dis. 10: 465–469.

  87. Herrmann DC, Pantchev N, Vrhovec MG, Barutzki D, Wilking H, Fröhlich A, Lüder CG, Conraths FJ, Schares G (2010) Atypical Toxoplasma gondii genotypes identified in oocysts shed by cats in Germany. Int. j. parasitol. 40: 285-292.

  88. Klun I, Djurkovic-Djakovic O, Katic-Radivojevic S, Nikolic A (2006) Cross-sectional survey on Toxoplasma gondii infection in cattle, sheep and pigs in Serbia: seroprevalence and risk factors. Vet. parasitol. 135: 121–131.

  89. Panadero R, Painceira A, López C, Vázquez L, Paz A, Díaz P, Dacal V, Cienfuegos S, Fernández G, Lago N, Díez-Baños P, Morrondo P (2010) Seroprevalence of Toxoplasma gondii and Neospora caninum in wild and domestic ruminants sharing pastures in Galicia (Northwest Spain). Res. vet. sci 88: 111–115.

  90. Beral M, Rossi S, Aubert D, Gasqui P, Terrier ME, Klein F, Geers R, Abrial D, Gilot-Fromont E, Richomme C, Hars J, Jourdain E (submitted) Environmental factors associated with the seroprevalence of Toxoplasma gondii in wild boar (Sus scrofa), France.

  91. Richomme C, Afonso E, Tolon V, Ducrot C, Halos L, Alliot A, Perret C, Thomas M, Boireau P, Gilot-Fromont E (2010) Risk factors for Toxoplasma gondii infection in wild boar from the Mediterranean island of Corsica. Epidemiol. infect. 138: 1257–1266.

  92. Langlais M, Lélu M, Avenet C, Gilot-Fromont E (2012) A simplified model system for Toxoplasma gondii spread within a heterogeneous environment. Nonlinear Dynamics, doi: 10.1007/s11071-011-0255-4.

  93. Lopes WDZ, dos Santos TR, dos Santos da Silva R, Rossanese WM, de Souza FA, D’Ark de Faria Rodrigues J, Paranhos de Mendonça R, Soares VE, da Costa AJ (2010) Seroprevalence of and risk factors for Toxoplasma gondii in sheep raised in the Jaboticabal, microregion, São Paulo State, Brazil. Res. vet. sci 161: 324-326.

  94. Mainar RC, de la Cruz C, Asencio A, Dominguez L, Vazquez-Boland IA (1996) Prevalence of agglutination antibodies to Toxolasma gondii in small ruminants of the Madrid region, Spain, and identification of factors influencing seropositivity by multivariate analysis. Vet. res. com. 20: 153-159.

  95. Mateus-Pinilla NE, Hannon B, Weigel M (2002) A computer simulation of the prevention of the transmission of Toxoplasma gondii on swine farms using a feline T-gondii vaccine. Prev. vet. med. 55: 17–36.

  96. Kijlstra A, Jongert E (2008) Control of the risk of human toxoplasmosis transmitted by meat. Int. j. parasitol. 38: 1359–1370.

  97. Gilot-Fromont E, Aubert D, Belkilani S, Hermitte P, Gibout O, Geers R, Villena I (2009) Landscape, herd management and within-herd seroprevalence of Toxoplasma gondii in beef cattle herds from Champagne-Ardenne, France. Vet. parasitol. 161: 36-40.

  98. Hill DE, Chirukandoth S, Dubey JP (2005) Biology and epidemiology of Toxoplasma gondii in man and animals. Anim. health res. rev. 6: 41-61.

  99. Cabezón O, García-Bocanegra I, Molina-López R, Marco I, Blanco JM, Höfle U, Margalida A, Bach-Raich E, Darwich L, Echeverría I, Obón E, Hernández M, Lavín S, Dubey JP, Almería S (2011) Seropositivity and risk factors associated with Toxoplasma gondii infection in wild birds from Spain. PloS ONE 6: 1–7.

  100. Sobrino R, Cabezón O, Millán J, Pabón M, Arnal MC, Luco DF, Gortázar C, Dubey JP, Almería S (2007) Seroprevalence of Toxoplasma gondii antibodies in wild carnivores from Spain. Vet. parasitol. 148: 187-192.

  101. García-Bocanegra I, Dubey JP, Martínez F, Vargas A, Cabezón O, Zorrilla I, Arenas A, Almería S (2010). Factors affecting seroprevalence of Toxoplasma gondii in the endangered Iberian lynx (Lynx pardinus). Vet. parasitol. 167: 36-42.

  102. Degen AA, Kam M, Khokhlova IS, Krasnov BR, Barraclough TG (1998) Average daily metabolic rate of rodents: habitat and dietary comparisons. Funct. ecol. 12: 63–73.

  103. Speakman JR (2005) Body size, energy metabolism and lifespan. J. exp. biol. 208: 1717–1730.

  104. Ottaviani D, Cairns SC, Oliverio M, Boitani L (2006) Body mass as a predictive variable of homerange size among Italian mammals and birds. J. zool. 269: 317–330.

  105. Ruiz A, Frenkel JK (1980) Intermediate and transport hosts of Toxoplasma gondii in Costa Rica. Am. J. trop. med. hyg. 29: 1161–1166.

  106. Lindsay DS, Phelps KK, Smith SA, Flick G, Sumner SS, Dubey JP (2001) Removal of Toxoplasma gondii oocysts from seawater by Eastern oysters (Crassostrea virginica). J eukariot. microbiol. 48: S197-S198.

  107. Putignani L, Mancinelli L, Del Chierico F, Menichella D, Adlerstein D, Angelici MC, Marangi N, Berrilli F, Caffara M, di Regalbono A (2011) Investigation of Toxoplasma gondii presence in farmed shellfish by nested PCR and real-time PCR fluorescent amplicon generation assay (FLAG). Exp. parasitol 127: 409-417.

  108. Dubey JP (2004) Toxoplasmosis - a waterborne zoonosis. Vet. parasitol. 126: 57-72.

  109. Bollo E, Pregel P, Gennero S, Pizzoni E, Rosati S, Nebbia P, Biolatti B (2003) Health status of a population of nutria (Myocastor coypus) living in a protected area in Italy. Res. vet. sci. 75: 21-25.

  110. Nardoni S, Angelici MC, Mugnaini L, Mancianti F (2011). Prevalence of Toxoplasma gondii infection in Myocastor coypus in a protected Italian wetland. Parasite and Vectors 23: 240-243.

  111. Almeria S, Calvete C, Pages A, Gauss CBL, Dubey, JP (2004). Factors affecting the seroprevalence of Toxoplasma gondii infection in wild rabbits (Oryctolagus cuniculus) from Spain. Vet. parasitol. 123: 265–270.

  112. Gamarra JA, Cabezón O, Pabón M, Arnal MC, Luco DF, Dubey JP, Gortázar C, Almería S (2008) Prevalence of antibodies against Toxoplasma gondii in roe deer from Spain. Vet. parasitol. 153: 152–156.

  113. Germain E, Benhamou S, Poulle ML (2008) Spatio-temporal sharing between the European wildcat, the domestic cat and their hybrids. J. zool. 276: 195–203.

  114. Jokelainen P, Isomursu M, Näreaho A, Oksanen A (2011) Natural Toxoplasma gondii infections in European brown hares and mountain hares in Finland: proportional mortality rate, antibody prevalence, and genetic characterization. J. wildl. dis. 47: 154–163.

  115. Jokelainen P, Näreaho A, Knaapi S, Oksanen A, Rikula U, Sukura A (2010) Toxoplasma gondii in wild cervids and sheep in Finland: north-south gradient in seroprevalence. Vet. parasitol. 171: 331-336.

  116. Sepúlveda MA, Muñoz-Zanzi C, Rosenfeld C, Jara R, Pelican KM, Hill D (2011) Toxoplasma gondii in feral American minks at the Maullín river, Chile. Vet. parasitol. 175: 60–65.

  117. Stieve E, Beckmen K, Kania SA, Widner A, Patton S (2010) Neospora caninum and Toxoplasma gondii antibody prevalence in Alaska wildlife. J. wildl. dis. 46: 348-355.

  118. Vikoren T, Tharaldsen J, Fredriksen B, Handeland K (2004) Prevalence of Toxoplasma gondii antibodies in wild red deer, roe deer, moose, and reindeer from Norway. Vet. parasitol. 120: 159-169.

  119. Zarnke RL, Dubey JP, Kwok OC, Ver Hoef JM (2000) Serologic survey for Toxoplasma gondii in selected wildlife species from Alaska. J. wildl. dis. 36: 219-224.

  120. Miller MA, Miller WA, Conrad PA, James ER, Melli AC, Leutenegger CM, Dabritz HA, Packham AE, Paradies D, Harris M, Ames J, Jessup DA, Worcester K, Grigg ME (2008) Type X Toxoplasma gondii in a wild mussel and terrestrial carnivores from coastal California: New linkages between terrestrial mammals, runoff and toxoplasmosis of sea otters. Int. j. parasitol. 38: 1319–1328.

  121. Massie GN, Ware MW, Villegas EN, Black MW (2010) Uptake and transmission of Toxoplasma gondii oocysts by migratory, filter-feeding fish. Vet. parasitol. 169: 296-303.

  122. Prestrud KW, Asbakk K, Fuglei E, Mørk T, Stien A, Ropstad E, Tryland M, Gabrielsen GW, Lydersen C, Kovacs KM, Loonen MJ, Sagerup K, Oksanen A (2007) Serosurvey for Toxoplasma gondii in arctic foxes and possible sources of infection in the high Arctic of Svalbard. Vet parasitol. 150: 6-12.

  123. Prestrud KW, Asbakk K, Mørk T, Fuglei E, Tryland M, Su C (2008) Direct high-resolution genotyping of Toxoplasma gondii in arctic foxes (Vulpes lagopus) in the remote arctic Svalbard archipelago reveals widespread clonal Type II lineage. Vet parasitol. 158: 121-128.

  124. Maubon D, Ajzenberg D, Brenier-Pinchart MP, Dardé ML, Pelloux H (2008) What are the respective host and parasite contributions to toxoplasmosis? Trends parasitol. 24: 299–303.

  125. Innes EA (1997) Toxoplasmosis: comparative species susceptibility and host immune response. Comp. immunol. microbiol. infect. dis. 20: 131-138.

  126. Shimizu K (1958) Studies on toxoplasmosis I: An outbreak of toxoplasmosis among hares (Lepus timidus ainu) in Sapporo. Jap. j. vet. res. 6: 157–166.

  127. Gustafsson K, Järplid B (1997) Toxoplasma gondii infection in the mountain hare (Lepus timidus) and domestic rabbit (Oryctolagus cuniculus). I. Pathology. J. comp. pathol. 117: 351–360.

  128. Gustafsson K, Wattrang E, Fossum C, Heegaard PMH, Lind P, Uggla A (1997) Toxoplasma gondii infection in the mountain hare (Lepus timidus) and domestic rabbit (Oryctolagus cuniculus). II. Early immune reactions. J. comp. pathol. 117: 361–369.

  129. Sedlak K, Literak I, Faldyna M, Toman M, Benak J (2000) Fatal toxoplasmosis in brown hares (Lepus europaeus): Possible reasons of their high susceptibility to the infection. Vet. parasitol. 93: 13–28.

  130. Kenny DE, Lappin MR, Knightly F, Baler J, Brewer M, Getzy DM (2002) Toxoplasmosis in Pallas' cats (Otocolobus felis manul) at the Denver Zoological Gardens. J. zoo wildl. med. 33: 131-138.

  131. Basso W, Edelhofer R, Zenker W, Möstl K, Kübber-Heiss A, Prosl H (2005) Toxoplasmosis in Pallas' cats (Otocolobus manul) raised in captivity. Parasitology 130: 293-299. Erratum in: Parasitology 130: 586.

  132. Brown M, Lappin MR, Brown JL, Munkhtsog B, Swanson WF (2005) Exploring the ecologic basis for extreme susceptibility of Pallas' cats (Otocolobus manul) to fatal toxoplasmosis. J wildl dis. 41: 691-700.

  133. Convention on international trade in threatened species (2001) Checklist of CITES species Convention on International Trade in Threatened Species, Geneva, Switzerland, http://www.felineconservation.org/feline_species/pallas__cat.htm.

  134. Ajzenberg D, Bañuls AL, Tibayrenc M, Dardé ML (2002) Microsatellite analysis of Toxoplasma gondii shows considerable polymorphism structured into two main clonal groups. Int j. parasitol. 32:27-38.

  135. Su C, Khan A, Zhou P, Majumdar D, Ajzenberg D, Dardé ML, Xing-Quan Zhu XQ, Ajioka JW, Rosenthal BM, Dubey JP, Sibley LD (2012) Globally diverse Toxoplasma gondii isolates comprise six major clades originating from a small number of distinct ancestral lineages. Proc. nat. acad. sci. doi: 10.1073/pnas.1203190109.

  136. Ajzenberg D, Collinet F, Mercier A, Vignoles P, Dardé ML (2010) Genotyping of Toxoplasma gondii isolates with 15 microsatellite markers in a single multiplex PCR assay. J. clin. microbiol. 48: 4641-4645.

  137. De Craeye S, Speybroeck N, Ajzenberg D, Dardé ML, Collinet F, Tavernier P, Van Gucht S, Dorny P, Dierick K (2010) Toxoplasma gondii and Neospora caninum in wildlife: common parasites in Belgian foxes and Cervidae? Vet. parasitol. 178: 64-69.

  138. Richomme C, Aubert D, Gilot-Fromont E, Ajzenberg D, Mercier A, Ducrot C, Ferté H, Delorme D, Villena I (2009) Genetic characterization of Toxoplasma gondii from wild boar (Sus scrofa) in France. Vet. parasitol. 164: 296–300.

  139. Aubert D, Ajzenberg D, Richomme C, Gilot-Fromont E, Terrier ME, de Gevigney C, Game Y, Maillard D, Gibert P, Dardé ML, Villena I (2010) Molecular and biological characteristics of Toxoplasma gondii isolates from wildlife in France. Vet. parasitol. 171: 346-349.

  140. Aubert D, Terrier ME, Dumètre A, Barrat J, Villena I (2008) Prevalence of Toxoplasma gondii in raptors from France. J. wildl. dis. 44: 172-173.

  141. Jokelainen P, Isomursu M, Nareaho A, Oksanen A (2010) Toxoplasma gondii killing European brown hares and mountain hares in Finland: Proportional mortality rate, seroprevalence, and genetic characterization. 9th Biennial Conference of the European Wildlife, Association, Vlieland, The Netherlands, 13 to 16 September 2010.

  142. Su C, Zhang X, Dubey JP (2006) Genotyping of Toxoplasma gondii by multilocus PCR-RFLP markers: a high resolution and simple method for identification of parasites. Int. j. parasitol. 36: 841-848.

  143. Aspinall TV, Marlee D, Hyde JE, Sims PF (2002) Prevalence of Toxoplasma gondii in commercial meat products as monitored by polymerase chain reaction - food for thought? Int. j. parasitol. 32: 1193-1199.

  144. Dumètre A, Ajzenberg D, Rozette L, Mercier A, Dardé ML (2006) Toxoplasma gondii infection in sheep from Haute-Vienne, France: seroprevalence and isolate genotyping by microsatellite analysis. Vet. parasitol. 142: 376-379.

  145. Halos L, Thébault A, Aubert D, Thomas M, Perret C, Geers R, Alliot A, Escotte-Binet S, Ajzenberg D, Dardé ML, Durand B, Boireau P, Villena I (2010) An innovative survey underlining the significant level of contamination by Toxoplasma gondii of ovine meat consumed in France. Int. j. parasitol. 40: 193-200.

  146. Owen MR, Trees AJ (1999) Genotyping of Toxoplasma gondii associated with abortion in sheep. J parasitol. 85: 382-384.

  147. Jungersen G, Jensen L, Rask MR, Lind P (2002) Non-lethal infection parameters in mice separate sheep Type II Toxoplasma gondii isolates by virulence. Comp. immunol. microbiol. infect. dis. 25: 187-195.

  148. Dubey JP, Velmurugan GV, Rajendran C, Yabsley MJ, Thomas NJ, Beckmen KB, Sinnett D, Ruid D, Hart J, Fair PA, McFee WE, Shearn-Bochsler V, Kwok OC, Ferreira LR, Choudhary S, Faria EB, Zhou H, Felix TA, Su C (2011) Genetic characterisation of Toxoplasma gondii in wildlife from North America revealed widespread and high prevalence of the fourth clonal type. Int. j. parasitol. 41: 1139-1147.

  149. Wendte JM, Gibson AK, Grigg ME (2011) Population genetics of Toxoplasma gondii: new perspectives from parasite genotypes in wildlife. Vet. parasitol. 182: 96-111.

  150. Smith DD, Frenkel JK (1995) Prevalence of antibodies to Toxoplasma gondii in wild mammals of Missouri and east central Kansas: biologic and ecologic considerations of transmission. J. wildl. dis. 31: 15-21.

  151. de Thoisy B, Demar M, Aznar C, Carme B (2003) Ecologic correlates of Toxoplasma gondii exposure in free-ranging neotropical mammals. J. wildl. dis. 39: 456-459.

  152. Santos PS, Albuquerque GR, da Silva VM, Martin AR, Marvulo MF, Souza SL, Ragozo AM, Nascimento CC, Gennari SM, Dubey JP, Silva JC. (2011) Seroprevalence of Toxoplasma gondii in free-living Amazon River dolphins (Inia geoffrensis) from central Amazon, Brazil. Vet. parasitol. 29: 171-173.

  153. Sobral CA, Amendoeira MR, Teva A, Patel BN, Klein CH (2005) Seroprevalence of infection with Toxoplasma gondii in indigenous Brazilian populations. Am. j. trop. med. hyg. 72: 37-41.

  154. Berengo A, Pampiglione S, De Lalla F (1974) Serological studies on toxoplasmosis in some groups of Babiga Pygmies in Central Africa. Riv. parassitol. 35: 81-86.

  155. Johnson WE, Eizirik E, Pecon-Slattery J, Murphy WJ, Antunes A, Teeling E, O'Brien SJ (2006) The late Miocene radiation of modern Felidae: a genetic assessment. Science 311: 73-77.

  156. IUCN SSC Group CS (1996) Cat Website. Available: http://lynx.uio.no/lynx/catsgportal/cat-website/20_cat-website/home/index_en.htm. 02.04.2012.

  157. Elmore SA, Jones JL, Conrad PA, Patton S, Lindsay DS, Dubey JP (2010) Toxoplasma gondii: epidemiology, feline clinical aspects, and prevention. Trends parasitol. 26: 190-196.

  158. Ullmann LS, da Silva RC, de Moraes W, Cubas ZS, dos Santos LC, Hoffmann JL, Moreira N, Guimaraes AM, Montaño P, Langoni H, Biondo AW (2010) Serological survey of Toxoplasma gondii in captive Neotropical felids from Southern Brazil. Vet. parasitol. 172: 144-146.

  159. Bevins SN, Carver S, Boydston EE, Lyren LM, Alldredge M, Logan KA, Riley SP, Fisher RN, Vickers TW, Boyce W, Salman M, Lappin MR, Crooks KR, VandeWoude S (2012) Three pathogens in sympatric populations of pumas, bobcats, and domestic cats: implications for infectious disease transmission. PLoS ONE 7: e31403.

  160. Boothroyd JC (2009) Expansion of host range as a driving force in the evolution of Toxoplasma. Mem. inst. Oswaldo Cruz 104: 179-184.

  161. Carme B, Demar-Pierre M (2006) [Toxoplasmosis in French Guiana. Atypical neo-tropical features of a cosmopolitan parasitosis]. Med. trop. (Mars) 66: 495-503.

  162. Carme B, Demar M, Ajzenberg D, Dardé ML (2009) Severe acquired toxoplasmosis caused by wild cycle of Toxoplasma gondii, French Guiana. Emerg. infect. dis. 15: 656-658.

  163. Dardé ML, Villena I, Pinon JM, Beguinot I (1998) Severe toxoplasmosis caused by a Toxoplasma gondii strain with a new isoenzyme type acquired in French Guyana. J. clin. microbiol. 36: 324.

  164. Ajzenberg D, Banuls AL, Su C, Dumetre A, Demar M, Carme B, Dardé ML (2004) Genetic diversity, clonality and sexuality in Toxoplasma gondii. Int. j. parasitol. 34: 1185-1196.

  165. Mercier A, Ajzenberg D, Devillard S, Demar MP, de Thoisy B, Bonnabau H, Collinet F, Boukhari R, Blanchet D, Simon S, Carme B, Dardé ML (2011) Human impact on genetic diversity of Toxoplasma gondii: Example of the anthropized environment from French Guiana. Infect. genet. evol. 11: 1378-1387.

  166. Elbez-Rubinstein A, Ajzenberg D, Dardé ML, Cohen R, Dumètre A, Yera H, Gondon E, Janaud JC, Thulliez P (2009) Congenital toxoplasmosis and reinfection during pregnancy: case report, strain characterization, experimental model of reinfection, and review. J. infect. dis. 199: 280-285.

  167. Grigg ME, Bonnefoy S, Hehl AB, Suzuki Y, Boothroyd JC (2001) Success and virulence in Toxoplasma as the result of sexual recombination between two distinct ancestries. Science 294: 161-165.

  168. Su C, Evans D, Cole RH, Kissinger JC, Ajioka JW, Sibley LD (2003) Recent expansion of Toxoplasma through enhanced oral transmission. Science 299: 414-416.

  169. Mercier A, Devillard S, Ngoubangoye B, Bonnabau H, Bañuls AL, Durand P, Salle B, Ajzenberg D, Dardé ML (2010) Additional Haplogroups of Toxoplasma gondii out of Africa: Population structure and mouse-virulence of strains from Gabon. PLoS negl. trop. dis 4: e876.

  170. Ajzenberg D, Yera H, Marty P, Paris L, Dalle F, Menotti J, Aubert D, Franck J, Bessieres MH, Quinio D, Pelloux H, Delhaes L, Desbois N, Thulliez P, Robert-Gangneux F, Kauffmann-Lacroix C, Pujol S, Rabodonirina M, Bougnoux ME, Cuisenier B, Duhamel C, Duong TH, Filisetti D, Flori P, Gay-Andrieu F, Pratlong F, Nevez G, Totet A, Carme B, Bonnabau H, Dardé ML, Villena I (2009) Genotype of 88 Toxoplasma gondii isolates associated with toxoplasmosis in immunocompromised patients and correlation with clinical findings. J. infect. dis. 199: 1155-1167.

  171. Lehmann T, Marcet PL, Graham DH, Dahl ER, Dubey JP (2006) Globalization and the population structure of Toxoplasma gondii. Proc. natl. acad. sci. U S A 103: 11423-11428.

  172. Dubey JP, Quirk T, Pitt JA, Sundar N, Velmurugan GV, Kwok OC, Leclair D, Hill R, Su C (2008) Isolation and genetic characterization of Toxoplasma gondii from raccoons (Procyon lotor), cats (Felis domesticus), striped skunk (Mephitis mephitis), black bear (Ursus americanus), and cougar (Puma concolor). J. parasitol. 94: 42-45.

  173. Kapperud G, Jenum PA, Stray-Pedersen B, Melby KK, Eskild A, Eng J (1996) Risk factors for Toxoplasma gondii infection in pregnancy. Results of a prospective case-control study in Norway. Am. j. epidemiol. 144: 405-412.

  174. Bowie WR, King AS, Werker DH, IsaacRenton JL, Bell A, Eng SB, Marion SA (1997) Outbreak of toxoplasmosis associated with municipal drinking water. Lancet 350: 173-177.

  175. Aubert D, Villena I (2009) Detection of Toxoplasma gondii oocysts in water: proposition of a strategy and evaluation in Champagne-Ardenne Region, France. Memorias Do Instituto Oswaldo Cruz 104: 290-295.

  176. Baril L, Ancelle T, Goulet V, Thulliez P, Tirard-Fleury V, Carme B (1999) Risk factors for Toxoplasma infection in pregnancy: A case-control study in France. Scand. j. infect. dis. 31: 305-309.

  177. AFSSA (2005) Toxoplasmose : état des connaissances et évaluation du risque lié à l’alimentation Rapport du groupe de travail « Toxoplasma gondii » de l’Afssa. http://www.anses.fr/cgi-bin/countdocs.cgi?Documents/MIC-Ra-Toxoplasmose.pdf.

  178. Opsteegh M, Prickaerts S, Frankena K, Evers EG (2011) A quantitative microbial risk assessment for meatborne Toxoplasma gondii infection in The Netherlands. Int. j. food microbiol. 150: 103-114.

  179. Kijlstra A, Meerburg BG, Mul MF (2004) Animal-friendly production systems may cause re-emergence of Toxoplasma gondii. Njas-Wageningen Journal of Life Sciences 52: 119-132.

  180. van der Giessen J, Fonville M, Bouwknegt M, Langelaar M, Vollema A (2007) Seroprevalence of Trichinella spiralis and Toxoplasma gondii in pigs from different housing systems in The Netherlands. Vet. parasitol. 148: 371-374.

  181. Meerburg BG, Van Riel JW, Cornelissen JB, Kijlstra A, Mul MF (2006) Cats and goat whey associated with Toxoplasma gondii infection in pigs. Vector-Borne and Zoonotic Diseases 6: 266-274.

  182. Kijlstra A, Meerburg B, Cornelissen J, De Craeye S, Vereijken P, Jongert E (2008) The role of rodents and shrews in the transmission of Toxoplasma gondii to pigs. Vet. parasitol. 156: 183-190.

  183. Dubey JP, Hill DE, Rozeboom DW, Rajendran C, Choudhary S, Ferreira LR, Kwok OC, Su C (2012) High prevalence and genotypes of Toxoplasma gondii isolated from organic pigs in northern USA. Vet parasitol. in press.

  184. Kijlstra A, Jongert E (2009) Toxoplasma-safe meat: close to reality? Trends parasitol. 25: 18-22.

  185. Lélu M, Gilot-Fromont E, Aubert D, Afonso E, Dupuis E, Gotteland C, Dardé ML, Marnef F, Poulle ML, Richaume-Jolion A, Villena I (2011) Development of a sensitive method for Toxoplasma gondii oocysts extraction in soil samples. Vet. parasitol. 183: 59-67.

  186. Villena I, Aubert D, Gomis P, Ferté H, Inglard JC, Denis-Bisiaux H, Dondon JM, Pisano E, Ortis N, Pinon JM (2004) Evaluation of a strategy for Toxoplasma gondii oocyst detection in water. Appl. environ. microbiol. 70: 4035–4039.

  187. Kourenti C, Karanis P (2006) Evaluation and applicability of a purification method coupled with nested PCR for the detection of Toxoplasma oocysts in water. Lett. appl. microbiol. 43: 475-481.

  188. Borchardt MA, Spencer SK, Bertz PD, Ware MW, Dubey JP, Alan Lindquist HD (2009) Concentrating Toxoplasma gondii and Cyclospora cayetanensis from surface water and drinking water by continuous separation channel centrifugation. J. appl. microbiol. 107: 1089-1097.

  189. Du F, Zhanga Q, Yu Q, Hu M, Zhou Y, Zhao J (2012) Soil contamination of Toxoplasma gondii oocysts in pig farms in central China. Vet. parasitol. doi:10.1016/j.vetpar.2011.12.036.

  190. Hill D, Coss C, Dubey JP, Wroblewski K, Sautter M, Hosten T, Muñoz-Zanzi C, Mui E, Withers S, Boyer K, Hermes G, Coyne J, Jagdis F, Burnett A, McLeod P, Morton H, Robinson D, McLeod R (2011) Identification of a sporozoite-specific antigen from Toxoplasma gondii. J. parasitol. 97: 328-37.

  191. Muñoz-Zanzi CA, Fry, P Lesina B, Hill D (2010) Toxoplasma gondii Oocyst–specific Antibodies and Source of Infection. Emerg. infect. dis 16: 1591-1596.

  192. Muñoz-Zanzi C, Tamayo R, Balboa J, Hill D (2012) Detection of oocyst-associated toxoplasmosis in swine from Southern Chile. Zoonoses pub. health. doi: 10.1111/j.1863-2378.2012.01471.x.

  193. Boyer K, Hill D, Mui E, Wroblewski K, Karrison T, Dubey JP, Sautter M, Noble AG, Withers S, Swisher C, Heydemann P, Hosten T, Babiarz J, Lee D, Meier P, McLeod R (2011) Toxoplasmosis Study Group. Unrecognized ingestion of Toxoplasma gondii oocysts leads to congenital toxoplasmosis and causes epidemics in North America. Clin. infect. dis. 53: 1081-1089.