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Toxoplasma gondii: history and diagnostic test development

Published online by Cambridge University Press:  16 November 2015

Heidi M. Wyrosdick
Affiliation:
Department of Biomedical and Diagnostic Sciences, College of Veterinary Medicine, University of Tennessee, 2407 River Dr, Knoxville, Tennessee 37996, USA
John J. Schaefer*
Affiliation:
Department of Biomedical and Diagnostic Sciences, College of Veterinary Medicine, University of Tennessee, 2407 River Dr, Knoxville, Tennessee 37996, USA
*
*Corresponding author. E-mail: jschaef6@utk.edu

Abstract

Toxoplasma gondii is a protozoa that causes toxoplasmosis in people and other animals. It is considered one of the most common parasitic infections in the world due to its impressive range of hosts, widespread environmental contamination and the diverse means by which animals can be infected. Despite its ubiquity and numerous ongoing research efforts into both its basic biology and clinical management, many aspects of diagnosis and management of this disease are poorly understood. The range of diagnostic options that is available for veterinary diagnostic investigators are notably more limited than those available to medical diagnosticians, making accurate interpretation of each test result critical. The current review joins other reviews on the parasite with a particular emphasis on the history and continued development of diagnostic tests that are useful for veterinary diagnostic investigations. An understanding of the strengths and shortcomings of current diagnostic techniques will assist veterinary and public health officials in formulating effective treatment and control strategies in diverse animal populations.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2015 

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References

Al-Adhami, BH and Gajadhar, AA (2014). A new multi-host species indirect ELISA using protein A/G conjugate for detection of anti-Toxoplasma gondii IgG antibodies with comparison to ELISA-IgG, agglutination assay and Western blot. Veterinary Parasitology 200: 6673.CrossRefGoogle ScholarPubMed
Andersen, MC, Martine, BJ and Roemer, GW (2004). Use of matrix population models to estimate the efficacy of euthanasia versus trap-neuter-return for management of free-roaming cats. Journal of the American Veterinary Medical Association 225: 18711876.Google Scholar
Assadi-Rad, AM, New, J and Patton, S (1995). Risk factors associated with transmission of Toxoplasma gondii to sows kept in different management systems in Tennessee. Veterinary Parasitology 57: 289297.Google Scholar
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: 359367.Google Scholar
Belaz, S, Gangneux, J-P, Dupretz, P, Guiguen, C and Robert-Gangneux, F (2015). A 10-year retrospective comparison of two target sequences, REP-529 and B1, for Toxoplasma gondii detection by quantitative PCR. Journal of Clinical Microbiology 53: 12941300.Google Scholar
Bhide, MR, Curlik, J, Travnicek, M and Lazar, P (2004). Protein A/G dependent ELISA a promising diagnostic tool in Lyme disease seroprevalence in game animals and hunting dogs. Comparative Immunology, Microbiology & Infectious Diseases 27: 191199.CrossRefGoogle Scholar
Burg, JL, Grover, CM, Pouletty, P and Boothroyd, JC (1989). Direct and sensitive detection of a pathogenic protozoan, Toxoplasma gondii, by polymerase chain-reaction. Journal of Clinical Microbiology 27: 17871792.CrossRefGoogle ScholarPubMed
Calderaro, A, Piccolo, G, Gorrini, C, Peruzzi, S, Zerbini, L, Bommezzadri, S, Dettori, F and Chezzi, C (2006). Comparison between two real-time PCR assays and a nested-PCR for the detection of Toxoplasma gondii . Acta Biomedica 77: 7580.Google Scholar
Cassaing, S, Bessieres, MH, Berry, A, Berrebi, A, Fabre, R and Magnaval, JF (2006). Comparison between two amplification sets for molecular diagnosis of toxoplasmosis by real-time PCR. Journal of Clinical Microbiology 44: 720724.Google Scholar
Chabbert, E, Lachaud, L, Crobu, L and Bastien, P (2004). Comparison of two widely used PCR primer systems for detection of Toxoplasma in amniotic fluid, blood, and tissues. Journal of Clinical Microbiology 42: 17191722.Google Scholar
Cole, RA, Lindsay, DS, Howe, DK, Roderick, CL, Dubey, JP, Thomas, NJ and Baeten, LA (2000). Biological and molecular characterizations of Toxoplasma gondii strains obtained from southern sea otters (Enhydra lutris nereis). Journal of Parasitology 86: 526530.Google Scholar
Cook, AJC, Gilbert, RE, Buffolano, W, Zufferey, J, Petersen, E, Jenum, PA, Foulon, W, Semprini, AE, Dunn, DT and On behalf of the European Research Network on Congenital Toxoplasmosis (2000). Sources of Toxoplasma infection in pregnant women: European multicenter case-control study. BMJ 321: 142147.Google Scholar
Crist, SC, Stewart, RL Jr, Rinehart, JP and Needham, GR (1999). Surveillance for Toxoplasma gondii in the white-tailed deer (Odocoileus virginianus) in Ohio. Ohio Journal of Science 99: 3437.Google Scholar
Dabritz, HA and Conrad, PA (2010). Cats and Toxoplasma: implications for public health. Zoonoses and Public Health 57: 3452.Google Scholar
Dabritz, HA, Gardner, IA, Miller, MA, Lappin, MR, Atwill, ER, Packham, AE, Melli, AC and Conrad, PA (2007a). Evaluation of two Toxoplasma gondii serologic tests used in a serosurvey of domestic cats in California. Journal of Parasitology 93: 806816.Google Scholar
Dabritz, HA, Miller, MA, Atwill, ER, Gardner, IA, Leutenegger, C, Melli, AC and Conrad, PA (2007b). Detection of T. gondii-like oocysts in cat feces and estimates of the environmental oocyst burden. Journal of the American Veterinary Medical Association 231: 16761684.Google Scholar
Dehkordi, FS, Borujeni, MR, Rahimi, E and Abdizadeh, R (2013). Detection of Toxoplasma gondii in raw caprine, ovine, buffalo, bovine and camel milk using cell cultivation, cat bioassay, capture ELISA and PCR methods in Iran. Foodborne Pathogens and Disease 10: 120125.Google Scholar
Denkers, EY, Schneider, AG, Cohen, SB and Butcher, BA (2012). Phagocyte responses to protozoan infection and how Toxoplasma gondii meets the challenge. Public Library of Science Pathogens 8: e1002794.Google Scholar
Desmonts, G and Remington, JS (1980). Direct agglutination test for diagnosis of Toxoplasma infection: method for increasing sensitivity and specificity. Journal of Clinical Microbiology 11: 562568.Google Scholar
deSouza, SLP, Gennari, SM, Yai, LEO, D'Auria, SRN, Cardoso, SMS, Junior, JSG and Dubey, JP (2003). Occurrence of Toxoplasma gondii antibodies in sera from dogs of the urban and rural areas from Brazil. Revista Brasileira de Parasitologia Veterinaria 12: 13.Google Scholar
Dubey, JP (1995). Duration of immunity to shedding of Toxoplasma gondii oocysts by cats. Journal of Parasitology 81: 410415.Google Scholar
Dubey, JP (2001). Oocyst shedding by cats fed isolated bradyzoites and comparison of infectivity of bradyzoites of the VEG strain Toxoplasma gondii to cats and mice. Journal of Parasitology 87: 215219.CrossRefGoogle ScholarPubMed
Dubey, JP (2008). The history of Toxoplasma gondii – the first 100 years. Journal of Eukaryotic Microbiology 55: 467475.Google Scholar
Dubey, JP (2010). Toxoplasmosis of Animals and Humans. 2nd edn. Boca Raton, FL: CRC Press.Google Scholar
Dubey, JP and Adams, DS (1990). Prevalence of Toxoplasma gondii antibodies in dairy goats from 1982 to 1984. Journal of the American Veterinary Medical Association 196: 295296.Google Scholar
Dubey, JP and Desmonts, G (1987). Serological responses of equids fed Toxoplasma gondii oocysts. Equine Veterinary Journal 19: 337339.Google Scholar
Dubey, JP and Jones, JL (2014). Comments on “Detection of Toxoplasma gondii in raw caprine, ovine, buffalo, bovine and camel milk using cell cultivation, cat bioassay, capture ELISA, and PCR methods in Iran”. Foodborne Pathogens and Disease 11: 500.CrossRefGoogle Scholar
Dubey, JP and Thulliez, P (1989). Serologic diagnosis of toxoplasmosis in cats fed Toxoplasma gondii tissue cysts. Journal of the American Veterinary Medical Association 194: 12971299.Google Scholar
Dubey, JP and Welcome, FL (1988). Toxoplasma gondii-induced abortion in sheep. Journal of the American Veterinary Medical Association 193: 697700.Google Scholar
Dubey, JP, Christie, E and Pappas, PW (1977). Characterization of Toxoplasma gondii from the feces of naturally infected cats. Journal of Infectious Diseases 136: 432435.Google Scholar
Dubey, JP, Gamble, HR, Hill, D, Sreekumar, C, Romand, S and Thulliez, P (2002a). High prevalence of viable Toxoplasma gondii infection in market weight pigs from a farm in Massachusetts. Journal of Parasitology 88: 12341238.Google Scholar
Dubey, JP, Saville, WJA, Stanek, JF and Reed, SM (2002b). Prevalence of Toxoplasma gondii antibodies in domestic cats from rural Ohio. Journal of Parasitology 88: 802803.CrossRefGoogle ScholarPubMed
Dubey, JP, Hill, DE, Jones, JL, Hightower, AW, Kirkland, E, Roberts, JM, Marcet, PL, Lehmann, T, Vianna, MCB, Miska, K, Sreekumar, C, Kwok, OCH, Shen, SK and Gamble, HR (2005). Prevalence of viable Toxoplasma gondii in beef, chicken, and pork from retail meat stores in the United States: risk assessment to consumers. Journal of Parasitology 91: 10821093.CrossRefGoogle ScholarPubMed
Dubey, JP, Sundar, N, Hill, D, Velmurugan, GV, Bandini, LA, Kwok, OCH, Majumdar, D and Su, C (2008a). High prevalence and abundant atypical genotypes of Toxoplasma gondii isolated from lambs destined for human consumption in the USA. International Journal of Parasitology 38: 9991006.Google Scholar
Dubey, JP, Velmurugan, GV, Ulrich, V, Gill, J, Carstensen, M, Sundar, N, Kwok, OCH, Thulliez, P, Majumdar, D and Su, C (2008b). Transplacental toxoplasmosis in naturally-infected white-tailed deer: isolation and genetic characterisation of Toxoplasma gondii from foetuses of different gestational ages. International Journal of Parasitology 38: 10571063.CrossRefGoogle ScholarPubMed
Dubey, JP, Bhatia, CR, Lappin, MR, Ferreira, LR, Thorn, A and Kwok, OCH (2009a). Seroprevalence of Toxoplasma gondii and Bartonella spp. antibodies in cats from Pennsylvania. Journal of Parasitology 95: 578580.Google Scholar
Dubey, JP, Jenkins, MC, Kwok, OCH, Zink, RL, Michalski, ML, Ulrich, V, Gill, J, Cartensen, M and Thulliez, P (2009b). 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: 330334.Google Scholar
Dubey, JP, Dennis, PM, Verma, SK, Choudhary, S, Ferreira, LR, Oliveira, S, Kwok, OCH, Butler, E, Carstensen, M and Su, C (2014a). 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: 270275.Google Scholar
Dubey, JP, Verma, SK, Ferreira, LR, Oliveira, S, Cassinelli, AB, Ying, Y, Kwok, OCH, Tuo, W, Chiesa, OA, Jones, JL (2014b). Detection and survival of Toxoplasma gondii in milk and cheese from experimentally infected goats. Journal of Food Protection 77: 17471753.CrossRefGoogle ScholarPubMed
Eliasson, M, Andersson, R, Olsson, A, Wigzell, H and Uhlen, M (1989). Differential IgG-binding characteristics of staphylococcal protein A, streptococcal protein G, and a chimeric protein AG. Journal of Immunology 142: 575581.Google Scholar
Ferguson, DJP (2009). Toxoplasma gondii: 1908–2008, homage to Nicolle, Manceaux and Splendore. Memorias do Instituto Oswaldo Cruz 104: 133148.CrossRefGoogle ScholarPubMed
Filisetti, D, Gorcii, M, Pernot-Marino, E, Villard, O and Candolfi, E (2003). Diagnosis of congenital toxoplasmosis: comparison of targets for detection of Toxoplasma gondii by PCR. Journal of Clinical Microbiology 41: 48264828.Google Scholar
Freeman, K, Oakley, L, Pollak, A, Buffolano, W, Petersen, E, Semprini, AE, Salt, A, Gilbert, R and European Multicentre Study on Congenital Toxoplasmosis (2005). Association between congenital toxoplasmosis and preterm birth, low birthweight and small for gestational age birth. British Journal of Obstetrics and Gynaecology 112: 3137.Google Scholar
Frenkel, JK and Friedlander, S (1951). Pathology of Neonatal Disease, Pathogenesis, Diagnosis, and Treatment Public Health Service Publication No. 141. Washington, DC, USA: United States Government Printing Office, Toxoplasmosis, pp. 1150.Google Scholar
Frenkel, JK, Dubey, JP and Miller, NL (1970). Toxoplasma gondii in cats: fecal stages identified as coccidian oocysts. Science 167: 893896.Google Scholar
Gamble, HR, Dubey, JP and Lambillotte, DN (2005). Comparison of a commercial ELISA with the modified agglutination test for detection of Toxoplasma infection in the domestic pig. Veterinary Parasitology 128: 177181.Google Scholar
Garcia-Vazques, Z, Rosario-Cruz, R, Diaz-Garcia, G and Hernandez-Baumgarten, O (1993). Seroprevalence of Toxoplasma gondii infection in cattle, swine, and goats in four Mexican states. Preventive Veterinary Medicine 17: 127132.Google Scholar
Gardner, IA, Greiner, M and Dubey, JP (2009). Statistical evaluation of test accuracy studies for Toxoplasma gondii in food animal intermediate hosts. Zoonoses and Public Health 57: 8294.Google Scholar
Harden, CL and Hair, LS (1994). Diagnosis of central nervous system toxoplasmosis in AIDS patients confirmed by autopsy. AIDS 8: 11881189.Google Scholar
Hartley, WJ and Marshall, SC (1957). Toxoplasmosis as a cause of ovine perinatal mortality. New Zealand Veterinary Journal 5: 119124.Google Scholar
Hill, DE, Chirukandoth, S, Dubey, JP, Lunney, JK and Gamble, HR (2006). Comparison of detection methods for Toxoplasma gondii in naturally and experimentally infected swine. Veterinary Parasitology 141: 917.Google Scholar
Hill, RE, Zimmerman, JJ, Wills, RW, Patton, S and Clark, WR (1998). Seroprevalence of antibodies against Toxoplasma gondii in free-ranging mammals in Iowa. Journal of Wildlife Diseases 34: 811815.Google Scholar
Hogan, MJ (1951). Ocular Toxoplasmosis. New York: Columbia University Press.Google Scholar
Homan, WL, Vercammen, M, de Braekeleer, J and Verschueren, H (2000). Identification of a 200- to 300-fold repetitive 529 bp DNA fragment in Toxoplasma gondii, and its use for diagnostic and quantitative PCR. International Journal of Parasitology 30: 6795.Google Scholar
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: 172173.Google Scholar
Hutchison, WM (1965). Experimental transmission of Toxoplasma gondii . Nature 206: 961962.CrossRefGoogle ScholarPubMed
Janků, J (1923). Pathogenesa a pathologická anatomie tak nazvaneho vrozeného kolombu žluté skvrany voku normálné velikem a microphthalmickém s nalezem parasitu v sítnici. Časopis lékařeů českŷck [Pathogenesis and pathologic anatomy of the “congenital coloboma” of the macula lutea in an eye of normal size, with microscopic detection of parasites in the retina] 62, 1021–1027, 1052–1059, 1081–1085, 1111, 1138–1143 (For English translation, see Janků, J., 1959. Cesk. Parasitol. 6, 9–58).Google Scholar
Jessup, DA (2004). The welfare of feral cats and wildlife. Journal of the American Veterinary Medical Association 225: 13771383.Google Scholar
Jittapalapong, S, Nimsupan, B, Pinyopanuwat, N, Chimnoi, W, Kabeya, H and Maruyama, S (2007). Seroprevalence of Toxoplasma gondii antibodies in stray cats and dogs in the Bangkok metropolitan area, Thailand. Veterinary Parasitology 145: 138141.Google Scholar
Jones, JL, Parise, ME and Fiore, AE (2014). Neglected parasitic infections in the United States: toxoplasmosis. American Journal of Tropical Medicine and Hygiene 90: 794799.Google Scholar
Kimbita, EN, Xuan, X, Huang, X, Miyazawa, X, Fukumoto, S, Mishima, M, Suzuki, H, Sugimoto, C, Nagaswaw, H, Fujisaki, K, Suzuki, N, Mikami, T and Igarashi, I (2001). Serodiagnosis of Toxoplasma gondii infection in cats by enzyme-linked immunosorbent assay using recombinant SAG1. Veterinary Parasitology 102: 3544.Google Scholar
Klun, I, Djurkovic-Djakovic, O and Thulliez, P (2007). Comparison of a commercial ELISA with the modified agglutination test for the detection of Toxoplasma gondii infection in naturally exposed sheep. Zoonoses and Public Health 54: 165168.Google Scholar
Kodym, P, Machala, L, Rohacova, H, Sirocka, B and Maly, M (2006). Evaluation of a commercial IgE ELISA in comparison with IgA and IgM ELISAs, IgG avidity assay and complement fixation for the diagnosis of acute toxoplasmosis. Clinical Microbiology and Infection 13: 4047.Google Scholar
Lappin, MR and Powell, CC (1991). Comparison of latex agglutination, indirect hemagglutination, and ELISA techniques for the detection of Toxoplasma gondii-specific antibodies in the serum of cats. Journal of Veterinary Internal Medicine 5: 299301.Google Scholar
Levaditi, C, Schoen, R and Sanchis Bayarri, V (1928). L'encephalo-myelite toxoplasmique chronique du lapin et de la souris. Comptes Rendus de Societe Biologique 99: 3740.Google Scholar
Liesenfeld, O, Press, C, Montoya, JG, Gill, R, Isaac-Renton, JL, Hedman, K and Remington, JS (1997). False-positive results in immunoglobulin M (IgM) Toxoplasma antibody tests and importance of confirmatory testing: the Platelia Toxo IgM test. Journal of Clinical Microbiology 35: 174178.Google Scholar
Lindsay, DS, Dubey, JP, Upton, SJ and Ridley, RK (1990). Serological prevalence of Neospor a caninum and Toxoplasma gondii in dogs from Kansas. Journal of the Helminthological Society of Washington 57: 8688.Google Scholar
Lindsay, DS, Phelps, KK, Smith, SA, Flick, G, Sumner, SS and Dubey, JP (2001). Removal of Toxoplasma gondii oocyst from sea water by eastern oysters (Crassostrea virginica). Journal of Eukaryotic Microbiology 48 (suppl.): 197S198S.CrossRefGoogle Scholar
Lindsay, DS, Weiss, LM and Suzuki, Y (2003). Toxoplasmosis in: Richardson, D & Krause, P (eds.) North American Parasitic Zoonoses. New York: Springer US, pp. 129-150.Google Scholar
Lindsay, DS, Collins, MV, Jordan, CN, Flick, GJ and Dubey, JP (2005). Effects of high pressure processing on infectivity of Toxoplasma gondii oocysts for mice. Journal of Parasitology 91: 699701.Google Scholar
Longcore, T, Rich, C, and Sullivan, LM (2009). Critical assessment of claims regarding management of feral cats by trap-neuter-return. Conservation Biology 23: 887894.Google Scholar
Lopez, A, Dietz, VJ, Wilson, M, Navin, TR and Jones, JL (2000). Preventing congenital toxoplasmosis. MMWR. Recommendations and reports: Morbidity and mortality weekly report. Recommendations and reports/Centers for Disease Control, 49: 59-68.Google Scholar
Luft, BJ, Conley, F, Remington, JS, Laverdiere, M, Wagner, KF, Levine, JF, Craven, PC, Strandberg, DA, File, TM, Rice, N and Meunier-Carpentier, F (1983). Outbreak of central-nervous-system toxoplasmosis in Western Europe and North America. Lancet 321: 781784.Google Scholar
Lunde, MN (1973). Laboratory methods in the diagnosis of toxoplasmosis. Health Laboratory Science 10: 319328.Google Scholar
Luria, BJ, Levy, JK, Lappin, MR, Breitschwerdt, EB, Legendre, AM, Hernandez, JA, Gorman, AP and Lee, IT (2004). Prevalence of infectious diseases in feral cats in northern Florida. Journal of Feline Medicine and Surgery 6: 287296.Google Scholar
Lynfield, R and Guerina, NG (1997). Toxoplasmosis. Pediatrics in Review 18: 7583.Google Scholar
Mainar-Jaime, RC and Barberan, M (2007). Evaluation of the diagnostic accuracy of the modified agglutination test (MAT) and an indirect ELISA for the detection of serum antibodies against Toxoplasma gondii in sheep through Bayesian approaches. Veterinary Parasitology 148: 122129.CrossRefGoogle Scholar
Massie, GN, Ware, MW, Villegas, EN and Black, MW (2010). Uptake and transmission of Toxoplasma gondii oocysts by migratory, filter-feeding fish. Veterinary Parasitology 169: 296303.Google Scholar
McSporran, KD, McCaughan, C, Currall, JHS and Demsteegt, A (1985). Toxoplasmosis in goats. New Zealand Veterinary Journal 33: 3940.Google Scholar
Mead, PS, Slutsker, L, Dietz, V, McCaig, LF, Bresee, JS, Shapiro, C, Griffin, PM, and Tauxe, RV (1999). Food-related illness and death in the United States. Emerging Infectious Diseases 5: 607624.Google Scholar
Meireles, LR, Galisteo, AJ Jr, Pompeu, E and Andrade, HF Jr (2004). Toxoplasma gondii spreading in an urban area evaluated by seroprevalence in free-living cats and dogs. Tropical Medicine and International Health 9: 876881.Google Scholar
Mello, U (1910). Un cas de toxoplasmose du chien observe a Turin. Bulletin de la Societe de Pathologie Exotique et de ses Filiales 3: 359363.Google Scholar
Miller, MA, Gardner, IA, Kreuder, C, Paradies, DM, Worcester, KR, Jessup, DA, Dodd, E, Harris, MD, Ames, JA, Packham, AE and Conrad, PA (2002). Coastal freshwater runoff is a risk factor for Toxoplasma gondii infection of southern sea otters (Enhydra lutris nereis). International Journal of Parasitology 32: 9971006.CrossRefGoogle ScholarPubMed
Nicolle, C and Manceaux, L (1909). Sur un protozoaire nouveau du gondi. Comptes Rendus de l'Academie des Sciences 148: 369372.Google Scholar
Nogales, M, Martin, A, Tershy, BR, Donlan, CJ, Veitch, D, Puerta, N, Wood, B, Alonso, J (2004). A review of feral cat eradiction on Islands. Conservation Biology 18: 310319.Google Scholar
Olafson, P and Monlux, WS (1942). Toxoplasma infection in animals. Cornell Veterinarian 32: 76190.Google Scholar
Papini, RA, Buzzone, G, Nardoni, S, Rocchigiani, G and Mancianti, F (2015). Seroprevalence and genotyping of Toxoplasma gondii in horses slaughtered for human consumption in Italy. Journal of Equine Veterinary Science 35: 657661.Google Scholar
Patton, S, Johnson, SS and Puckett, K (1990). Prevalence of Toxoplasma gondii antibodies in nine populations of dairy goats: compared titers using modified direct agglutination and indirect hemagglutination. Journal of Parasitology 76: 7477.Google Scholar
Reischl, U, Bretagne, S, Kruger, D, Ernault, P and Costa, J-M (2003). Comparison of two DNA targets for the diagnosis of toxoplasmosis by real-time PCR using fluorescence resonance energy transfer hybridization probes. BMC Infectious Diseases 3: 7.Google Scholar
Reiter-Owona, I, Petersen, E, Joynson, D, Aspock, H, Darde, ML, Disko, R, Dreazen, O, Dumon, H, Grillo, R, Gross, U, Hayde, M, Holliman, R, Ho-Yen, DO, Janitschke, K, Jenum, PA, Naser, K, Olszewski, M, Thulliez, P and Seitz, HM (1999). The past and present role of the Sabin-Feldman dye test in the serodiagnosis of toxoplasmosis. Bulletin of the World Health Organization 77: 929935.Google ScholarPubMed
Remington, JS and Desmonts, G (1990). Toxoplasmosis. In: Remington, JS and Klein, JO (eds) Infectious Diseases of the Fetus and Newborn Infant. Philadelphia, PA: Saunders, pp. 89195.Google Scholar
Remington, JS, McLeod, R and Thulliez, P (2001). Toxoplasmosis. In: Remington, JS and Klein, J (eds) Infectious Diseases of the Fetus and Newborn Infant. Philadelphia: WB Saunders, pp. 205346.Google Scholar
Remington, JS, Thulliez, P and Montoya, JG (2004). Recent developments for diagnosis of toxoplasmosis. Journal of Clinical Microbiology 42: 941945.Google Scholar
Roberts, A, Hedman, K, Luyasu, V, Zufferey, J, Bessieres, M-H, Blatz, R-M, Candolfi, E, Decoster, A, Enders, G, Gross, U, Guy, E, Hayde, M, Ho-Yen, D, Johnson, J, Lecolier, B, Naessens, A, Pelloux, H, Thulliez, P and Petersen, E (2001). Multicenter evaluation of strategies for serodiagnosis of primary infection with Toxoplasma gondii . The European Journal of Clinical Microbiology and Infectious Diseases 20: 467474.CrossRefGoogle ScholarPubMed
Rorman, E, Zamir, CS, Rilkis, I and Ben-David, H (2006). Congenital toxoplasmosis – prenatal aspects of Toxoplasma gondii infection. Reproductive Toxicology 4: 458472.Google Scholar
Sabin, AB (1942). Toxoplasmosis. A recently recognized disease of human beings. Advances in Pediatrics 1: 153.Google Scholar
Sabin, AB and Feldman, HA (1948). Dyes as microchemical indicators of a new immunity phenomenon affecting a protozoan parasite (Toxoplasma). Science 108: 660663.Google Scholar
Sabin, AB and Olitsky, PK (1937). Toxoplasma and obligate intracellular parasitism. Science 85: 336338.Google Scholar
Santos, TR, Costa, AJ, Toniollo, GH, Luvizotto, MC, Benetti, AH, Santos, RR, Matta, DH, Lopes, WD, Oliveira, JA and Oliveira, GP (2009). Prevalence of anti-Toxoplasma gondii antibodies in dairy cattle, dogs, and humans from the Jauru micro-region, Mato Grosso state, Brazil. Veterinary Parasitology 161: 324326.Google Scholar
Schaefer, JJ, White, HA, Schaaf, SL, Mohammed, HO and Wade, SE (2011). Modification of a commercial Toxoplasma gondii immunoglobulin G enzyme-linked immunosorbent assay for use in multiple animal species. Journal of Veterinary Diagnostic Investigation 23: 297301.Google Scholar
Schaefer, JJ, White, HA, Schaaf, SL, Mohammed, HO and Wade, SE (2012). Chimeric protein A/G conjugate for detection of anti-Toxoplasma gondii immunoglobulin G in multiple animal species. Journal of Veterinary Diagnostic Investigation 24: 572575.CrossRefGoogle ScholarPubMed
Schaefer, JJ, Kirchgessner, MS, Whipps, CM, Mohammed, HO, Bunting, EM and Wade, SE (2013). Prevalence of antibodies to Toxoplasma gondii in white-tailed deer (Odocoileus virginianus) in New York State, USA. Journal of Wildlife Diseases 49: 940945.Google Scholar
Schares, G, Pantchev, N, Barutzki, D, Heydorn, AO, Bauer, C and Conraths, FJ (2005). Oocysts of Neospora caninum, Hammondia heydorni, Toxoplasma gondii and Hammondia hammondi in faeces collected from dogs in Germany. International Journal of Parasitology 35: 15251537.Google Scholar
Schares, G, Vrhovec, MG, Pantchev, N, Herrmann, DC and Conraths, FJ (2008). Occurrence of Toxoplasma gondii and Hammondia hammondi oocysts in the faeces of cats from Germany and other European countries. Veterinary Parasitology 152: 3445.Google Scholar
Schatzberg, SJ, Haley, NJ, Barr, SC, deLahunta, A, Olby, N, Munana, K and Sharp, NJH (2003). Use of a multiplex polymerase chain reaction assay in the antemortem diagnosis of toxoplasmosis and neosporosis in the central nervous system of cats and dogs. American Journal of Veterinary Research 64: 15071513.Google Scholar
Schwab, DJ and McDevitt, JJ (2003). Development of a PCR-enzyme immunoassay oligoprobe detection method for Toxoplasma gondii oocysts, incorporating PCR controls. Applied Environnebtak Microbiology 69: 58195825.Google Scholar
Shaapan, RM, El-Nawawi, FA and Tawfik, FAA (2008). Sensitivity and specificity of various serological tests for the detection of Toxoplasma gondii infection in naturally infected sheep. Veterinary Parasitology 153: 359362.Google Scholar
Shapiro, K, Krusor, C, Mazzillo, FFM, Conrad, PA, Largier, JL, Mazet, JAK and Silver, MW (2014). Aquatic polymers can drive pathogen transmission in coastal ecosystems. Proceedings of the Royal Society of London B: Biological Sciences 281: 20141287. http://dx.doi.org/10.1098/rspb.2014.1287 Google Scholar
Shen, L, Zhichung, L, Biaucheng, Z and Huayuan, Y (1990). Prevalence of Toxoplasma gondii infection in man and animals in Guangdong, Peoples’ Republic of China. Veterinary Parasitology 34: 357360.Google Scholar
Silva, NM, Lourenco, EV, Silva, DAO and Mineo, JR (2002). Optimisation of cut-off titres in Toxoplasma gondii specific ELISA and IFAT in dog sera using immunoreactivity to SAG-1 antigen as a molecular marker of infection. Veterinary Journal 163: 9498.Google Scholar
Spencer, JA, Higginbotham, MJ and Blagburn, BL (2003). Seroprevalence of Neospora caninum and Toxoplasma gondii in captive and free-ranging nondomestic felids in the United States. Journal of Zoo and Wildlife Medicine 34: 246249.Google Scholar
Splendore, A (1908). Un nuovo protozoa parassita de’ conigli, incontrato nelle lesion anatomiche d'une malattia che ricorda in molti punti il Kala-azar dell’ uomo. Nota preliminare pel. Rev Soc Scient Sao Paulo 3: 109112.Google Scholar
Su, C, Zhang, X and Dubey, JP (2006). Genotyping of Toxoplasma gondii by multilocus PCR-RFLP markers: a high resolution and simple method for identification of parasites. International Journal of Parasitology 36: 841848.Google Scholar
Tassi, P (2007). Toxoplasma gondii infection in horses. A review. Parassitologia 49: 715.Google Scholar
Tenter, AM, Heckeroth, AR and Weiss, LM (2000). Toxoplasma gondii: from animals to humans. International Journal of Parasitology 30: 12171258.Google Scholar
Torres, CM (1927). Morphologie d'un nouveau parasite de l'homme, Encephalitozoon chagasi, N. sp., observe dans un cas de meningo-encephalo-myelite congenitale avec myosite et myocardite. Comptes Rendus Societe de Biologie 97: 17871790.Google Scholar
Toxoplasmosis. Centers for Disease Control and Prevention, 10 Jan. 2013. Web. 01 July 2015.Google Scholar
Tuazon, CU (1989). Toxoplasmosis in AIDS patients. Journal of Antimicrobial Chemotherapy 23 (suppl. A): 7782.Google Scholar
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: 4144.Google Scholar
Vollaire, MR, Radecki, SV and Lappin, MR (2005). Seroprevalence of Toxoplasma gondii antibodies in clinically ill cats in the United States. American Journal of Veterinary Research 66: 874877.Google Scholar
Wahab, T, Edvinsson, B, Palm, D and Lindh, J (2010). Comparison of the AF146527 and B1 repeated elements, two real-time PCR targets used for detection of Toxoplasma gondii . Journal of Clinical Microbiology 48: 591592.Google Scholar
Weinman, D and Chandler, AH (1954). Toxoplasmosis in swine and rodents. Reciprocal oral infection and potential human hazard. Proceedings of the Society for Experimental Biology and Medicine 87: 211216.Google Scholar
Weiss, LM and Kim, K (2007). Toxoplasma gondii: the model apicomplexan: perspectives and methods. Amsterdam; Boston, Elsevier/Academic Press ISBN: 9780123695420.Google Scholar
Wendte, JM, Gibson, AK and Grigg, ME (2011). Population genetics of Toxoplasma gondii: new perspectives from parasite genotypes in wildlife. Veterinary Parasitology 182: 96111.Google Scholar
Werre, SR, Jacobson, RH, Bowman, DD, Dubey, JP and Mohammed, HO (2002). Evaluation of kinetics and single-read enzyme-linked immunoassays for detection of Toxoplasma gondii antibodies in sheep. Journal of Veterinary Diagnostic Investigation 14: 225230.Google Scholar
Wilson, M, Ware, DA and Walls, KW (1987). Evaluation of commercial serodiagnostic kits for toxoplasmosis. Journal of Clinical Microbiology 25: 22622265.Google Scholar
Wilson, M, Remington, JS, Clavet, C, Varney, G, Press, C, Ware, D and The FDA Toxoplasmosis ad hoc Working Group (1997). Evaluation of six commercial kits for detection of human immunoglobulin M antibodies to Toxoplasma gondii . Journal of Clinical Microbiology 35: 31123115.Google Scholar
Wolf, A, Cohen, D and Paige, BH (1939a). Human toxoplasmosis: occurrence in infants as an encephalomyelitis verification by transmission to animals. Science 89: 226227.Google Scholar
Wolf, A, Cowen, D, Paige, BH (1939b). Toxoplasmic encephalomyelitis III. A new case of granulomatous encephalomyelitis due to a protozoon. American Journal of Pathology 15: 657694.Google Scholar
Zaki, M (1995). Seroprevalence of Toxoplasma gondii in domestic animals in Pakistan. Journal of the Pakistan Medical Association 45: 45.Google Scholar
Zhang, D, Wang, Z, Fang, R, Nie, H, Feng, H, Zhou, Y and Zhao, J (2010). Use of protein AG in ELISA for serodiagnosis of Toxoplasma gondii infection in four species of animals. Clinical and Vaccine Immunology 17: 485486.Google Scholar