Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-22T18:47:54.313Z Has data issue: false hasContentIssue false
  • English
  • Français

Sarcocystis neurona, Neospora spp. and Toxoplasma gondii infections in horses and equine protozoal myeloencephalitis (EPM): five decades of personal experience, perspectives and update

Published online by Cambridge University Press:  09 March 2022

J. P. Dubey Open the ORCID record for J. P. Dubey [Opens in a new window]
J. P. Dubey*
Affiliation:
United States Department of Agriculture, Agricultural Research Service, Animal Parasitic Diseases Laboratory, Beltsville Agricultural Research Center, Building 1001, Beltsville, MD20705-2350, USA
*
Author for correspondence: J. P. Dubey, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Sarcocystis neurona, Neospora spp. and Toxoplasma gondii are related protozoans; they were considered the same parasite until 1970s. Two of these parasites, S. neurona and Neospora spp. are associated with a neurological syndrome in horses, called equine protozoal myeloencephalitis (EPM). The diagnosis and treatment of EPM are difficult. Most cases of EPM are related to S. neurona while only a few are due to Neospora spp. infections. There are two species of Neospora, Neospora caninum that has a wide host range and Neospora hughesi that has been found only in horses. Currently, T. gondii is not considered as a cause of EPM in horses, although it causes neurological illness in many other hosts, including humans. The present review provides an update on history, life cycle, diagnosis and treatment of these three infections in horses.

Keywords

ClinicalhorsesNeospora sppSarcocystis neuronaToxoplasma gondii
Type
Review Article
Information
Parasitology , Volume 149 , Issue 6 , May 2022 , pp. 717 - 728
Check for updates
Creative Commons
This is a work of the US Government and is not subject to copyright protection within the United States. Published by Cambridge University Press.
Copyright
Copyright © United States Department of Agriculture, [2022]

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*Dedicated to the memory of Dr William J. Saville, late professor, Department of Veterinary Preventive Medicine, The Ohio State University, Columbus, Ohio, USA, for his contributions to EPM.

References

Aciöz, M, Bozkaya, F and Babür, C (2021) Seroprevalence of Toxoplasma gondii antibodies using Sabin–Feldman dye test among equines in Isparta province, Turkey. Parasitologists United Journal 14, 146–150. doi: 10.21608/PUJ.2021.69445.112CrossRefGoogle Scholar
Al-Khalidi, NW and Dubey, JP (1979) Prevalence of Toxoplasma gondii infection in horses. Journal of Parasitology 65, 331–334.CrossRefGoogle ScholarPubMed
Antonello, AM, Pivoto, FL, Camillo, G, Braunig, P, Sangioni, LA, Pompermayer, E and Vogel, FSF (2012) The importance of vertical transmission of Neospora sp. in naturally infected horses. Veterinary Parasitology 187, 367–370.CrossRefGoogle ScholarPubMed
Arruda, IF, Freitas, WA, Carrijo, KF, Paz, PS, Silva, MM, Sudré, AP, Marques-Santos, F, Fonseca, ABM, Amendoeira, MRR and Millar, PR (2020) Occurrence of anti-Toxoplasma gondii antibodies and risk factors associated with infection in equids slaughtered for human consumption in Brazil. Revista Brasileira de Parasitologia Veterinária 29, e002320.CrossRefGoogle ScholarPubMed
Beech, J (1974) Equine protozoan encephalomyelitis. Veterinary Medicine Small Animal Clinician 69, 1562–1566.Google ScholarPubMed
Beech, J and Dodd, DC (1974) Toxoplasma-like encephalomyelitis in the horse. Veterinary Pathology 11, 87–96.CrossRefGoogle Scholar
Berná, L, Marquez, P, Cabrera, A, Greif, G, Francia, ME and Robello, C (2021) Reevaluation of the Toxoplasma gondii and Neospora caninum genomes reveals misassembly, karyotype differences, and chromosomal rearrangements. Genome Research 31, 823–833.CrossRefGoogle ScholarPubMed
Bernardino, PN, Smith, WA, Conrad, PA, Packham, AE, Tamez-Trevino, E, Barnum, S and Pusterla, N (2021) Molecular detection of Sarcocystis neurona in cerebrospinal fluid from 210 horses with suspected neurologic disease. Veterinary Parasitology 291, 109372.CrossRefGoogle ScholarPubMed
Blazejewski, T, Nursimulu, N, Pszenny, V, Dangoudoubiyam, S, Namasivayam, S, Chiasson, MA, Chessman, K, Tonkin, M, Seshadri Swapna, L, Hung, SS, Bridgers, J, Ricklefs, SM, Boulanger, MJ, Dubey, JP, Porcella, SF, Kissinger, JC, Howe, DK, Grigg, ME and Parkinson, J (2015) Systems-based analysis of the Sarcocystis neurona genome identifies pathways that contribute to a heteroxenous life cycle. mBio 6, e2445–e2414.CrossRefGoogle ScholarPubMed
Borges-Silva, W, de Jesus, RF, Ferreira, R and Gondim, LFP (2020) Reactivity of horse sera to antigens derived from Sarcocystis falcatula-like and Sarcocystis neurona. Frontiers in Veterinary Science 7, Article 573016, 1–8. doi: 10.3389/fvets.2020.573016CrossRefGoogle ScholarPubMed
Bowden, GD, Land, KM, O'Connor, RM and Fritz, HM (2018) High-throughput screen of drug repurposing library identifies inhibitors of Sarcocystis neurona growth. International Journal for Parasitology: Drugs and Drug Resistance 8, 137–144.Google ScholarPubMed
Cabral, LDR, Sato, AP, de Sousa, RS, Rossa, AP, Sanches, AWD, Bortoleto, CT and Dittrich, RL (2022) Detection of Neospora spp. and Sarcocystis neurona in amniotic fluid and placentas from mares. Veterinary Parasitology 303, Article 109678, e1–4. doi: 10.1016/j.vetpar.2022.109678CrossRefGoogle ScholarPubMed
Cheadle, MA, Lindsay, DS, Rowe, S, Dykstra, CC, Williams, MA, Spencer, JA, Toivio-Kinnucan, MA, Lenz, SD, Newton, JC, Rolsma, MD and Blagburn, BL (1999) Prevalence of antibodies to Neospora sp. in horses from Alabama and characterisation of an isolate recovered from a naturally infected horse. International Journal for Parasitology 29, 1537–1543.CrossRefGoogle ScholarPubMed
Cusick, PK, Sells, DM, Hamilton, DP and Hardenbrook, HJ (1974) Toxoplasmosis in two horses. Journal of the American Veterinary Medical Association 164, 77–80.Google ScholarPubMed
Daft, BM, Barr, BC, Collins, N and Sverlow, K (1996) Neospora encephalomyelitis and polyradiculoneuritis in an aged mare with Cushing's disease. Equine Veterinary Journal 28, 240–243.Google Scholar
Dame, JB, MacKay, RJ, Yowell, CA, Cutler, TJ, Marsh, A and Greiner, EC (1995) Sarcocystis falcatula from passerine and psittacine birds: synonymy with Sarcocystis neurona, agent of equine protozoal myeloencephalitis. Journal of Parasitology 81, 930–935.CrossRefGoogle ScholarPubMed
Davis, SW, Speer, CA and Dubey, JP (1991) In vitro cultivation of Sarcocystis neurona from the spinal cord of a horse with equine protozoal myelitis. Journal of Parasitology 77, 789–792.CrossRefGoogle ScholarPubMed
Duarte, PC, Conrad, PA, Barr, BC, Wilson, WD, Ferraro, GL, Packham, AE, Carpenter, TE and Gardner, IA (2004a) Risk of transplacental transmission of Sarcocystis neurona and Neospora hughesi in California horses. Journal of Parasitology 90, 1345–1351.CrossRefGoogle Scholar
Duarte, PC, Conrad, PA, Wilson, WD, Ferraro, GL, Packham, AE, Bowers-Lepore, J, Carpenter, TE and Gardner, IA (2004b) Risk of postnatal exposure to Sarcocystis neurona and Neospora hughesi in horses. American Journal of Veterinary Research 65, 1047–1052.CrossRefGoogle Scholar
Dubey, JP (1974) Toxoplasmosis in horses. Journal of the American Veterinary Medical Association 165, 668.Google ScholarPubMed
Dubey, JP (2000) Prevalence of Sarcocystis species sporocysts in wild caught opossums (Didelphis virginiana). Journal of Parasitology 86, 705–710.CrossRefGoogle Scholar
Dubey, JP (2010) Toxoplasmosis of Animals and Humans, 2nd Edn. Boca Raton, Florida, USA: CRC Press.Google Scholar
Dubey, JP (2022) Toxoplasmosis of Animals and Humans, 3rd Edn. Boca Raton, Florida, USA: CRC Press.Google Scholar
Dubey, JP and Porterfield, ML (1986) Toxoplasma-like sporozoa in an aborted equine fetus. Journal of the American Veterinary Medical Association 188, 1312–1313.Google Scholar
Dubey, JP and Desmonts, G (1987) Serological responses of equids fed Toxoplasma gondii oocysts. Equine Veterinary Journal 19, 337–339.CrossRefGoogle ScholarPubMed
Dubey, JP and Beattie, CP (1988) Toxoplasmosis of Animals and Man. Boca Raton, Florida, USA: CRC Press.Google Scholar
Dubey, JP and Porterfield, ML (1990) Neospora caninum (Apicomplexa) in an aborted equine fetus. Journal of Parasitology 76, 732–734.CrossRefGoogle Scholar
Dubey, JP, Davis, GW, Koestner, A and Kiryu, K (1974) Equine encephalomyelitis due to a protozoan parasite resembling Toxoplasma gondii. Journal of the American Veterinary Medical Association 165, 249–255.Google ScholarPubMed
Dubey, JP, Carpenter, JL, Speer, CA, Topper, MJ and Uggla, A (1988) Newly recognized fatal protozoan disease of dogs. Journal of the American Veterinary Medical Association 192, 1269–1285.Google ScholarPubMed
Dubey, JP, Davis, SW, Speer, CA, Bowman, DD, de Lahunta, A, Granstrom, DE, Topper, MJ, Hamir, AN, Cummings, JF and Suter, MM (1991) Sarcocystis neurona n. sp. (Protozoa: Apicomplexa), the etiologic agent of equine protozoal myeloencephalitis. Journal of Parasitology 77, 212–218.CrossRefGoogle Scholar
Dubey, JP, Saville, WJA, Lindsay, DS, Stich, RW, Stanek, JF, Speer, CA, Rosenthal, BM, Njoku, CJ, Kwok, OCH, Shen, SK and Reed, SM (2000) Completion of the life cycle of Sarcocystis neurona. Journal of Parasitology 86, 1276–1280.CrossRefGoogle ScholarPubMed
Dubey, JP, Fritz, D, Lindsay, DS, Shen, SK, Kwok, OCH and Thompson, KC (2001a) Diclazuril preventive therapy of gamma interferon knockout mice fed Sarcocystis neurona sporocysts. Veterinary Parasitology 94, 257–264.CrossRefGoogle Scholar
Dubey, JP, Liddell, S, Mattson, D, Speer, CA, Howe, DK and Jenkins, MC (2001b) Characterization of the Oregon isolate of Neospora hughesi from a horse. Journal of Parasitology 87, 345–353.CrossRefGoogle Scholar
Dubey, JP, Lindsay, DS, Saville, WJA, Reed, SM, Granstrom, DE and Speer, CA (2001c) A review of Sarcocystis neurona and equine protozoal myeloencephalitis (EPM). Veterinary Parasitology 95, 89–131.CrossRefGoogle Scholar
Dubey, JP, Howe, DK, Furr, M, Saville, WJ, Marsh, AE, Reed, SM and Grigg, ME (2015) An update on Sarcocystis neurona infections in animals and equine protozoal myeloencephalitis (EPM). Veterinary Parasitology 209, 1–42.CrossRefGoogle Scholar
Dubey, JP, Calero-Bernal, R, Rosenthal, BM, Speer, CA and Fayer, R (2016) Sarcocystosis of Animals and Humans, 2nd Edn. Boca Raton, Florida, USA: CRC Press.Google Scholar
Dubey, JP, Hemphill, A, Calero-Bernal, R and Schares, G (2017a) Neosporosis in Animals. Boca Raton, Florida, USA: CRC Press. doi:10.1201/9781315152561CrossRefGoogle Scholar
Dubey, R, Harrison, B, Dangoudoubiyam, S, Bandini, G, Cheng, K, Kosber, A, Agop-Nersesian, C, Howe, DK, Samuelson, J, Ferguson, DJP and Gubbels, MJ (2017b) Differential roles for inner membrane complex proteins across Toxoplasma gondii and Sarcocystis neurona development. mSphere 2, e00409–17.CrossRefGoogle Scholar
Dubey, JP, Murata, FHA, Cerqueira-Cézar, CK and Kwok, OCH (2020) Toxoplasma gondii infections in horses, donkeys, and other equids: the last decade. Research in Veterinary Science 132, 492–499.CrossRefGoogle ScholarPubMed
Evers, F, Garcia, JL, Navarro, IT, Zulpo, DL, Nino, BSL, Ewald, MPC, Pagliari, S, de Almeida, JC and Freire, RL (2013) Diagnosis and isolation of Toxoplasma gondii in horses from Brazilian slaughterhouses. Revista Brasileira de Parasitologia Veterinária 22, 58–63.CrossRefGoogle ScholarPubMed
Feldman, HA and Miller, LT (1956) Serological study of toxoplasmosis prevalence. American Journal of Hygiene 64, 320–335.Google ScholarPubMed
Fenger, CK, Granstrom, DE, Langemeier, JL, Stamper, S, Donahue, JM, Patterson, JS, Gajadhar, AA, Marteniuk, JV, Xiaomin, Z and Dubey, JP (1995) Identification of opossums (Didelphis virginiana) as the putative definitive host of Sarcocystis neurona. Journal of Parasitology 81, 916–919.CrossRefGoogle ScholarPubMed
Fenger, CK, Granstrom, DE, Gajadhar, AA, Williams, NM, McCrillis, SA, Stamper, S, Langemeier, JL and Dubey, JP (1997) Experimental induction of equine protozoal myeloencephalitis in horses using Sarcocystis sp. Sporocysts from the opossum (Didelphis virginiana). Veterinary Parasitology 68, 199–213.CrossRefGoogle Scholar
Finno, CJ, Aleman, M and Pusterla, N (2007) Equine protozoal myeloencephalitis associated with neosporosis in 3 horses. Journal of Veterinary Internal Medicine 21, 1405–1408.CrossRefGoogle ScholarPubMed
Finno, CJ, Eaton, JS, Aleman, M and Hollingsworth, SR (2010) Equine protozoal myeloencephalitis due to Neospora hughesi and equine motor neuron disease in a mule. Veterinary Ophthalmology 13, 259–265.CrossRefGoogle Scholar
Furr, M and Kennedy, T (2020) Effects of coadministration of corn oil and ponazuril on serum and cerebrospinal fluid concentrations of ponazuril in horses. Journal of Veterinary Internal Medicine 34, 1321–1324.CrossRefGoogle ScholarPubMed
Gaji, RY, Zhang, D, Breathnach, CC, Vaishnava, S, Striepen, B and Howe, DK (2006) Molecular genetic transfection of the coccidian parasite Sarcocystis neurona. Molecular and Biochemical Parasitology 150, 1–9.CrossRefGoogle ScholarPubMed
Gomes, FA, Jansen, AM, Machado, RZ, Pena, HFJ, Fumagalli, MJ, Silva, A, Alves, BF, Roque, ALR and Figueiredo, LTM (2019) Serological evidence of arboviruses and coccidia infecting horses in the Amazonian region of Brazil. PLoS ONE 14, e0225895.CrossRefGoogle ScholarPubMed
Gondim, LFP, Soares, RM, Tavares, AS, Borges-Silva, W, de Jesus, RF, Llano, HAB and Gondim, LQ (2019) Sarcocystis falcatula-like derived from opossum in Northeastern Brazil: in vitro propagation in avian cells, molecular characterization and bioassay in birds. International Journal for Parasitology: Parasites and Wildlife 10, 132–137.Google ScholarPubMed
Gray, ML, Harmon, BG, Sales, L and Dubey, JP (1996) Visceral neosporosis in a 10-year-old horse. Journal of Veterinary Diagnostic Investigation 8, 130–133.CrossRefGoogle Scholar
Granstrom, DE, MacPherson, JM, Gajadhar, AA, Dubey, JP, Tramontin, R and Stamper, S (1994) Differentiation of Sarcocystis neurona from eight related coccidia by random amplified polymorphic DNA assay. Molecular Cellular Probes 8, 353–356. doi: 10.1006/mcpr.1994.1051CrossRefGoogle ScholarPubMed
Hamir, AN, Tornquist, SJ, Gerros, TC, Topper, MJ and Dubey, JP (1998) Neospora caninum-associated equine protozoal myeloencephalitis. Veterinary Parasitology 79, 269–274.CrossRefGoogle ScholarPubMed
Henker, LC, Bandinelli, MB, de Andrade, CP, Bianchi, MV, Sonne, L, Driemeier, D, Soares, JF and Pavarini, SP (2020) Pathological, immunohistochemical, and molecular findings of equine protozoal myeloencephalitis due to Sarcocystis neurona infection in Brazilian horses. Tropical Animal Health and Production 52, 3809–3817.CrossRefGoogle ScholarPubMed
Howe, DK, Yeargan, M, Simpson, L and Dangoudoubiyam, S (2018) Molecular genetic manipulation of Sarcocystis neurona. Current Protocols in Microbiology 48, 20D.2.1–20D.2.14.CrossRefGoogle ScholarPubMed
Hunyadi, L, Papich, MG and Pusterla, N (2015) Pharmacokinetics of a low dose and FDA-labeled dose of diclazuril administered orally as a pelleted topdressing in adult horses. Journal of Veterinary Pharmacology and Therapeutics 38, 243–248.CrossRefGoogle ScholarPubMed
Hunyadi, L, Papich, MG and Pusterla, N (2018) Diclazuril nonlinear mixed-effects pharmacokinetic modelling of plasma concentrations after oral administration to adult horses every 3–4 days. Veterinary Journal 242, 74–76.CrossRefGoogle ScholarPubMed
James, KE, Smith, WA, Conrad, PA, Packham, AE, Guerrero, L, Ng, M and Pusterla, N (2015) Seroprevalence of Sarcocystis neurona and Neospora hughesi among healthy horses in the United States. Proceedings of the American Association of Equine Practitioners 61, 524.Google Scholar
James, KE, Smith, WA, Packham, AE, Conrad, PA and Pusterla, N (2017) Toxoplasma gondii seroprevalence and association with equine protozoal myeloencephalitis: a case-control study of Californian horses. Veterinary Journal 224, 38–43.CrossRefGoogle ScholarPubMed
Khan, A, Fujita, AW, Randle, N, Regidor-Cerrillo, J, Shaik, JS, Shen, K, Oler, AJ, Quinones, M, Latham, SM, Akanmori, BD, Cleaveland, S, Innes, EA, Ryan, U, Šlapeta, J, Schares, G, Ortega-Mora, LM, Dubey, JP, Wastling, JM and Grigg, ME (2019) Global selective sweep of a highly inbred genome of the cattle parasite Neospora caninum. Proceedings of the National Academy of Sciences of the United States of America 116, 22764–22773.CrossRefGoogle ScholarPubMed
Kimble, KM, Gomez, G, Szule, JA, Dubey, JP, Buchanan, B and Porter, BF (2021) Systemic toxoplasmosis in a horse. Journal of Comparative Pathology 182, 27–31.CrossRefGoogle ScholarPubMed
Klun, I, Uzelac, A, Villena, I, Mercier, A, Bobić, B, Nikolić, A, Rajnpreht, I, Opsteegh, M, Aubert, D, Blaga, R, van der Giessen, J and Djurković-Djaković, O (2017) The first isolation and molecular characterization of Toxoplasma gondii from horses in Serbia. Parasites & Vectors 10, 167.CrossRefGoogle ScholarPubMed
Leon, A, Richard, E, Fortier, C, Laugier, C, Fortier, G and Pronost, S (2012) Molecular detection of Coxiella burnetii and Neospora caninum in equine aborted foetuses and neonates. Preventive Veterinary Medicine 104, 179–183.CrossRefGoogle ScholarPubMed
Lindsay, DS, Steinberg, H, Dubielzig, RR, Semrad, SD, Konkle, DM, Miller, PE and Blagburn, BL (1996) Central nervous system neosporosis in a foal. Journal of Veterinary Diagnostic Investigation 8, 507–510.CrossRefGoogle Scholar
Lindsay, DS, Nazir, MM, Maqbool, A, Ellison, SP and Strobl, JS (2013) Efficacy of decoquinate against Sarcocystis neurona in cell cultures. Veterinary Parasitology 196, 21–23.CrossRefGoogle ScholarPubMed
Locatelli-Dittrich, R, Dittrich, JR, Richartz, RRTB, Gasino Joineau, ME, Antunes, J, Pinckney, RD, Deconto, I, Hoffmann, DCS and Thomaz-Soccol, V (2006) Investigation of Neospora sp. and Toxoplasma gondii antibodies in mares and in precolostral foals from Parana State, Southern Brazil. Veterinary Parasitology 135, 215–221.CrossRefGoogle ScholarPubMed
Lorenzi, H, Khan, A, Behnke, MS, Namasivayam, S, Swapna, LS, Hadjithomas, M, Karamycheva, S, Pinney, D, Brunk, BP, Ajioka, JW, Ajzenberg, D, Boothroyd, JC, Boyle, JP, Dardé, ML, Diaz-Miranda, MA, Dubey, JP, Fritz, HM, Gennari, SM, Gregory, BD, Kim, K, Saeij, JPJ, Su, C, White, MW, Zhu, XQ, Howe, DK, Rosenthal, BM, Grigg, ME, Parkinson, J, Liu, L, Kissinger, JC, Roos, DS and Sibley, LD (2016) Local admixture of amplified and diversified secreted pathogenesis determinants shapes mosaic Toxoplasma gondii genomes. Nature Communications 7, 10147.CrossRefGoogle ScholarPubMed
Marsh, AE, Barr, BC, Madigan, J, Lakritz, J, Nordhausen, R and Conrad, PA (1996) Neosporosis as a cause of equine protozoal myeloencephalitis. Journal of the American Veterinary Medical Association 209, 1907–1913.Google ScholarPubMed
Marsh, AE, Barr, BC, Packham, AE and Conrad, PA (1998) Description of a new Neospora species (Protozoa: Apicomplexa: Sarcocystidae). Journal of Parasitology 84, 983–991.CrossRefGoogle Scholar
Mayhew, IG, de Lahunta, A, Whitlock, RH and Pollock, RVH (1976) Equine protozoal myeloencephalitis. In: Proceedings of the 22nd Annual Convention of the American Association of Equine Practitioners, Dallas, Texas, USA. November–December, pp. 107–114.Google Scholar
Mazuz, ML, Mimoun, L, Schvartz, G, Tirosh-Levy, S, Savitzki, I, Edery, N, Blum, SE, Baneth, G, Pusterla, N and Steinman, A (2020) Detection of Neospora caninum infection in aborted equine fetuses in Israel. Pathogens (Basel, Switzerland) 9, 962.Google Scholar
Mittelman, NS, Stefanovski, D and Johnson, AL (2018) Utility of C-reactive protein and serum amyloid A in the diagnosis of equine protozoal myeloencephalitis. Journal of Veterinary Internal Medicine 32, 1726–1730.CrossRefGoogle Scholar
Munday, BL (1970) The epidemiology of toxoplasmosis with particular reference to the Tasmanian environment (Master's Thesis). University of Sydney.Google Scholar
Ojo, KK, Dangoudoubiyam, S, Verma, SK, Scheele, S, Derocher, AE, Yeargan, M, Choi, R, Smith, TR, Rivas, KL, Hulverson, MA, Barrett, LK, Fan, E, Maly, DJ, Parsons, M, Dubey, JP, Howe, DK and Van Voorhis, WC (2016) Selective inhibition of Sarcocystis neurona calcium-dependent protein kinase 1 for equine protozoal myeloencephalitis therapy. International Journal for Parasitology 46, 871–880.CrossRefGoogle ScholarPubMed
Packham, AE, Conrad, PA, Wilson, WD, Jeanes, LV, Sverlow, KW, Gardner, IA, Daft, BM, Marsh, AE, Blagburn, BL, Ferraro, GL and Barr, BC (2002) Qualitative evaluation of selective tests for detection of Neospora hughesi antibodies in serum and cerebrospinal fluid of experimentally infected horses. Journal of Parasitology 88, 1239–1246.CrossRefGoogle ScholarPubMed
Paştiu, AI, Györke, A, Kalmár, Z, Bolfǎ, P, Rosenthal, BM, Oltean, M, Villena, I, Spînu, M and Cozma, V (2015) Toxoplasma gondii in horse meat intended for human consumption in Romania. Veterinary Parasitology 212, 393–395.CrossRefGoogle ScholarPubMed
Pena, HFJ, Pinheiro, TM, Soares, HS, Oliveira, S, Alves, BF, Ferreira, MN and Gennari, SM (2018) Typical Brazilian genotype of Toxoplasma gondii isolated from a horse destined for human consumption in Europe from a slaughterhouse. Parasitology Research 117, 3305–3308.CrossRefGoogle ScholarPubMed
Pitel, PH, Romand, S, Pronost, S, Foucher, N, Gargala, G, Maillard, K, Thulliez, P, Collobert-Laugier, C, Tainturier, D, Fortier, G and Ballet, JJ (2003) Investigation of Neospora sp. antibodies in aborted mares from Normandy, France. Veterinary Parasitology 118, 1–6.CrossRefGoogle ScholarPubMed
Pivoto, FL, de Macêdo Junior, AG, da Silva, MV, Ferreira, FB, Silva, DAO, Pompermayer, E, Sangioni, LA, Mineo, TWP and Vogel, FSF (2014) Serological status of mares in parturition and the levels of antibodies (IgG) against protozoan family Sarcocystidae from their pre colostral foals. Veterinary Parasitology 199, 107–111.CrossRefGoogle ScholarPubMed
Pomares, C, Ajzenberg, D, Bornard, L, Bernardin, G, Hasseine, L, Dardé, ML and Marty, P (2011) Toxoplasmosis and horse meat, France. Emerging Infectious Diseases 17, 1327–1328.CrossRefGoogle ScholarPubMed
Pronost, S, Pitel, PH, Romand, S, Thulliez, P, Collobert, C and Fortier, G (1999) Neospora caninum: première mise en évidence en France sur un avorton équin, analyse et perspectives. Pratique Véterinaire Equine 31, 111–114.Google Scholar
Pusterla, N, Conrad, PA, Packham, AE, Mapes, SM, Finno, CJ, Gardner, IA, Barr, BC, Ferraro, GL and Wilson, WD (2011) Endogenous transplacental transmission of Neospora hughesi in naturally infected horses. Journal of Parasitology 97, 281–285.CrossRefGoogle ScholarPubMed
Pusterla, N, Mackie, S, Packham, A and Conrad, PA (2014a) Serological investigation of transplacental infection with Neospora hughesi and Sarcocystis neurona in broodmares. Veterinary Journal 202, 649–650.CrossRefGoogle Scholar
Pusterla, N, Tamez-Trevino, E, White, A, VanGeem, J, Packham, A, Conrad, PA and Kass, P (2014b) Comparison of prevalence factors in horses with and without seropositivity to Neospora hughesi and/or Sarcocystis neurona. Veterinary Journal 200, 332–334.CrossRefGoogle Scholar
Reed, SM, Furr, M, Howe, DK, Johnson, AL, MacKay, RJ, Morrow, JK, Pusterla, N and Witonsky, S (2016) Equine protozoal myeloencephalitis: an updated consensus statement with a focus on parasite biology, diagnosis, treatment, and prevention. Journal of Veterinary Internal Medicine 30, 491–502.CrossRefGoogle Scholar
Rooney, JR, Prickett, ME, Delaney, FM and Crowe, MW (1970) Focal myelitis-encephalitis in horses. Cornell Veterinarian 50, 494–501.Google Scholar
Saville, WJA, Reed, SM, Dubey, JP, Granstrom, DE, Morley, PS, Hinchcliff, KW, Kohn, CW, Wittum, TE and Workman, JD (2017) Interobserver variation in the diagnosis of neurologic abnormalities in the horse. Journal of Veterinary Internal Medicine 31, 1871–1876.CrossRefGoogle Scholar
Schale, S, Howe, D, Yeargan, M, Morrow, JK, Graves, A and Johnson, AL (2018) Protozoal coinfection in horses with equine protozoal myeloencephalitis in the eastern United States. Journal of Veterinary Internal Medicine 32, 1210–1214.CrossRefGoogle ScholarPubMed
Thilsted, JP and Dubey, JP (1989) Neosporosis-like abortions in a herd of dairy cattle. Journal of Veterinary Diagnostic Investigation 1, 205–209.CrossRefGoogle Scholar
Vaishnava, S, Morrison, DP, Gaji, RY, Murray, JM, Entzeroth, R, Howe, DK and Striepen, B (2005) Plastid segregation and cell division in the apicomplexan parasite Sarcocystis neurona. Journal of Cell Science 118, 3397–3407.CrossRefGoogle ScholarPubMed
Van Voorhis, WC, Doggett, JS, Parsons, M, Hulverson, MA, Choi, R, Arnold, S, Riggs, MW, Hemphill, A, Howe, DK, Mealey, RH, Lau, AOT, Merritt, EA, Maly, DJ, Fan, E and Ojo, KK (2017) Extended-spectrum antiprotozoal bumped kinase inhibitors: a review. Experimental Parasitology 180, 71–83.CrossRefGoogle ScholarPubMed
Vardeleon, D, Marsh, AE, Thorne, JG, Loch, W, Young, R and Johnson, PJ (2001) Prevalence of Neospora hughesi and Sarcocystis neurona antibodies in horses from various geographical locations. Veterinary Parasitology 95, 273–282.CrossRefGoogle ScholarPubMed
Veronesi, F, Diaferia, M, Mandara, MT, Marenzoni, ML, Cittadini, F and Piergili Fioretti, D (2008) Neospora spp. infection associated with equine abortion and/or stillbirth rate. Veterinary Research Communications 32(Suppl. 1), S223–S226.CrossRefGoogle ScholarPubMed
Wobeser, BK, Godson, DL, Rejmanek, D and Dowling, P (2009) Equine protozoal myeloencephalitis caused by Neospora hughesi in an adult horse in Saskatchewan. Canadian Veterinary Journal 50, 851–853.Google Scholar
Zhou, M, Cao, S, Sevinc, F, Sevinc, M, Ceylan, O, Liu, M, Wang, G, Moumouni, PFA, Jirapattharasate, C, Suzuki, H, Nishikawa, Y and Xuan, X (2016) Enzyme-linked immunosorbent assays using recombinant TgSAG2 and NcSAG1 to detect Toxoplasma gondii and Neospora caninum-specific antibodies in domestic animals in Turkey. Journal of Veterinary Medical Science 78, 1877–1881.CrossRefGoogle ScholarPubMed