Abstract
Neosporosis and toxoplasmosis are important parasitic causes of abortions in small ruminants. This study verified the occurrence of these diseases in sheep fetuses from Santa Catarina State, Southern Brazil from 2015 to 2022. Sheep fetuses were necropsied with organ sampling for histopathology, and polymerase chain reaction (PCR) for Neospora caninum and Toxoplasma gondii using the Nc5 and SAG2 targets, respectively, in frozen brain tissue. Microbiological culture and RT-PCR for Pestivirus were conducted to discard other abortion causes. One positive fetus for toxoplasmosis was genotyped using multiplex multilocus nested PCR-RFLP (Mn-PCR-RFLP) with ten genetic markers. Fifty-five sheep fetuses were evaluated, with 10 (18.2%) cases of neosporosis and 7 (12.7%) cases of toxoplasmosis, comprising six and four flocks, respectively. Macroscopically, neosporosis abortions exhibited fetal mummification, maceration, and arthrogryposis. Toxoplasmosis abortions showed fetal mummification and maceration. The neosporosis abortions included lymphoplasmacytic myositis (70%; 7/10) and myocarditis (60%; 6/10), in addition to necrotizing encephalitis and gliosis (50%; 5/10). Toxoplasmosis abortions included lymphoplasmacytic necrotizing encephalitis (71.4%; 5/7), lymphoplasmacytic myositis (42.8%, 3/7), and myocarditis (14.3%; 1/7). Through PCR, N. caninum and T. gondii were detected in 6 (60%) and 5 (71.4%) fetuses, respectively. In one fetus, T. gondii genotyping was conducted, which was characterized as atypical genotype ToxoDB #98. All of the cases were negative for Pestivirus and bacterial agents. This study establishes the occurrence of these diseases as causes of abortions, malformations, mummification, and fetal maceration in sheep, with the characterization of an atypical T. gondii genotype in one of the fetuses.
Similar content being viewed by others
Data availability
The data that support the findings of this study are openly available.
References
Buxton D (1991) Toxoplasmosis. In: Martin WB, Aitken ID (eds) Diseases of Sheep, 2nd edn. Blackwell Scientific Publications, Oxford, pp 49–58
Calandra PM, Di Matía JM, Cano DB et al (2014) Endemic and epidemic bovine neosporosis: description of two events in beef cattle. Rev Arg Microbiol 46(4):315–319
Dardé ML, Bouteille B, Pestre-Alexandre M (1992) Isoenzyme analysis of 35 Toxoplasma gondii isolates and the biological and epidemiological implications. J Parasitol 78:786–794
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 Guiana. J Clin Microbiol 36(1):324
Feitosa TF, Vilela VLR, Batista SP et al (2024) Genetic diversity of Toxoplasma gondii in goats and sheep from the Northeast Region of Brazil destined for human consumption. Curr Res Parasitol Vector Borne Dis 5:100163
Gabardo MP, Oliveira JSV, Ecco R et al (2013) Outbreak of ovine abortion by toxoplasmosis in Southeastern Brazil. Braz J Vet Pathol 6(1):37–41
Garcia-Perez AL, Moreno B, Aduriz G (2003) Necropsia y toma de muestras de abortos ovinos. Rev Ovis 86:65–76
Henker LC, Vogel FSF, Cecco BS et al (2022) Abortion outbreak in a sheep flock caused by Toxoplasma gondii clonal type III. Parasitol Res 121:2633–2639
Howe DK, Sibley LD (1995) Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotype with human disease. J Infec Dis 172:1561–1566
Hurtado A, Aduriz G, Moreno B et al (2001) Single tube nested PCR for the detection of Toxoplasma gondii in fetal tissues from naturally aborted ewes. Vet Parasitol 102(1–2):17–27
Innes EA, Bartley PM, Buxton D (2009) Ovine toxoplasmosis. Parasitology 136(14):1887–1894
Instituto Brasileiro de Geografia e Estatística (2022) Rebanho de Ovinos (Ovelhas e Carneiros). https://www.ibge.gov.br/explica/producao-agropecuaria/ovino/sc. Accessed 28 Feb 2024
Isola J, DeVries S, Chu L et al (1994) Analysis of changes in DNA sequence copy number by comparative genomic hybridization in archival paraffin-embedded tumor samples. Am J Pathol 145(6):1301–1308
Lindsay DS, Dubey JP (2020) Neosporosis, Toxoplasmosis and Sarcocystosis in Ruminants. Vet Clin North Am Food Anim Pract 36(1):205–222
Masala G, Porcu R, Daga C et al (2007) Detection of pathogens in ovine and caprine abortion samples from Sardinia Italy by PCR. J Am Vet Med Assoc 19:96–98
McAllister MM, McGuire AM, Jolley WR et al (1996) Experimental neosporosis in pregnant ewes and their offspring. Vet Pathol 33(6):647–655
Meixner N, Sommer MF, Scuda N et al (2020) Comparative aspects of laboratory testing foi the detection of Toxoplasma gondii and its differentiation from Neospora caninum as the etiologic agent of ovine abortion. J Vet Diagn Invest 32(6):898–907
Moreno B, Collantes-Fernández E, Villa A et al (2012) Occurrence of Neospora caninum and Toxoplasma gondii infections in ovine and caprine abortions. Vet Parasitol 187(1–2):312–318
Moura AB, Silva MO, Trevisani N et al (2015) Toxoplasma gondii: soroprevalência e fatores de risco em ovelhas no planalto serrano de Santa Catarina Brasil. Rev Inst Adolfo Lutz 74(3):200–206
Müller N, Zimmermann V, Hentrich B et al (1996) Diagnosis of Neospora caninum and Toxoplasma gondii infection by PCR and DNA hybridization immunoassay. J Clin Microbiol 34(11):2850–2852
Oliveira JMB, Almeida JC, Melo RPB et al (2018) First description of clonal lineage type II (genotype #1) of Toxoplasma gondii in abortion outbreak in goats. Exp Parasitol 188(2018):21–25
Ossani RA, Borges HAT, Souza AP et al (2017) Toxoplasma gondii in milk of naturally infected dairy ewes on west mesoregion of Santa Catarina state, Brazil. Arq Bras Med Vet Zootec 69:1294–1300
Pereira-Bueno J, Quintanilla-Gonzalo A, Pérez-Pérez V et al (2004) Evaluation of ovine abortion associated with Toxoplasma gondii in Spain by different diagnostic techniques. Vet Parasitol 121(1–2):33–43
Pinto AP, Bacha FB, Santos BS et al (2012) Sheep abortion associated with Neospora caninum in Mato Grosso do Sul Brazil. Pesq Vet Bras 32(8):739–742
Qian W, Wang H, Su C et al (2012) Isolation and characterization of Toxoplasma gondii strains from stray cats revealed a single genotype in Beijing China. Vet Parasitol 187(3–4):408–413
Rosa LD, Moura AB, Güths MF et al (2011) Prevalence and risk factors for infection of Neospora caninum in sheep from Lages county, Santa Catarina State, Brazil. Rev Cienc Agrovet 10(2):127–137
Sakata FBLS, Bellato V, Sartor AA (2012) Anticorpos toxoplásmicos em ovinos de Lages, Santa Catarina, Brasil, e comparação utilizando RIFI e ELISA. Rev Bras Parasitol Vet 21(3):196–200
Schwab EK, Zhu XQ, Majumdar D et al (2014) Geographical patterns of Toxoplasma gondii genetic diversity revealed by multilocus PCR-RFLP genotyping. Parasitology 141(4):453–461
Sivachelvan MN, Ghali Ali M, Chibuzo GA (1996) Foetal age estimation in sheep and goats. Small Rumin Res 19(1):69–76
Su C, Shwab EK, Zhou P, Zhu XQ, Dubey JP (2010) Moving towards an integrated approach to molecular detection and identification of Toxoplasma gondii. Parasitology 137:1–11
Weber MN, Silveira S, Machado G et al (2014) High frequency of bovine viral diarrhea virus type 2 in Southern Brazil. Virus Res 295:117–124
Withoeft JA, Costa LS, Marian L et al (2022) Microcephaly and hydrocephalus in a sheep fetus infected with Neospora caninum in Southern Brazil – Short communication. Acta Vet Hung 70(3):226–229
Woods LW, Anderson ML (1992) Scoliosis and hydrocephalus in an ovine fetus infected with Toxoplasma gondii. J Vet Diagn Invest 4(2):220–222
Funding
Funding for this work was obtained from the Fundação de Amparo à Pesquisa e Inovação do Estado de Santa Catarina (FAPESC, 05/2018 – No.: 2019TR702) and by the Programa de Apoio à Pós-Graduação maintained by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (PROAP/CAPES, Finance code 001).
Author information
Authors and Affiliations
Contributions
J.A. Withoeft, L. Marian and R.A. Casagrande: wrote the main text and produced the images.
J.A. Withoeft, L. Marian, L.S. Costa, G.B. das Neves, M.G.L. Pinto, L.C. Miletti, R.A. Casagrande: performed the clinical, anatomopathological and molecular examination and diagnostic.
F.D. Fernandes and F.S.F Vogel: performed the genotyping of the samples. All authors reviewed the manuscript.
Corresponding author
Ethics declarations
Animal ethics
Not applicable.
Consent to participate
An Informed Consent Form was applied to sheep farmers to provide epidemiological information about their farm.
Consent for publication
Not applicable.
Conflict of Interest
The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Withoeft, J.A., Marian, L., da Costa, L.S. et al. Sheep abortions associated with Neospora caninum and Toxoplasma gondii infections in multiple flocks from Southern Brazil. Vet Res Commun (2024). https://doi.org/10.1007/s11259-024-10390-4
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11259-024-10390-4