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Acta Parasitologica

, Volume 64, Issue 4, pp 950–955 | Cite as

Ovine Abortion by Neospora caninum: First Case Reported in Argentina

  • Yanina P. HeckerEmail author
  • Eleonora L. Morrell
  • María A. Fiorentino
  • Ignacio Gual
  • Emilia Rivera
  • Franco Fiorani
  • Matías A. Dorsch
  • María L. Gos
  • Lais L. Pardini
  • María V. Scioli
  • Sergio Magariños
  • Fernando A. Paolicchi
  • Germán J. Cantón
  • Dadín P. Moore
Case report

Abstract

Purpose

The aim of this study was to describe for the first time a natural case of ovine abortion associated with Neospora caninum in a flock with reproductive losses in Argentina.

Materials and Methods

The analyzed flock consisted of 256 Texel sheep, of which 134 had been mated. A single blood sample was obtained by jugular vein puncture from 220 ewes (116 adult ewes, 104 yearling ewes) and 93 lambs. Serum samples and fetal fluid were tested using the indirect fluorescence antibody test to detect antibodies against N. caninum and T. gondii. Fetal and placental tissues from aborted fetus were examined by standard gross pathology procedures and were tested using histopathology and immunohistochemistry. Moreover, DNA from fetal and placental tissues was isolated and a PCR assay to detect N. caninum, T. gondii and Chlamydia spp. was used.

Results and Discussion

The pregnancy rate was 89% (119/134), the abortion rate was 8.4% (10/119) whereas the perinatal mortality rate was 15% (16/109). Out of 116 adult ewes sampled, 34.48% presented anti-N. caninum antibodies. Ten ewes had aborted, and one fetus was directly submitted to the diagnostic laboratory for further processing. Antibodies against N. caninum were detected in fetal fluid and in the aborted dam. Histopathological analysis in fetal tissues showed multifocal lymphohistiocytic glossitis, diffuse mild lymphohistiocytic endocarditis, pericarditis and focally extensive myocarditis. Severe multifocal necrotizing placentitis and diffuse mild lymphohistiocytic placentitis with the presence of lymphohistiocytic vasculitis were observed in placenta. N. caninum was immunolabeled in the placenta and fetal tongue. In addition, N. caninum DNA was detected in placenta, central neural system, lung and heart of the aborted fetus. There was no evidence of other infectious abortifacients in the aborted fetus.

Conclusion

The present study described for the first time an ovine abortion caused by N. caninum in Argentina. Further investigations at a larger scale are required to establish the role of N. caninum as an important cause of reproductive losses in sheep flocks from the region.

Keywords

Neospora caninum Reproductive losses Abortion Ovine 

Notes

Acknowledgements

This work was funded by a Research Grant from a Research Grants from Agencia Nacional de Promoción Científica y Tecnológica, FONCyT, PICT 2016-0195 and INTA PE 115055, Argentina and Red CYTED113RT0469 (PROTOZOOVAC). The authors thank Dr. Paola Della Rosa for their technical assistance.

Compliance with ethical standards

Conflict of interest

There are no financial or personal relationships with other people or organizations that could inappropriately influence this work.

References

  1. 1.
    Bartley PM, Guido S, Mason C, Stevenson H, Chianini F, Carty H, Innes EA, Katzer F (2019) Detection of Neospora caninum DNA in cases of bovine and ovine abortion in the South-West of Scotland. Parasitology 146:979–982.  https://doi.org/10.1017/S0031182019000301 CrossRefPubMedGoogle Scholar
  2. 2.
    Basso W, Venturini MC, Bacigalupe D, Kienast M, Unzaga JM, Larsen A, Machuca M, Venturini L (2005) Confirmed clinical Neospora caninum infection in a boxer puppy from Argentina. Vet Parasitol 131:299–303.  https://doi.org/10.1016/j.vetpar.2005.05.003 CrossRefPubMedGoogle Scholar
  3. 3.
    Bishop S, King J, Windsor P, Reichel MP, Ellis J, Slapeta J (2010) The first report of ovine cerebral neosporosis and evaluation of Neospora caninum prevalence in sheep in New South Wales. Vet Parasitol 170:137–142.  https://doi.org/10.1016/j.vetpar.2010.01.030 CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Buxton D, Maley SW, Wright S, Thompson KM, Rae AG, Innes EA (1998) The pathogenesis of experimental neosporosis in pregnant sheep. J Comp Pathol 118:267–279.  https://doi.org/10.1016/S0021-9975(07)80003-X CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Campero CM, Moore DP, Odeón AC, Cipolla AL, Odriozola E (2003) Aetiology of bovine abortion in Argentina. Vet Res Commun 27:359–369.  https://doi.org/10.1023/A:1024754003432 CrossRefPubMedGoogle Scholar
  6. 6.
    Campero LM, Gos ML, Moore DP, Regidor-Cerrillo J, Unzaga JM, Moré G, Ortega-Mora LM, Venturini MC (2018) Microsatellite pattern analysis of Neospora caninum from a naturally infected goat fetus. Vet Parasitol 255:58–60.  https://doi.org/10.1016/j.vetpar.2018.03.024 CrossRefPubMedGoogle Scholar
  7. 7.
    Dubey JP, Hartley WJ, Lindsay DS, Topper MJ (1990) Fatal congenital Neospora caninum infection in a lamb. J Parasitol 76:127–130.  https://doi.org/10.2307/3282640 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Dubey JP (2009) Toxoplasmosis in sheep—the last 20 years. Vet Parasitol 163:1–14.  https://doi.org/10.1016/j.vetpar.2009.02.026 CrossRefPubMedGoogle Scholar
  9. 9.
    Dubey JP, Shares G (2011) Neosporosis in animals—the last five years. Vet Parasitol 180:90–108.  https://doi.org/10.1016/j.vetpar.2011.05.031 CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Dubey JP, Hemphill A, Calero-Bernal R, Shares G (2017) Neosporosis in animals, 1st edn. CRC Press, FloridaCrossRefGoogle Scholar
  11. 11.
    Figliuolo LPC, Kasai N, Ragozo AMA, Paula VSO, Dias RA, Souza SLP, Gennari SM (2004) Prevalence of anti-Toxoplasma gondii and anti-Neospora caninum antibodies in ovine from São Paulo State, Brazil. Vet Parasitol 123:161–166.  https://doi.org/10.1016/j.vetpar.2004.06.006 CrossRefPubMedGoogle Scholar
  12. 12.
    Fiorentino MA, Stazionati M, Hecker Y, Morsella C, Cantón G, Romero Harry H, Velilla AV, Gallo Vaulet L, Rodríguez Fermepin M, Bedotti DO (2017) Campylobacter fetus subsp. fetus ovine abortion outbreak in Argentina. Revista Electrónica de Veterinaria 18: 11. http://www.veterinaria.org/revistas/redvet/n111117/111717.html
  13. 13.
    González-Warleta M, Castro-Hermida JA, Regidor-Cerrillo J, Benavides J, Álvarez-García G, Fuertes M, Ortega-Mora LM, Mezo M (2014) Neospora caninum infection as a cause of reproductive failure in a sheep flock. Vet Res 45:88.  https://doi.org/10.1186/s13567-014-0088-5 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    González-Warleta M, Castro-Hermida JA, Calvo C, Pérez V, Gutiérrez-Expósito D, Regidor-Cerrillo J, Ortega-Mora LM, Mezo M (2018) Endogenous transplacental transmission of Neospora caninum during successive pregnancies across three generations of naturally infected sheep. Vet Res 49:106.  https://doi.org/10.1186/s13567-018-0601-3 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Gual I, Giannitti F, Hecker YP, Shivers J, Entrocassi AC, Morrell EL, Pardini L, Fiorentino MA, Rodríguez Fermepin M, Unzaga JM, Cantón GJ, Venturini MC, Moore DP (2018) First case report of Toxoplasma gondii-induced abortions and stillbirths in sheep in Argentina. Vet Parasitol Reg Stud Rep 12:39–42.  https://doi.org/10.1016/j.vprsr.2018.01.001 CrossRefGoogle Scholar
  16. 16.
    Hässig M, Sager H, Reitt K, Ziegler D, Strabel D, Gottstein B (2003) Neospora caninum in sheep: a herd case report. Vet Parasitol 11:213–220.  https://doi.org/10.1016/j.vetpar.2003.07.029 CrossRefGoogle Scholar
  17. 17.
    Hecker Y, Moore DP, Manazza JA, Unzaga JM, Spath EJA, Pardini LL, Venturini MC, Roberi JL, Campero CM (2013) First report of seroprevalence of Toxoplasma gondii and Neospora caninum in dairy sheep from Humid Pampa, Argentina. Trop Anim Health Prod 45:1645–1647.  https://doi.org/10.1007/s11250-013-0396-1 CrossRefPubMedGoogle Scholar
  18. 18.
    Hecker YP, Moore DP, Quattrocchi V, Regidor-Cerrillo J, Verna A, Leunda MR, Morrell E, Ortega-Mora LM, Zamorano P, Venturini MC, Campero CM (2013) Immune response and protection provided by live tachyzoites and native antigens from the NC-6 Argentina strain of Neospora caninum in pregnant heifers. Vet Parasitol 197:436–446.  https://doi.org/10.1016/j.vetpar.2013.07.027 CrossRefPubMedGoogle Scholar
  19. 19.
    Hecker YP, Mogaburu Masson F, Armendano JI, Cora J, Flores Olivares C, Gual I, Pardini L, Moore DP, Moré G, Cantón GC (2018) Evaluation of frequency of antibodies against Toxoplasma gondii, Neospora caninum and Sarcocystis spp. and transmission routes in sheep from Humid Pampa, Argentina. Acta Parasitol 63(2):416–421.  https://doi.org/10.1515/ap-2018-0048 CrossRefPubMedGoogle Scholar
  20. 20.
    Howe L, West DM, Collett MG, Tattersfield G, Pattison RS, Pomroy WE, Kenyon PR, Morris ST, Williamson NB (2008) The role of Neospora caninum in three cases of unexplained ewe abortions in the southern North Island of New Zealand. Small Rumin Res 75:115–122.  https://doi.org/10.1016/j.smallrumres.2007.08.001 CrossRefGoogle Scholar
  21. 21.
    Howe L, Collett MG, Pattison RS, Marshall J, West DM, Pomroy WE (2012) Potential involvement of Neospora caninum in naturally occurring ovine abortions in New Zealand. Vet Parasitol 185:64–71.  https://doi.org/10.1016/j.vetpar.2011.10.033 CrossRefPubMedGoogle Scholar
  22. 22.
    Kobayashi Y, Yamada M, Omata Y, Koyama T, Saito A, Matsuda T, Okuyama K, Fujimoto S, Furuoka H, Matsui T (2001) Naturally-occurring Neospora caninum infection in an adult sheep and her twin fetuses. J Parasitol 87(2):434–436.  https://doi.org/10.1645/0022-3395(2001)087%5b0434:NONCII%5d2.0.CO;2 CrossRefPubMedGoogle Scholar
  23. 23.
    Moré G, Pardini L, Basso W, Machuca M, Bacigalupe D, Villanueva MC, Schares G, Venturini MC, Venturini L (2010) Toxoplasmosis and genotyping of Toxoplasma gondii in Macropus rufus and Macropus giganteus in Argentina. Vet Parasitol 169:57–61.  https://doi.org/10.1016/j.vetpar.2009.12.004 CrossRefPubMedGoogle Scholar
  24. 24.
    Moreno B, Collantes-Fernández E, Villa A, Navarro A, Regidor-Cerrillo J, Ortega-Mora LM (2012) Occurrence of Neospora caninum and Toxoplasma gondii infections in ovine and caprine abortions. Vet Parasitol 187:312–318.  https://doi.org/10.1016/j.vetpar.2011.12.034 CrossRefPubMedGoogle Scholar
  25. 25.
    Paolicchi FA, Nuñez M, Fiorentino MA, Malena RC, Trangoni M, Cravero S, Estein SM (2013) Immune response and reproductive consequences in experimentally infected ewes with Brucella ovis during late pregnancy. Rev Argent Microbiol 45(1):13–20PubMedGoogle Scholar
  26. 26.
    Sachse K (2004) Specificity and performance of PCR detection assays for microbial pathogens. Mol Biotechnol 26(1):61–80.  https://doi.org/10.1385/MB:26:1:61 CrossRefPubMedGoogle Scholar
  27. 27.
    SENASA (2017) Estratificación de establecimientos con existencias ovinas según tamaño de la majada-Marzo 2017. Data base: SIGSA, Dirección de Control de Gestión y Programas Especiales, Dirección Nacional de Sanidad Animal. http://www.senasa.gov.ar/cadena-animal/ovinos/informacion/informes-y-estadisticas
  28. 28.
    Soares HS, Ahid SMM, Bezerra ACDS, Pena HFJ, Días RA, Gennari SM (2009) Prevalence of anti-Toxoplasma gondii and anti-Neospora caninum antibodies in sheep from Mossoró, Rio Grande do Norte, Brazil. Vet Parasitol 160:211–214.  https://doi.org/10.1016/j.vetpar.2008.10.102 CrossRefPubMedGoogle Scholar
  29. 29.
    West DM, Pomroy WE, Collett MG, Hill FI, Ridler AL, Kenyon PR, Morris ST, Pattison RS (2006) A possible role for Neospora caninum in ovine abortion in New Zealand. Small Rumin Res 62:135–138.  https://doi.org/10.1016/j.smallrumres.2005.07.041 CrossRefGoogle Scholar
  30. 30.
    Weston JF, Howe L, Collett MG, Pattison RS, Williamson NB, West DM, Pomroy WE, Syed-Hussain SS, Morris ST, Kenyon PR (2009) Dose-titration challenge of young pregnant sheep with Neospora caninum tachyzoites. Vet Parasitol 164:183–191.  https://doi.org/10.1016/j.vetpar.2009.05.013 CrossRefPubMedGoogle Scholar

Copyright information

© Witold Stefański Institute of Parasitology, Polish Academy of Sciences 2019

Authors and Affiliations

  • Yanina P. Hecker
    • 1
    • 2
    Email author
  • Eleonora L. Morrell
    • 2
  • María A. Fiorentino
    • 2
  • Ignacio Gual
    • 2
    • 3
  • Emilia Rivera
    • 2
  • Franco Fiorani
    • 1
    • 3
  • Matías A. Dorsch
    • 2
    • 3
  • María L. Gos
    • 1
    • 4
  • Lais L. Pardini
    • 1
    • 4
  • María V. Scioli
    • 2
  • Sergio Magariños
    • 5
  • Fernando A. Paolicchi
    • 2
    • 3
  • Germán J. Cantón
    • 2
  • Dadín P. Moore
    • 1
    • 2
    • 3
  1. 1.National Research Council (CONICET)Buenos AiresArgentina
  2. 2.Animal Health GroupNational Institute of Agricultural Technology (INTA)BalcarceArgentina
  3. 3.Faculty of Agricultural SciencesNational University of Mar del PlataBalcarceArgentina
  4. 4.Immunoparasitology Laboratory, Faculty of Veterinary MedicineNational University of La PlataLa PlataArgentina
  5. 5.Private PractitionerRanchosArgentina

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