Abstract
Neospora caninum has been implicated as a sporadic cause of abortion and perinatal deaths in sheep flocks globally. However, its significance as a reproductive pathogen for sheep in Australia remains unknown. The aims of this study were to (i) determine the seroprevalence of N. caninum in Australian breeding ewes and (ii) examine if natural exposure to N. caninum is associated with poor reproductive performance of primiparous ewes in southern Australia. Thirty flocks of primiparous ewes (aged 1–2 years old at lambing) from 28 farms in three states (Western Australia, South Australia and Victoria) were monitored between mating and lamb marking. Blood samples were also collected from multiparous mature ewes (aged 3 years or older) at each farm. Seroprevalence for anti-N. caninum IgG using indirect ELISA was determined for a subset of primiparous ewes that were predominantly determined to be pregnant and subsequently failed to rear a lamb (n = 1279) and randomly selected mature multiparous ewes with unknown reproductive status (n = 558). Neopsora caninum apparent seroprevalence was 0.16% (95% confidence interval 0.03%, 0.5%) in primiparous ewes, with seropositivity identified in two ewes from farms located in South Australia and Victoria. There was no evidence of seropositivity in mature ewes with apparent seroprevalence 0% (0%, 0.45%). These findings suggest that N. caninum infection was not widespread in primiparous ewes or mature multiparous ewes on these farms, and exposure to N. caninum infection was unlikely to explain abortion and perinatal mortalities observed for primiparous ewes.
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References
Abo-Shehada MN, Abu-Halaweh MM (2010) Flock-level seroprevalence of, and risk factors for Neospora caninum among sheep and goats in northern Jordan. Prev Vet Med 93(1):25–32. https://doi.org/10.1016/j.prevetmed.2009.08.004
Allworth MB, Wrigley HA, Cowling A (2017) Fetal and lamb losses from pregnancy scanning to lamb marking in commercial sheep flocks in southern New South Wales. Anim Prod Sci 57(10):2060–2065. https://doi.org/10.1071/AN16166
Australian Government Bureau of Meteorology (2021) Australian climate averages—rainfall. http://www.bom.gov.au/jsp/ncc/climate_averages/rainfall/index.jsp. Accessed June 2021 2021
Bishop S, King J, Windsor P, Reichel MP, Ellis J, Šlapeta J (2010) The first report of ovine cerebral neosporosis and evaluation of Neospora caninum prevalence in sheep in New South Wales. Vet Parasitol 170(1):137–142. https://doi.org/10.1016/j.vetpar.2010.01.030
Brown LD, Cai TT, DasGupta A (2001) Interval estimation for a binomial proportion. Statist Sci 16(2):101–133. https://doi.org/10.1214/ss/1009213286
Buxton D, Wright S, Maley SW, Rae AG, Lundén A, Innes EA (2001) Immunity to experimental neosporosis in pregnant sheep. Parasite Immunol 23(2):85–91. https://doi.org/10.1046/j.1365-3024.2001.00362.x
Clune T et al (2021a) Ovine abortion and stillbirth investigations in Australia. Aust Vet J 99(3):72–78. https://doi.org/10.1111/avj.13040
Clune T et al (2021b) Chlamydia pecorum detection in aborted and stillborn lambs from Western Australia. Vet Res 52(1):84. https://doi.org/10.1186/s13567-021-00950-w
Cosendey RIJ et al (2018) Seroprevalence of anti-Neospora caninum antibodies in sheep from the rapidly expanding flock of Rio de Janeiro, Brazil. Vet Parasitol Reg Stud Reports 14:59–62. https://doi.org/10.1016/j.vprsr.2018.09.001
Devleesschauwer B, Torgerson P, Charlier J (2015) Prevalence: tools for prevalence assessment studies. R package version 0.4.0. http://cran.r-project.org/package=prevalence. Accessed 1 Jul 2021
Dubey JP, Schares G (2011) Neosporosis in animals—the last five years. Vet Parasitol 180(1–2):90–108. https://doi.org/10.1016/j.vetpar.2011.05.031
Fordyce G, Holroyd RG, Taylor J, Kirkland PD (2013) Neospora caninum and reproductive wastage in extensively managed Queensland beef herds. Aust Vet J 91(9):385–390. https://doi.org/10.1111/avj.12097
Frössling J, Nødtvedt A, Lindberg A, Björkman C (2008) Spatial analysis of Neospora caninum distribution in dairy cattle from Sweden. Geospat Health 3(1):39–45. https://doi.org/10.4081/gh.2008.230
González-Warleta M et al (2018) Endogenous transplacental transmission of Neospora caninum during successive pregnancies across three generations of naturally infected sheep. Vet Res 49(1):106. https://doi.org/10.1186/s13567-018-0601-3
González-Warleta M et al (2014) Neospora caninum infection as a cause of reproductive failure in a sheep flock. Vet Res 45(1):88–88. https://doi.org/10.1186/s13567-014-0088-5
Hässig M, Sager H, Reitt K, Ziegler D, Strabel D, Gottstein B (2003) Neospora caninum in sheep: a herd case report. Vet Parasitol 117(3):213–220. https://doi.org/10.1016/j.vetpar.2003.07.029
Helmick B, Otter A, McGarry J, Buxton D (2002) Serological investigation of aborted sheep and pigs for infection by Neospora caninum. Res Vet Sci 73(2):187–189. https://doi.org/10.1016/S0034-5288(02)00093-0
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(2–4):64–71. https://doi.org/10.1016/j.vetpar.2011.10.033
Howe L et al (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(2):115–122. https://doi.org/10.1016/j.smallrumres.2007.08.001
Kilgour R (1992) Lambing potential and mortality in Merino sheep as ascertained by ultrasonography. Aust J Exp Agric 32(3):311–313. https://doi.org/10.1071/EA9920311
King JS, Šlapeta J, Jenkins DJ, Al-Qassab SE, Ellis JT, Windsor PA (2010) Australian dingoes are definitive hosts of Neospora caninum. Int J Parasitol 40(8):945–950. https://doi.org/10.1016/j.ijpara.2010.01.008
Kleemann DO, Walker SK (2005) Fertility in South Australian commercial Merino flocks: sources of reproductive wastage. Theriogenology 63(8):2075–2088. https://doi.org/10.1016/j.theriogenology.2004.06.017
Lindsay DS, Dubey JP (2020) Neosporosis, toxoplasmosis, and sarcocystosis in ruminants: an update. Vet Clin North Am Food Anim Pract 36(1):205–222. https://doi.org/10.1016/j.cvfa.2019.11.004
Liu Z-K, Li J-Y, Pan H (2015) Seroprevalence and risk factors of Toxoplasma gondii and Neospora caninum infections in small ruminants in China. Prev Vet Med 118(4):488–492. https://doi.org/10.1016/j.prevetmed.2014.12.017
McInnes LM, Ryan UM, O’Handley R, Sager H, Forshaw D, Palmer DG (2006) Diagnostic significance of Neospora caninum DNA detected by PCR in cattle serum. Vet Parasitol 142(3):207–213. https://doi.org/10.1016/j.vetpar.2006.07.013
Moloney BJ, Kirkland PD, Heuer C (2017) Neospora caninum in beef herds in New South Wales, Australia. 1: seroprevalence study. Aust Vet J 95(3):72–79. https://doi.org/10.1111/avj.12561
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(1):312–318. https://doi.org/10.1016/j.vetpar.2011.12.034
Nasir A, Lanyon SR, Schares G, Anderson ML, Reichel MP (2012) Sero-prevalence of Neospora caninum and Besnoitia besnoiti in South Australian beef and dairy cattle. Vet Parasitol 186(3–4):480–485. https://doi.org/10.1016/j.vetpar.2011.11.032
Osawa T, Wastling J, Maley S, Buxton D, Innes EA (1998) A multiple antigen ELISA to detect Neospora-specific antibodies in bovine sera, bovine foetal fluids, ovine and caprine sera. Vet Parasitol 79(1):19–34. https://doi.org/10.1016/S0304-4017(98)00156-3
Refshauge G, Atkinson T, Robertson SM, Hernandez-Jover M, Allworth B, Friend M (2020) Reducing kid loss—select and project. Phase 1 Final report. Meat and Livestock Australia, North Sydney, Australia. https://www.mla.com.au/research-and-development/reports/2020/reducing-kid-loss-select-and-protect---phase-1/. Accessed 1 Feb 2021
Reichel MP, Alejandra Ayanegui-Alcérreca M, Gondim LFP, Ellis JT (2013) What is the global economic impact of Neospora caninum in cattle—the billion dollar question. Int J Parasitol 43(2):133–142. https://doi.org/10.1016/j.ijpara.2012.10.022
Reichel MP, McAllister MM, Pomroy WE, Campero C, Ortega-Mora LM, Ellis JT (2014) Control options for Neospora caninum—is there anything new or are we going backwards? Parasitology 141(11):1455–1470. https://doi.org/10.1017/S0031182014000158
Reichel MP, Ross GP, McAllister MM (2008) Evaluation of an enzyme-linked immunosorbent assay for the serological diagnosis of Neospora caninum infection in sheep and determination of the apparent prevalence of infection in New Zealand. Vet Parasitol 151(2):323–326. https://doi.org/10.1016/j.vetpar.2007.11.002
Sergeant ESG (2021) Epitools epidemiological calculators. Ausvet Pty Ltd. http://epitools.ausvet.com.au. Accessed 20 Feb 2021 2021
Shorten PR, Edwards SJ, Juengel JL (2021) The role of reproductive loss on flock performance: a comparison of nine industry flocks. Transl Anim Sci 5(1):txab013–txab013. https://doi.org/10.1093/tas/txab013
Speybroeck N, Devleesschauwer B, Joseph L, Berkvens D (2013) Misclassification errors in prevalence estimation: Bayesian handling with care. Int J Public Health 58(5):791–795. https://doi.org/10.1007/s00038-012-0439-9
Stoessel Z, Taylor LF, McGowan MR, Coleman GT, Landmann JK (2003) Prevalence of antibodies to Neospora caninum within central Queensland beef cattle. Aust Vet J 81(3):165–166. https://doi.org/10.1111/j.1751-0813.2003.tb11081.x
Villagra-Blanco R, Barrantes-Granados O, Montero-Caballero D, Romero-Zúñiga JJ, Dolz G (2019) Seroprevalence of Toxoplasma gondii and Neospora caninum infections and associated factors in sheep from Costa Rica. Parasite Epidemiol Control 4:e00085. https://doi.org/10.1016/j.parepi.2019.e00085
West DM et al (2006) A possible role for Neospora caninum in ovine abortion in New Zealand. Small Rumin Res 62(1):135–138. https://doi.org/10.1016/j.smallrumres.2005.07.041
Westermann T et al (2021) Chlamydia pecorum associated sporadic ovine abortion. Vet Pathol 58(1):114–122. https://doi.org/10.1177/0300985820967451
Acknowledgements
We thank the participating farmers who provided access to their animals and facilities, conducted lambing rounds and collected and stored lambs for necropsy. We thank Celia Smuts, Janine Simmonds and the staff at VetPath Laboratories for their assistance with the serological testing. We thank Tom La and Nyree Philip (Murdoch University), Ryan O’Handley, Louis Lignereux and Rob Paterson (University of Adelaide), Andrew Whale, Mary McQuillan and Patrick Hannemann (Livestock Logic, Hamilton, Victoria), Sean McGrath (Millicent Veterinary Hospital), Simon Edwards and Michelle Smart (Willunga Veterinary Hospital) and Lauryn Stewart and Deb Lehmann (Kangaroo Island Veterinary Hospital) for assistance with sample collection and feedback on the study design. We thank Johann Schroder for helpful feedback on the study design and manuscript.
Funding
This study was funded by Meat and Livestock Australia (B.AHE.0318). Tom Clune received post-graduate scholarships from Meat and Livestock Australia and Sheep Industry Business Innovation (Department of Primary Industries and Regional Development, Western Australia). Equipment used for this project was funded by the Murdoch University Veterinary Trust.
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Conceptualisation: Tom Clune, Caroline Jacobson, Amy Lockwood, Serina Hancock, Andrew Thompson, Sue Beetson.
Methodology: Tom Clune, Caroline Jacobson, Sue Beetson, Ryan O’Handley.
Formal analysis and investigation: Tom Clune, Caroline Jacobson, Mieghan Bruce, Amy Lockwood, Serina Hancock, Angus Campbell, Elsa Glanville, Daniel Brooks, Colin Trengove.
Writing—original draft preparation: Tom Clune, Caroline Jacobson, Amy Lockwood.
Writing—review and editing: Tom Clune, Amy Lockwood, Serina Hancock, Andrew Thompson, Mieghan Bruce, Sue Beetson, Angus Campbell, Elsa Glanville, Daniel Brooks, Colin Trengove, Ryan O’Handley, Caroline Jacobson.
Funding acquisition: Caroline Jacobson, Serina Hancock, Andrew Thompson.
Resources: Caroline Jacobson, Serina Hancock, Andrew Thompson, Ryan O’Handley.
Supervision: Caroline Jacobson, Serina Hancock, Andrew Thompson.
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All procedures were conducted according to guidelines of the Australian Code of Practice for the Use of Animals for Scientific Purposes and were approved by the Murdoch University Animal Ethics Committee (R3004/17).
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Participating farms have consented to publication of data. The manuscript was approved for publication by the funding body (Meat and Livestock Australia).
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Clune, T., Lockwood, A., Hancock, S. et al. Neospora caninum is not an important contributor to poor reproductive performance of primiparous ewes from southern Australia: evidence from a cross-sectional study. Parasitol Res 120, 3875–3882 (2021). https://doi.org/10.1007/s00436-021-07328-z
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DOI: https://doi.org/10.1007/s00436-021-07328-z