Abstract
Neosporosis in cattle is a globally important disease, causing abortions and significant economic losses if epidemic abortions occur. In Serbia, however, studies of Neospora caninum infection in cattle are few and are based on limited samples and/or from limited areas. We thus performed a nationwide study to examine the seroprevalence of N. caninum infection in a sample of cows randomly selected from dairy farms in 12 epidemiological units from throughout Serbia, as well as the possible transmission risk factors. Sera from a total of 1496 cattle were tested by competitive ELISA, and N. caninum–specific antibodies were shown in 7.2% animals (95% confidence interval CI, 6.6–7.9%), ranging from 2.2 to 12% across the epidemiological units. At least one seropositive animal was detected on 10.7% (95% CI, 9.7–11.8%) of farms, with a range of 5.9–25.9%. Logistic regression analysis showed that the single risk factor for infection in individual animals was keeping cows in loose-stalls (OR = 3.31, 95% CI = 1.95–5.60, P < 0.001). Risk factors for the presence of infection on farms also included housing in loose-stalls (OR = 18.49, 95% CI = 5.40–63.36, P < 0.001), and herd size > 100 animals (OR = 24.08, 95% CI = 3.85–150.50, P = 0.001). In view of the relatively low prevalence of infection showed at both the individual and farm level, this is the perfect time to undertake appropriate preventive measures to improve animal health and reduce economic losses.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Almería S, López-Gatius F, García-Ispierto I, Nogareda C, Bech-Sàbat G, Serrano B, Santolaria P, Yániz JL (2009) Effects of crossbreed pregnancies on the abortion risk of Neospora caninum-infected dairy cows. Vet Parasitol 163:323–329. https://doi.org/10.1016/j.vetpar.2009.04.026
Álvarez-García G, García-Culebras A, Gutiérrez-Expósito D, Navarro-Lozano V, Pastor-Fernández I, Ortega-Mora LM (2013) Serological diagnosis of bovine neosporosis: a comparative study of commercially available ELISA tests. Vet Parasitol 198:85–95. https://doi.org/10.1016/j.vetpar.2013.07.033
Anderson ML, Blanchard PC, Barr BC, Dubey JP, Hoffman RL, Conrad PA (1991) Neospora-like protozoan infection as a major cause of abortion in California dairy cattle. J Am Vet Med Assoc 198:241–244
Anderson ML, Andrianarivo AG, Conrad PA (2000) Neosporosis in cattle. Anim Reprod Sci 60-61:417–431. https://doi.org/10.1016/S0378-4320(00)00117-2
Anon (2008) Statistical Yearbook оf the Republic of Serbia, XLI ed. Statistical Office of the Republic of Serbia, Belgrade, p 219
Anon (2009) Statistical Yearbook оf the Republic of Serbia, XLII ed. Statistical Office of the Republic of Serbia, Belgrade, p 215
Anon (2010) Statistical Yearbook оf the Republic of Serbia, XLIII ed. Statistical Office of the Republic of Serbia, Belgrade, p 212
Anon (2011) Statistical Yearbook оf the Republic of Serbia, XLIV ed. Statistical Office of the Republic of Serbia, Belgrade, p 211
Bañales P, Fernandez L, Repiso MV, Gil A, Dargatz DA, Osawa T (2006) A nationwide survey on seroprevalence of Neospora caninum infection in beef cattle in Uruguay. Vet Parasitol 139:15–20. https://doi.org/10.1016/j.vetpar.2006.03.004
Bartels CJ, Arnaiz-Seco JI, Ruiz-Santa-Quitera A, Björkman C, Frössling J, von Blumröder D, Conraths FJ, Schares G, van Maanen C, Wouda W, Ortega-Mora LM (2006) Supranational comparison of Neospora caninum seroprevalences in cattle in Germany, the Netherlands, Spain and Sweden. Vet Parasitol 137:17–27. https://doi.org/10.1016/j.vetpar.2005.12.016
Bártová E, Sedlak K, Budíková M (2015) A study of Neospora caninum and Toxoplasma gondii antibody seroprevalence in healthy cattle in the Czech Republic. Ann Agric Environ Med 22:32–34. https://doi.org/10.5604/12321966.1141365
Baszler TV, Adams S, Vander-Schalie J, Mathison BA, Kostovic M (2001) Validation of a commercially available monoclonal antibody-based competitive-inhibition enzyme-linked immunosorbent assay for detection of serum antibodies to Neospora caninum in cattle. J Clin Microbiol 39:3851–3857. https://doi.org/10.1128/JCM.39.11.3851-3857.2001
Beck R, Marinculić A, Mihaljević Ž, Benić M, Martinković F (2010) Seroprevalence and potential risk factors of Neospora caninum infection in dairy cattle in Croatia. Vet Arhiv 80:163–171
Bjerkås I, Mohn SF, Presthus J (1984) Unidentified cyst-forming sporozoon causing encephalomyelitis and myositis in dogs. Z Parasitenkd 70:271–274
Björkman C, Sager H, Schares G (2007) Diagnostic techniques – serology. In: Ortega-Mora L, Gottstein B, Conraths F, Buxton D (eds) Protozoal abortion in farm ruminants: guidelines for diagnosis and control. CAB International, Wallingford, pp 63–74
Cvetojević Đ, Milićević V, Kureljušić B, Savić B (2018) Seroprevalence of Neospora caninum in dairy cows in Belgrade City area, Serbia. J Hellenic Vet Med Soc 69:979–983. https://doi.org/10.12681/jhvms.18026
Dubey JP (2003) Review of Neospora caninum and neosporosis in animals. Korean J Parasitol 41:1–16. https://doi.org/10.3347/kjp.2003.41.1.1
Dubey JP, Schares G (2011) Neosporosis in animals – the last five years. Vet Parasitol 180:90–108. https://doi.org/10.1016/j.vetpar.2011.05.031
Dubey JP, Carpenter JL, Speer CA, Topper MJ, Uggla A (1988) Newly recognized fatal protozoan disease of dogs. J Am Vet Med Assoc 192:1269–1285
Dubey JP, Schares G, Ortega-Mora LM (2007) Epidemiology and control of neosporosis and Neospora caninum. Clin Microbiol Rev 20:323–367. https://doi.org/10.1128/CMR.00031-06
Dubey JP, Jenkins MC, Rajendran C, Miska K, Ferreira LR, Martins J, Kwok OCH, Choudhary S (2011) Gray wolf (Canis lupus) is a natural definitive host for Neospora caninum. Vet Parasitol 181:382–387. https://doi.org/10.1016/j.vetpar.2011.05.018
Eiras C, Arnaiz I, Álvarez-García G, Ortega-Mora LM, Sanjuánl ML, Yus E, Diéguez FJ (2011) Neospora caninum seroprevalence in dairy and beef cattle from the northwest region of Spain, Galicia. Prev Vet Med 98:128–132. https://doi.org/10.1016/j.prevetmed.2010.10.014
Frössling J, Uggla A, Björkman C (2005) Prevalence and transmission of Neospora caninum within infected Swedish dairy herds. Vet Parasitol 128:209–218. https://doi.org/10.1016/j.vetpar.2004.12.006
Gavrea RR, Iovu A, Losson B, Cozma V (2011) Seroprevalence of Neospora caninum in dairy cattle from north-west and centre of Romania. Parasite 18:349–351. https://doi.org/10.1051/parasite/2011184349
Gavrilović P, Živulj A, Todorović I, Jovanović M, Parunović J (2013) Investigation of importance of Neospora caninum in aetiology of abortion in dairy cows in Serbia. Rev Med Vet (Toulouse) 164:100–104
Gondim LFP, McAllister MM, Pitt WC, Zemlicka DE (2004) Coyotes (Canis latrans) are definitive hosts of Neospora caninum. Int J Parasitol 34:159–161. https://doi.org/10.1016/j.ijpara.2004.01.001
Greiner M, Franke CR, Böhning D, Schlattmann P (1994) Construction of an intrinsic cut-off value for the sero-epidemiological study of Trypanosoma evansi infections in a canine population in Brazil: a new approach towards an unbiased estimation of prevalence. Acta Trop 56:97–109. https://doi.org/10.1016/0001-706X(94)90044-2
Hässig M, Gottstein B (2002) Epidemiological investigations of abortions due to Neospora caninum on Swiss dairy farms. Vet Rec 150:538–542
Hobson JC, Duffield TF, Kelton D, Lissemore K, Hietala SK, Leslie KE, McEwen B, Peregrine AS (2005) Risk factors associated with Neospora caninum abortion in Ontario Holstein dairy herds. Vet Parasitol 127:177–188. https://doi.org/10.1016/j.vetpar.2004.09.025
Hornok S, Edelhofer R, Hajtós I (2006) Seroprevalence of neosporosis in beef and dairy cattle breeds in Northeast Hungary. Acta Vet Hung 54:485–491. https://doi.org/10.1556/AVet.54.2006.4.6
Hůrková L, Halova D, Modrý D (2005) The prevalence of Neospora caninum antibodies in bulk milk of dairy herds in the Czech Republic: a case report. Vet Med (Praha) 50:549–552
Imre K, Morariu S, Ilie MS, Imre M, Ferrari N, Genchi C, Dărăbuş G (2012) Serological survey of Neospora caninum infection in cattle herds from western Romania. J Parasitol 98:683–685. https://doi.org/10.1645/GE-3023.1
Jacobson RH (1998) Validation of serological assays for diagnosis of infectious diseases. Rev Sci Tech 17:469–526
King JS, Slapeta J, Jenkins DJ, Al-Qassab SE, Ellis JT, Windsor PA (2010) Australian dingoes are definitive hosts of Neospora caninum. Int J Parasitol 40:945–950. https://doi.org/10.1016/j.ijpara.2010.01.008
Klevar S, Norström M, Tharaldsen J, Clausen T, Björkman C (2010) The prevalence and spatial clustering of Neospora caninum in dairy herds in Norway. Vet Parasitol 170:153–157. https://doi.org/10.1016/j.vetpar.2010.02.005
Klun I (2014) Seroepizootiology and molecular diagnosis of Neospora caninum infection in cattle in Serbia. Dissertation, University of Belgrade Faculty of Veterinary Medicine
Klun I, Nikolić A, Vujanić M, Ivović V, Bobić B, Djurković-Djaković O (2008) Pilot study of Neospora caninum seroprevalence in cattle in Serbia. 10th European Multicolloquium of Parasitology, Paris, France, 24–28.08. Program & Abstract Book, p 192
Kowalczyk SJ, Czopowicz M, Weber CN, Müller E, Witkowski L, Kaba J (2016) Herd-level seroprevalence of Neospora caninum infection in dairy cattle in central and northeastern Poland. Acta Parasitol 61:63–65. https://doi.org/10.1515/ap-2016-0006
Kuruca LJ, Spasojević-Kosić LJ, Simin S, Savović M, Lauš S, Lalošević V (2013) Neospora caninum antibodies in dairy cows and domestic dogs from Vojvodina, Serbia. Parasite 20:40. https://doi.org/10.1051/parasite/2013036
Kyaw T, Virakul P, Muangyai M, Suwimonteerabutr J (2004) Neospora caninum seroprevalence in dairy cattle in central Thailand. Vet Parasitol 121:255–263. https://doi.org/10.1016/j.vetpar.2004.01.014
Lassen B, Orro T, Aleksejev A, Raaperi K, Järvis T, Viltrop A (2012) Neospora caninum in Estonian dairy herds in relation to herd size, reproduction parameters, bovine virus diarrhoea virus, and bovine herpes virus 1. Vet Parasitol 190:43–50. https://doi.org/10.1016/j.vetpar.2012.05.021
López-Gatius F, Santolaria P, Yániz JL, Garbayo JM, Almería S (2005) The use of beef bull semen reduced the risk of abortion in Neospora-seropositive dairy cows. J Vet Med B Infect Dis Vet Public Health 52:88–92. https://doi.org/10.1111/j.1439-0450.2004.00818.x
McAllister MM, Dubey JP, Lindsay DS, Jolley WR, Wills RA, McGuire AM (1998) Dogs are definitive hosts of Neospora caninum. Int J Parasitol 28:1473–1478. https://doi.org/10.1016/S0020-7519(98)00138-6
Mickey RM, Greenland S (1989) The impact of confounder selection criteria on effect estimation. Am J Epidemiol 129:125–137. https://doi.org/10.1093/oxfordjournals.aje.a115101
Mitrea IL, Enachescu V, Radulescu R, Ionita M (2012) Seroprevalence of Neospora caninum infection on dairy cattle in farms from southern Romania. J Parasitol 98:69–72. https://doi.org/10.1645/GE-2972.1
Otranto D, Llazari A, Testini G, Traversa D, Frangipane di Regalbono A, Badan M, Capelli G (2003) Seroprevalence and associated risk factors of neosporosis in beef and dairy cattle in Italy. Vet Parasitol 118:7–18. https://doi.org/10.1016/j.vetpar.2003.10.008
Pabón M, López-Gatius F, García-Ispierto I, Bech-Sàbat G, Nogareda C, Almería S (2007) Chronic Neospora caninum infection and repeat abortion in dairy cows: a 3-year study. Vet Parasitol 147:40–46. https://doi.org/10.1016/j.vetpar.2007.03.017
Pavičić LJ, Lalošević V, Spasojević-Kosić LJ, Lauš S, Simin S (2011) Seroprevalence of Neospora caninum in dogs. Contemp Agric 60:453–457
Rodriguez I, Choromanski L, Rodgers SJ, Weinstock D (2002) Survey of Neospora caninum antibodies in dairy and beef cattle from five regions of the United States. Vet Ther 3:396–401
Schares G, Bärwald A, Staubach C, Ziller M, Klöss D, Wurm R, Rauser M, Labohm R, Dräger K, Fasen W, Hess RG, Conraths FJ (2003) Regional distribution of bovine Neospora caninum infection in the German state of Rhineland-Palatinate modelled by logistic regression. Int J Parasitol 33:1631–1640. https://doi.org/10.1016/S0020-7519(03)00266-2
Schares G, Bärwald A, Staubach C, Ziller M, Klöss D, Schröder R, Labohm R, Dräger K, Fasen W, Hess RG, Conraths FJ (2004) Potential risk factors for bovine Neospora caninum infection in Germany are not under the control of the farmers. Parasitology 129:301–309. https://doi.org/10.1017/S0031182004005700
Schares G, Wilking H, Bolln M, Conraths FJ, Bauer C (2009) Neospora caninum in dairy herds in Schleswig-Holstein, Germany. Berl Munch Tierarztl Wochenschr 122:47–50
Softic A, Asmare K, Granquist EG, Godfroid J, Fejzic N, Skjerve E (2018) The serostatus of Brucella spp., Chlamydia abortus, Coxiella burnetii and Neospora caninum in cattle in three cantons in Bosnia and Herzegovina. BMC Vet Res 14(40). https://doi.org/10.1186/s12917-018-1361-z
Thilsted JP, Dubey JP (1989) Neosporosis-like abortions in a herd of dairy cattle. J Vet Diagn Investig 1:205–209. https://doi.org/10.1177/104063878900100301
Thrusfield M (2005) Surveys. In: Veterinary Epidemiology, 3rd edn. Blackwell Science, Oxford, 228–246
Vidić B, Grgić Ž, Savić S, Bugarski D (2011) Neospora caninum causes abortions in cows. Scientific Symposium Reproduction of Domestic Animals, Divčibare, Serbia, 13–16.10. Proceedings, pp 133–134
Yániz JL, López-Gatius F, García-Ispierto I, Bech-Sàbat G, Serrano B, Nogareda C, Sanchez-Nadal JA, Almeria S, Santolaria P (2010) Some factors affecting the abortion rate in dairy herds with high incidence of Neospora-associated abortions are different in cows and heifers. Reprod Domest Anim 45:699–705. https://doi.org/10.1111/j.1439-0531.2008.01337.x
Funding
This study was supported by a grant (III 41019) from the Ministry of Education, Science and Technological Development of the Republic of Serbia.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
As sampling was part of routine diagnostic procedures, no ethical permission was necessary under Serbian legislation (Animal Welfare Act, Official Gazette RS 41/2009).
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Section Editor: Daniel K. Howe
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Klun, I., Ćirković, V., Maletić, M. et al. Seroprevalence of Neospora caninum infection and associated risk factors in dairy cattle in Serbia. Parasitol Res 118, 1875–1883 (2019). https://doi.org/10.1007/s00436-019-06307-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-019-06307-9