Abstract
The aims of the present study were to determine the Neospora caninum and Toxoplasma gondii seropositivity rates in farmed red deer hinds from Argentina and their relationship with reproductive losses. Over a 2-year period, 449 hinds from 4 commercial farms were serologically tested at late gestation for N. caninum and T. gondii by IFAT. During the first year, a sequential serological analysis was carried out at 3 different time points to analyze antibody dynamics from mating until the end of the gestation period. Fetal and postnatal mortality rates were estimated by 3 successive ultrasound scannings (us) annually and a breeding control carried out after the calving period. Ultrasound fetal measurements were used to estimate conception date and gestational age of abortions. The seropositivity rate for N. caninum was 25.5% (37/145) for the yearlings and 34.2% (104/304) for the adults, while for T. gondii was 64.3% (93/145) and 78.3% (238/304), respectively. Abortions detected at us1 and us2 were 13/21 (61.9%) with a range of gestational age of 30–87 days, while abortions detected at us3 were 8/21 (38.1%) with a range of gestational age of 49–209 days. The fetal mortality rate was 4% and 5.8%, while the postnatal mortality rate was 18.8% and 4.1% of 101 yearlings and 294 adult pregnant hinds, respectively. Most seropositive hinds to both protozoans showed a stable antibody titer pattern from mating to the end of gestation, and a lower proportion developed an increase in titers suggesting infection recrudescence. Seroconversion during the gestational period was demonstrated in 6 and 50 hinds for N. caninum and T. gondii, respectively. Hinds with fetal mortality were more likely to be seropositive to N. caninum (OR = 3.1) or have N. caninum titers ≥400 (OR = 27.4) than hinds that weaned a fawn. No statistical associations were detected for T. gondii seropositivity and reproductive losses. The pregnancy rate was not affected by N. caninum or T. gondii infection, while the serological evidence of N. caninum causing postnatal mortality was marginal. Based on serological evidence, N. caninum would be a potential abortigenic agent in red deer hinds.
Similar content being viewed by others
References
Almeria S, Vidal D, Ferrer D, Pabon M, Fernandez-de-Mera MI, Ruiz-Fons F, Alzaga V, Marco I, Calvete C, Lavin S, Gortazar C, Lopez-Gatius F, Dubey JP (2007) Seroprevalence of Neospora caninum in non-carnivorous wildlife from Spain. Vet Parasitol 143(1):21–28. https://doi.org/10.1016/j.vetpar.2006.07.027
Audigé LM, Wilson PR, Morris RS (1999) Reproductive performance of farmed red deer (Cervus elpahus) in New Zealand I. Descriptive data. Anim Reprod Sci 55:127–141
Audigé LM, Wilson PR, Morris RS (2000) Reproductive performance of farmed red deer (Cervus elaphus) in New Zealand: V Mob and individual hind risk factors associated with calf rearing to weaning. Prevent Vet Med 44:189–204
Bartova E, Sedlak K, Pavlik I, Literak I (2007) Prevalence of Neospora caninum and Toxoplasma gondii antibodies in wild ruminants from the countryside or captivity in the Czech Republic. J Parasitol 93(5):1216–1218. https://doi.org/10.1645/GE-1126R.1
Basso W, More G, Quiroga MA, Balducchi D, Schares G, Venturini MC (2014) Neospora caninum is a cause of perinatal mortality in axis deer (Axis axis). Vet Parasitol 199(3-4):255–258. https://doi.org/10.1016/j.vetpar.2013.10.020
Buxton D (1998) Protozoan infections (Toxoplasma gondii, Neospora caninum and Sarcocystis spp.) in sheep and goats: recent advances. Vet Res 29(3-4):289–310
De Craeye S, Speybroeck N, Ajzenberg D, Darde ML, Collinet F, Tavernier P, Van Gucht S, Dorny P, Dierick K (2011) Toxoplasma gondii and Neospora caninum in wildlife: common parasites in Belgian foxes and Cervidae? Vet Parasitol 178(1-2):64–69. https://doi.org/10.1016/j.vetpar.2010.12.016
Deer Industry Manual (2000) Deer Master Project, South Canterbury and North Otago Branch NZDFA
Dubey JP (2010) Toxoplasmosis of animals and humans, vol, 2nd edn. CRC Press, Boca raton
Dubey JP, Schares G (2006) Diagnosis of bovine neosporosis. Vet Parasitol 140(1-2):1–34. https://doi.org/10.1016/j.vetpar.2006.03.035
Dubey JP, Rigoulet J, Lagourette P, George C, Longeart L, LeNet JL (1996) Fatal transplacental neosporosis in a deer (Cervus eldi siamensis). J Parasitol 82(2):338–339
Dubey JP, Jenkins MC, Kwok OC, Ferreira LR, Choudhary S, Verma SK, Villena I, Butler E, Carstensen M (2013) Congenital transmission of Neospora caninum in whitetailed deer (Odocoileus virginianus). Vet Parasitol 196(519-22):519–522
Dubey JP, Dennis PM, Verma SK, Choudhary S, Ferreira LR, Oliveira S, Kwok OC, Butler E, Carstensen M, Su C (2014) Epidemiology of toxoplasmosis in white tailed deer (Odocoileus virginianus): occurrence, congenital transmission, correlates of infection, isolation, and genetic characterization of Toxoplasma gondii. Vet Parasitol 202(3-4):270–275. https://doi.org/10.1016/j.vetpar.2014.01.006
Dubey JP, Hemphill A, Calero-Bernal R, Schares G (2017) Neosporosis in animals. CRC Press, Boca Raton
Gozdzik K, Jakubek EB, Bjorkman C, Bien J, Moskwa B, Cabaj W (2010) Seroprevalence of Neospora caninum in free living and farmed red deer (Cervus elaphus) in Poland. Pol J Vet Sci 13(1):117–120
Guy CS, Williams DJL, Kelly DF, McGarry JW, Guy F, Bjorkman C, Smith RF, Trees AJ (2001) Neospora caninum in persistently infected, pregnant cows: spontaneous transplacental infection is associated with an acute increase in maternal antibody. Vet Rec 149(15):443–449. https://doi.org/10.1136/vr.149.15.443
Halová D, Mulcahy G, Rafter P, Turčeková L, Grant T, de Waal T (2013) Toxoplasma gondii in Ireland: seroprevalence and novel molecular detection method in sheep, pigs, deer and chickens. Zoonoses Public Health 60:168–173
Innes EA, Andrianarivo AG, Bjorkman C, Williams DJ, Conrad PA (2002) Immune responses to Neospora caninum and prospects for vaccination. Trends Parasitol 18(11):497–504. https://doi.org/10.1016/s1471-4922(02)02372-3
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
Martinez MM, Merás A, Di Micco S, Ratti MC, Cerruti MM (2008) Development of a panel for use in red deer maternity assessment. International Society of Animal Genetics Congress, Amsterdam. (2024)
More G, Bacigalupe D, Basso W, Rambeaud M, Beltrame F, Ramirez B, Venturini MC, Venturini L (2009) Frequency of horizontal and vertical transmission for Sarcocystis cruzi and Neospora caninum in dairy cattle. Vet Parasitol 160(1-2):51–54. https://doi.org/10.1016/j.vetpar.2008.10.081
Patel KK, Burrows E, Heuer C, Asher GW, Wilson PR, Howe L (2019) Investigation of Toxoplasma gondii and association with early pregnancy and abortion rates in New Zealand farmed red deer (Cervus elaphus). Parasitol Res 118(7):2065–2077. https://doi.org/10.1007/s00436-019-06355-1
Revol B, Wilson P (1990) Rectal ultrasonographic pregnancy. Diagnosis and foetal ageing of red deer.
Rocchigiani G, Nardoni S, D’Ascenzi C, Nicoloso S, Picciolli F, Papini R, Mancianti F (2016) Seroprevalence of Toxoplasma gondii and Neospora caninum in red deer from Central Italy. Annals Agric Environ Med 23(4):699–701
Rodriguez AM, Maresca S, Cano DB, Armendano JI, Combessies G, Lopez-Valiente S, Odriozola ER, Spath EJ, Odeon AC, Campero CM, Moore DP (2016) Frequency of Neospora caninum infections in beef cow-calf operations under extensive management. Vet Parasitol 219:40–43. https://doi.org/10.1016/j.vetpar.2016.02.002
Soldati S, Kiupel M, Wise A, Maes R, Botteron C, Robert N (2004) Meningoencephalomyelitis caused by Neospora caninum in a juvenile fallow deer (Dama dama). J Vet Med 51:280–283
Wilson PR, Patel KK, Asher GW, Howe L, Heuer C (2012) Sinclair G (2012) Clinical investigations of foetal loss in farmed red deer. Proc Deer Branch NZVA:107–110
Acknowledgments
We would like to thank Isidoro Ercoli for his excellent technical assistance and Dr. Yanina P. Hecker for her kind suggestions about this manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
All the authors declare no conflicts of interest.
Additional information
Section Editor: Berit Bangoura
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
Soler, J.P., Dellarupe, A. & Moré, G. Neospora caninum and Toxoplasma gondii infections and their relationship with reproductive losses in farmed red deer (Cervus elaphus). Parasitol Res 120, 1851–1860 (2021). https://doi.org/10.1007/s00436-021-07104-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-021-07104-z