Dynamics of Neospora caninum-Associated Abortions in a Dairy Sheep Flock and Results of a Test-and-Cull Control Programme

Abstract

Neospora caninum is an apicomplexan parasite that can cause abortions and perinatal mortality in sheep. Although ovine neosporosis has been described worldwide, there is a lack of information about the relationship between N. caninum serostatus and the reproductive performance. In this study, we described the infection dynamics in a dairy sheep flock with an abortion rate up to 25% and a N. caninum seroprevalence of 32%. Abortions were recorded in 36% and 9% of seropositive and seronegative sheep, respectively. Seropositive sheep were more likely to abort twice (OR = 4.44) or three or more times (OR = 10.13) than seronegative sheep. Endogenous transplacental transmission was the main route of transmission since 86% of seropositive sheep had seropositive offspring. Within dams that had any abortion, seropositive sheep were more likely than seronegative ones to have female descendants that aborted (OR = 8.12). The slight increase in seropositivity with the age, the low percentage of animals with postnatal seroconversion or with low avidity antibodies, and the seropositivity of one flock dog, indicated that horizontal transmission might have some relevance in this flock. A control programme based on selective culling of seropositive sheep and replacement with seronegative animals was effective in reducing the abortion rate to 7.2%.

Toxoplasma gondii and Neospora caninum infections in sheep and goats in Switzerland: Seroprevalence and occurrence in aborted foetuses

“…In addition, N. caninum DNA was detected in 2.4% (2/82; 95%CI: 0.3–8.5%) and 1.4% (1/73; 95%CI: 0.0–7.4%) of the tested sheep and goat foetuses, respectively, showing occurrence of vertical transmission of this parasite and suggesting its involvement as cause of abortion. Although the frequency of N. caninum -DNA detection in small ruminants was around ten times lower than that previously reported for Swiss cattle, in which N. caninum DNA was amplified in 29% (24/83) ( Gottstein et al, 1998 ) and 21% (50/242) ( Sager et al, 2001 ) of aborted bovine foetuses, this parasite was shown to cause important reproductive losses in some sheep flocks in Switzerland ( Hässig et al, 2003 ) as well as in other countries ( Della Rosa et al, 2021 ; Sánchez-Sánchez et al, 2021a , Sánchez-Sánchez et al, 2021b ; González-Warleta et al, 2018 ; Moreno et al, 2012 ); therefore, N. caninum should be also considered in the differential diagnosis of reproductive failure in small ruminants.…”

“…Neospora caninum is well recognised as a major abortifacient in cattle ( Dubey et al, 2017 ) and although it seems to have a lower clinical and economic importance in small ruminants, there is increasing evidence of its involvement in cases of abortion and reproductive failure both in sheep and goats worldwide ( Moreno et al, 2012 ; Della Rosa et al, 2021 ; Sánchez-Sánchez et al, 2021a , Sánchez-Sánchez et al, 2021b ; Unzaga et al, 2014 ; Dubey et al, 2017 ; Hässig et al, 2003 ).…”

“…N. caninum DNA was isolated from aborted foetuses. ( Sánchez-Sánchez et al, 2021a , Sánchez-Sánchez et al, 2021b ) Extremadura: Badajoz, and Andalusia: Córdoba and Jaén ELISA (ID Screen Neospora caninum Indirect Multispecies, ID.vet, France) 4/209 1.9 3/12 25.0 Culled Merino and crossbred ewes with no particular disease, extensive breeding systems ( Astorga et al, 2014 ) Castilla-La Mancha: Ciudad Real province ELISA (cELISA Neospora caninum Antibody Test Kit, VMRD, USA) 7/180 3.9 ns/17 ns Manchega sheep flocks, male and female sheep ( Ruiz-Fons et al, 2014 ) Galicia ELISA (ID Screen Neospora caninum Indirect Multi-species, ID.vet, France) 132/2400 5.5 32/44 72.7 Healthy adult sheep (> 6 months) from lamb-producing flocks ( Díaz et al, 2014 ) Galicia: Lugo Province ELISA (cELISA Neospora caninum Antibody Test Kit, VMRD, USA) 18/177 10.1 ns ns Meat crossbred ewes, semi-extensive breeding system, grazing with hay or silage supplement ( Panadero et al, 2010 ) Switzerland Country-wide ELISA (ID Screen® Neospora caninum Indirect, ID.vet, France) + immunoblot (in house) of inconclusive sera 5/653 0.8 4/143 2.8 Randomly sampled general sheep population, healthy animals, different sex and ages This study Zurich IFAT (in house, cut-off 1:160) 12/117 10.3 1/1 100 Ewes from a flock with abortion problems. N. caninum DNA detected in aborted foetuses ( Hässig et al, 2003 ) United Kingdom England and Wales ELISA (Mastazyme, Mast Diagnostics) + verification of positive sera by IFAT (in house, cut-off 1:50) 3/660 0.45 ns <...…”

“…Reactivation of chronic N. caninum infection during pregnancy and endogenous transplacental transmission of the parasite to the offspring is known to be a common event in cattle, but the information on the efficiency of vertical transmission in small ruminants is still limited ( Lindsay and Dubey, 2020 ). Nevertheless, there is initial evidence that this way of transmission is also efficient in the ovine and caprine hosts ( de Oliveira Junior et al, 2020 ; Feitosa et al, 2021 ; González-Warleta et al, 2018 ; Pereira et al, 2021 ; Sánchez-Sánchez et al, 2021b ).…”

Ovine Neosporosis: The Current Global Situation

“…Similar to bovine neosporosis, the life cycle of N. caninum in sheep begins with infection, which can occur horizontally via the ingestion of sporulated oocysts present in food or water [ 13 , 14 ], vertically via the transplacental route from a previously-infected sheep, which has recently been shown to be the main source of infection in sheep [ 15 , 16 ], as it is in cattle and goats [ 17 , 18 , 19 , 20 ]. Vertical transmission can occur after a pregnant sheep ingests sporulated oocysts, causing exogenous transplacental transmission, or after reactivation during gestation of a chronic infection, causing endogenous transplacental transmission [ 14 , 21 ].…”