Toxoplasmosis in Natural Populations of Ungulates in France: Prevalence and Spatiotemporal Variations

Abstract

Toxoplasmosis is characterized by a complex epidemiology. The risk of infection for humans depends on their contact with infective oocysts in a contaminated environment and on the amount of tissue cysts located within consumed meat. Unfortunately, the prevalence of tissue cysts is largely unknown for game species. Although herbivorous game species are a source of infection for humans, the level of infection found in wildlife can also be used to estimate environmental contamination. The aim of this study was to estimate the prevalence of Toxoplasma gondii infection and analyze its temporal dynamics in one population of chamois (Rupicapra rupicapra), one of mouflon (Ovis gmelini musimon), and two of roe deer (Capreolus capreolus) in France, surveyed during a period of 6 to 28 years. Taking into account individual risk factors, we specifically analyzed the relationship between T. gondii prevalence and meteorological conditions that may influence oocyst survival. Serum samples from 101 chamois, 143 mouflons, and 1155 roe deer were tested for antibodies against T. gondii using the modified agglutination test (MAT), an enzyme-linked immunosorbent assay (ELISA) assay, or both. Using MAT with a threshold of 1:6, seroprevalence was 14.7% in mouflon, 16.8% in chamois, and 43.7% in roe deer. In mouflon and roe deer, seroprevalence was positively correlated with age and/or body mass, in accordance with the hypothesis that antibodies have long-term persistence. In roe deer, seropositivity differed between the two populations and changed linearly over time between 1983 and 2010, increasing by a factor 1.75 every 10 years. Moreover, in this species, the highest prevalences were found during dry and cold years or during warm and moist years, depending on the population. Our results suggest that the risk for people to acquire infection through game meat increases over time, but with high variability according to the population of origin and meteorological conditions of the year.

Does land use within the home range drive the exposure of roe deer (Capreolus capreolus) to two abortive pathogens in a rural agro-ecosystem?

“…The high level of the mean apparent seroprevalence observed in our study (43.7 %) was in accordance with this general pattern and the results of several other studies in Europe 43.7 % in France, 52 % in Belgium, 21.2 % in Spain, 33.9 % in Norway, and 34 % in Sweden (Vikøren et al 2004;Gauss et al 2006;Malmsten et al 2011;De Craeye et al 2011;Gotteland et al 2014). By contrast, the prevalence of C. abortus in wild mammals is poorly documented (Pospischil et al 2012).…”

“…We showed that roe deer exposure to T. gondii varied among years in relation to rainfall and temperature. Interannual variability in seroprevalence as a function of yearly rainfall and temperature has also been described in two other roe deer populations in France (Gotteland et al 2014). These results thus confirm previous observations, indicating that the survival of oocysts, and thus the contact between roe deer and infectious T. gondii, is highest during wet years with mild winters (Lélu et al 2012).…”

“…Gotteland et al (2014) found that seroprevalence increased with age in only one of the two roe deer populations they studied. This suggests that the increase with age may be due to repeated exposure rather than to antibody persistence.…”

A systematic review and meta‐analysis of Toxoplasma gondii in roe deer (Capreolus capreolus) and red deer (Cervus elaphus) in Europe

“…Another possible source of heterogeneity could have been the age of the animal tested. Several authors recorded higher seroprevalence in older animals, claiming that this might reflect a longer period of exposure with an increase probability of acquiring the infestation (Almería et al., 2018; Gotteland et al., 2014; Heddergott et al., 2018; Sevila et al., 2014; Vikøren et al., 2004). However, we could not study the age‐prevalence pattern because not all the studies reported information about animal age or they did not apply homogenous criteria for age classification.…”

Toxoplasma gondii Infection in Seagull Chicks Is Related to the Consumption of Freshwater Food Resources

“…The highest seroprevalence observed in 2009 was not related to a particular colony, since no significant differences in seroprevalence were observed among colonies that year, and the variations seemed to be independent of the origin of the diet. Temporal, year-to-year variations have also been explained by the effect of variable meteorological conditions on the level of infection in domestic [ 26 ] and wild species [ 27 ]. Although seroprevalence fluctuation in wildlife populations has been studied [ 28 ], further studies will be needed to explain seroprevalence of T .…”