Environmental determinants of spatial and temporal variations in the transmission of Toxoplasma gondii in its definitive hosts

Abstract

Toxoplasmosis is a major zoonosis, and its prevention requires multiple approaches due to the complex life-cycle of its causative agent, Toxoplasma gondii. Environmental contamination by oocysts is a key factor in the transmission of T. gondii to both humans and meat-producing animals; however, its spatial and temporal variations are poorly understood. We analysed the distribution of T. gondii seropositivity in a sample of 210 cats, including the European wildcat (Felis silvestris silvestris), the domestic cat (Felis silvestris catus) and their hybrids that were collected in Central and Eastern France between 1996 and 2006. We searched for spatial variability among communes and temporal variations among years to relate this variability to landscape and meteorological conditions, which can affect the population dynamics of rodent hosts and the survival of oocysts. The overall seroprevalence was 65.2% (95% CI: 58.6-71.4). As expected, adults were more often infected than young individuals, while the occurrence of infection was not related to cat genotypes. Seroprevalence correlated significantly with farm density and the North-Atlantic Oscillation index, which describes temporal variations of meteorological conditions at the continental scale. The highest seroprevalence values were obtained in areas with high farm densities and during years with cool and moist winters. These results suggest that both farming areas and years with cool and wet winters are associated with increased T. gondii seroprevalence in cats. As cat infection determines the environmental contamination by oocysts, climate and landscape characteristics should be taken into account to improve the risk analysis and prevention of T. gondii.

Keywords: Farm density; Felis catus; Felis silvestris; Meteorological variations; North-Atlantic Oscillation index; Toxoplasmosis.

Graphical abstract

Fig. 1

European wildcat (Felis s. silvestris) distribution in France (grey area; Léger et al., 2008; Say et al., 2012), and locations of samples from domestic cats (Felis s. catus), wildcats and their hybrids. Cat types are represented by different symbols (see the bottom left of the map). One location might correspond to several individuals (1, 2, 3, or 8), the size of the dot being proportional to the number (indicated at the right of the symbols) of individuals collected in each commune.

Fig. 2

Interannual variations in Toxoplasma gondii seroprevalence in the three types of cats standardised by age (bars) during the study period. Line segments represent the 95% confidence intervals for seroprevalence, and the numbers in brackets indicate the sample sizes. Wildcats (Felis s. silvestris), domestic cats (Felis s. catus) and hybrids are pooled.

Fig. 3

Predicted relationships between NAO winter index and the probability of seropositivity for Toxoplasma gondii in all cats sampled; (a) juveniles and (b) adults. Points represent the observed seoprevalence values with 95% confidence intervals as whiskers. A median farm density (0.68 farm/km²) was used to calculate the predictions (full line). Minimal farm density (0 farm/km²) observed among sampled communes was used to calculate the minimal predictions of the model (dotted lines). High values of farm density (2 and 4 farms/km²) were used to calculate the maximal predictions of the model (dashed and dotted-dashed lines).