Abstract
Until now, no information on Toxoplasma gondii seroprevalence in Arctic foxes (Vulpes lagopus) was available in China. A serological survey was undertaken to assess T. gondii seroprevalence in farmed Arctic foxes in eastern and northeastern China. Antibodies to T. gondii were examined in 1346 farmed Arctic foxes using the modified agglutination test (MAT). A total of 113 (8.39%, 95% confidence interval [CI] 6.91–9.87) serum samples were positive to T. gondii at a 1:25 cutoff. Seroprevalence of T. gondii infection in male Arctic foxes was 8.68% (95% CI 6.75–10.6), which was higher than that in the female Arctic foxes (7.95%, 95% CI 5.65–10.26). The prevalence in polar foxes was 7.07% (95% CI 5.14–8.99), which was lower than that in the blue foxes (9.75%, 95% CI 7.49–11.99). T. gondii seroprevalence in Arctic foxes in Heilongjiang, Jilin, Liaoning, and Shandong Provinces was 9.85% (95% CI 5.75–13.95), 9.21% (95% CI 5.54–12.87), 7.37% (95% CI 5.22–9.51), and 8.68% (95% CI 5.66–11.70), respectively. There were no statistically significant differences between T. gondii seroprevalence and morphs, sex, or regions of Arctic foxes in logistic regression analysis (p < 0.05). The results of the present survey indicated that T. gondii infection in farmed Arctic foxes is prevalent in China. To our knowledge, this is the first report of T. gondii seroprevalence in Arctic foxes in China.
Introduction
T
According to their coat color phenotype in winter, the Arctic fox (Vulpes lagopus) is divided naturally into two color morphs—white and blue, named polar fox and blue fox, respectively (Filistowicz et al. 1997, Våge et al. 2005). It has been a several decades since Arctic foxes were introduced into China from the former Soviet Union in the 1950s (Zhang 2001). Today, it has become an important economic animal because its thick fur has high economic value (Tan et al. 2007). The farmed Arctic foxes usually feed on forage that contains small rodents, which may play an important role in the transmission of T. gondii to other animals (Yan et al. 2014).
Some investigations of T. gondii seroprevalence in wild Arctic foxes (Prestrud et al. 2007, Akerstedt et al. 2010) and farmed Arctic foxes (Górecki et al. 2012) have been described. However, there is no report on T. gondii infection in Arctic foxes in China. Therefore, the present study was conducted to evaluate the seroprevalence of T. gondii infection in farmed Arctic foxes in China for the first time.
Materials and Methods
The investigation site
The investigation was implemented in four provinces of northeastern China and parts of the east China, namely Jilin Province (121°38′–131°17′E, 40°52′–46°18′N), Heilongjiang Province (121°11′–135°05′E, 43°26′–53°33′N), Liaoning Province (118°53′–125°46′E; 38°43′–43°36′N), and Shandong Province (34°22′–38°23′N; 114°19′–122°43′E). The prevailing climate in northeastern China is a monsoon climate of medium latitudes type with long cold winters and short warm summers. Shandong is a coastal province of eastern China and has four distinct seasons. The four provinces are all major regions of Arctic fox farming.
Serum samples
Blood samples of a total of 1346 Arctic foxes were collected from June, 2014, to January, 2015, in Jilin Province, Heilongjiang province, Liaoning Province, and Shandong Province (Table 1). Blood was collected from the caudal vein of anesthesized Arctic foxes by local veterinary practitioners. Handling of Arctic foxes was performed in strict compliance with the Animal Ethics Procedures and Guidelines of the People's Republic of China. After centrifugation (1000 × g, 10 min), serum samples were obtained and stored at −20°C until used. Information about species, location of the farms, and gender were acquired from farm administrators.
Serological examination
Samples were assayed for antibodies to T. gondii using the modified agglutination test (MAT) according to the previous effective experimental procedures (Dubey et al. 1999, 2014). The test was defined as positive when positive results were obtained at dilutions of 1:25 or higher. Those sera with doubtful reactions were retested, and positive and negative controls were included in each test (Sobrino et al. 2007).
Statistical analysis
Seroprevalence was analyzed statistically considering gender, subspecies, and geographical origin of Arctic fox by chi-squared analysis in SPSS (release 18.0 standard version, SPSS Inc., Chicago, IL). Exploratory analysis was performed to explore variables potentially associated with exposure to T. gondii infection, and all factors were studied in a multivariable logistic regression model. Results were considered statistically significant when p < 0.05. Odds ratios (ORs) with 95% confidence intervals (CI) based on likelihood ratio statistics are reported.
Results and Discussion
Of 1346 serum samples, 113 (8.39%, 95% CI 6.91–9.87) samples were positive for T. gondii infection by MAT at a 1:25 cutoff, with titers of 1:25 in 66, 1:50 in 26, 1:100 in 9, 1:200 in 7, 1:400 in 3, 1:800 in 2 (Table 1). The prevalence of T. gondii infection in Arctic foxes from Jilin Province (n = 239), Heilongjiang Province (n = 203), Liaoning Province (n = 570), and Shandong Province (n = 334) was 9.21% (95% CI 5.54–12.87), 9.85% (95% CI 5.75–13.95), 7.37% (95% CI 5.22–9.51), and 8.68% (95% CI 5.66–11.70), respectively. T. gondii seroprevalence in male and female Arctic foxes was 8.68% (95% CI 6.75–10.61) and 7.95% (95% CI 5.65–10.26), respectively (Table 1). Furthermore, the prevalence of T. gondii infection in polar foxes and blue foxes was 7.07% (95% CI 5.14–8.99) and 9.75% (95% CI 7.49–11.99), respectively.
The total seroprevalence of T. gondii infection in farmed Arctic foxes in eastern and northeastern China was 8.39% (95% CI 6.91–9.87), which was lower than the seroprevalence of wild Arctic foxes in Svalbard at 43% from 1996 to 2004 (Prestrud et al. 2007) and 9.09% in 2005 and 2006 (Prestrud et al. 2008) by direct agglutination test, wild red fox (68%) in Hungary by microscopic agglutination test (Jakubek et al., 2007), and wild red fox (90%) in Missouri and Kansas using the Sabin–Feldman dye test (Smith and Frenkel 1995), but was higher than that in farmed Arctic foxes (0%) by PCR in Poland (Górecki et al. 2012). The seroprevelence of T. gondii in farmed Arctic foxes was lower than that in the wild Arctic foxes. This result is probably due to the fact that wild foxes are parts of the decomposer food chain, and most of their diet that comes from scavenging (Verin et al. 2013). This feeding behavior leads to an increased possibility of foxes ingesting meat containing Toxoplasma tissue cysts. Farmed foxes are omnivorous, and they are sometimes fed plant stuffs containing corn, wheat, and vegetables. Therefore, the different foraging patterns between wild foxes and farmed foxes may lead to different seroprevalences of T. gondii infection.
No significant effects of geographical location were observed on T. gondii seroprevalence in Arctic foxes (p > 0.05). The highest seroprevalence was reported for Heilongjiang Province and the lowest seroprevalence occurred in Liaoning Province. The different seroprevalences of T. gondii in farmed Arctic foxes are probably due to different density populations of Arctic foxes, feed ingredients, feeding conditions, different numbers of domestic cats and human population dispersion, and geographic and climatic conditions for farmed Arctic foxes.
Furthermore, logistic regression analysis indicates that gender and subspecies are not crucial factors for T. gondii seroprevalence in Arctic foxes (p > 0.05). T. gondii seroprevalence in male Arctic foxes was higher than that in the female Arctic foxes. This is probably due to different behavioral types (Górecki et al. 2012). Male Arctic foxes are more active and aggressive than females, thus increasing opportunities of contacting with T. gondii oocysts.
In China, Arctic foxes are domesticated as an economic animal whose fur is a good seller in the international market. Although most of the world's farmed fur is produced by European farmers, there are still approximately 1.5 million farmed foxes in China (Meng et al. 2014). T. gondii could be transmitted to humans through eating meat from an infected Arctic fox. This fact should be taken into account because consumption of raw or inadequately cooked meat should be regarded as a potential source of infection for humans (Gamarra et al. 2008). Furthermore, humans may be infected by T. gondii when handling and eviscerating animals (Lopes et al. 2011). Despite the economic burden of fox diseases, little research has examined the disease distribution in foxes. Foxes are highly susceptible to T. gondii infection (Verin et al. 2013), but this disease has not been reported over the last few decades in China. Therefore, the report of T. gondii seroprevalence in Arctic foxes in China highlights the importance of performing epidemiological surveys in farmed fox populations.
Conclusion
We have presented the first report of T. gondii seroprevalence (8.39%) in farmed Arctic foxes in China. Given the potential detriment to humans and other animals, as well as the potential for economic burden, this information has important implications for preventing and controlling T. gondii infection in farmed Arctic foxes in China.
Footnotes
Acknowledgments
Project support was provided by the Quality Inspection Special Public Welfare Industry Research (grant no. 201410061) and the Science Fund for Creative Research Groups of Gansu Province (grant no. 1210RJIA006). The Laboratoire de Parasitologie-Mycologie, Centre National de Référence de la Toxoplasmose, Centre de Ressources Biologiques Toxoplasma, Hôpital Maison Blanche, Reims Cédex, France, is thanked for providing the Toxoplasma MAT antigen.
Author Disclosure Statement
No completing financial interests exist. The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the funding agencies.