Abstract
Toxoplasma gondii causes serious infection worldwide in humans and animals. In this study, the seroepidemiology of toxoplasmosis was investigated in wild boars (Sus scrofa) (n=377), wild rabbits (cape hare, Lapus capensis) (n=331), and wild chickens (red junglefwol, Gallus gallus) (n=571) in 4 forested and country sided area of Hubei province of China. For this, blood samples were collected and tested by indirect hemagglutination test (IHA). The seroprevalence was found to be 7.2%, 5.1%, and 12.6% in wild boars, rabbits, and chickens, respectively, with significant differences among these species. The prevalence of T. gondii infection in male and female wild boars was found to be 7.9% and 6.5% (P<0.01), in male and female rabbits was 5.6% and 4.9% (P<0.01), and in male and female chickens was 17.1% and 7.7% (P<0.01), respectively, with significant differences between 2 genders of chickens (P<0.01). The findings of this study may help in planning of the prevention measures against T. gondii infection in wild animals in this area.
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Key words: Toxoplasma gondii, seroprevalence, indirect hemagglutination, wild boar, wild rabbit, wild chicken, Hubei province
Toxoplasma gondii is a world-widely distributed pathogen infecting almost all warm-blooded animals [
1,
2]. Toxoplasmosis caused by
T. gondii is one of the most prevalent zoonotic diseases in domestic and wild animals, including wild rabbits, chickens, and pigs [
3], causing fatality in rabbits [
4]. The pathogenicity of
T. gondii infection varies from symptomless infections to death [
1]. Previous studies have reported that rabbits infected with
T. gondii were a source of infection for cats which shed the environmentally resistant oocysts [
5]. Infected rabbits can be a source of infection to humans too. In fact, consumption of rabbit meat was recently associated with
T. gondii infection in humans in Mexico region [
6].
T. gondii infection in pigs has been shown to cause serious economic losses in many countries [
7–
9]. Apart from infecting the pigs,
T. gondii has also been reported to cause infection in dogs and chickens. Infection in dogs is very important for the reason that it may indicate the parasites pollution levels in their lives and can be considered as a mechanical vector [
10]. The chickens show less clinical signs of toxoplasmosis always following the chronic type of infection with high seropositive rates [
11]. Keeping in view the importance of chicken meat for human consumption,
T. gondii infection in these birds has been considered very dangerous, as the infected chickens may transmit the parasite to humans through undercooked meat [
2].
In humans,
T. gondii infection is asymptomatic generally [
12]; however, the risk to pregnant women is enormous developing severe diseases like encephalitis, abortion, blindness, and mental retardation [
13]. Toxoplasmosis has been reported to infect 1/3 of the world population [
14–
16]. However, limited reports are available or not focused of this infection in wild animals. So keeping in view, the current study was designed to investigate the prevalence of toxoplasmosis in wild pigs (wild boars), rabbits, and chickens in forested area of Hubei province, China.
The present study was performed under the instructions and approval of the ethics committee of Huazhong Agricultural University (permit no. 4200695757).
All the samples were collected in wild and forested area of Hubei province located in central part of China (
Fig. 1). A total of 1,279 blood samples from wild boars (
Sus scrofa) (n=377), wild rabbits (cape hare,
Lapus capensis) (n=331), and wild chickens (red junglefwol,
Gallus gallus) (
Table 1) were collected during 2010 to 2016. After collection, all the blood samples were centrifuged at 3,000 g for 20 min, and serum was separated and stored at −20°C till later analysis.
Each serum sample was tested for IgG antibodies against T. gondii by employing a commercial indirect agglutination test (IAT, Lanzhou Veterinary Research Institute of Chinese Academy of Agricultural Sciences, Gansu, China) according to the manufacturer’s instructions. The test was considered positive when a layer of agglutinated erythrocytes was formed in wells employing serum dilutions of 1:64 or higher, and positive and negative controls were included in each test. Statistical analysis was performed by chi-square test with Statistical Analysis System, Version 18.0 (SAS Institute, Cary, North Carolina, USA). The differences were considered statistically significant when P<0.05.
The results showed that the antibodies against
T. gondii was found in 377 wild boars (7.2%), 331 rabbits (5.1%), and 571 chickens (12.6%) with significant differences among 3 species (
P<0.01). The prevalence of
T. gondii infection in male and female wild boars was found to be 7.9% and 6.5% (
P<0.01), that in male and female rabbits was 5.6% and 4.9% (
P<0.01), and that in male and female chickens was 17.1% and 7.7% (
P<0.01), respectively. Significant differences were found between 2 genders of chickens (
P<0.01) (
Table 1).
Since the discovery of complete life cycle of
T. gondii in 1970, a large number of
T. gondii seropositive wild and domestic animals have been identified and reported globally [
2]. The current seroprevalence of
T. gondii in wild boars (7.2%) was lower than that reported previously in domesticated pigs in nearby Guizhou provinces and Chongqing area [
17–
19]. This may possibly be decided by the climatic conditions in these areas and of course, the domesticated region because of the lower annual average temperature and precipitation of Hubei province than Guizhou and Chongqing regions. As the survival rate of
T. gondii oocysts are longer in warmer and more humid environments [
5], this might be the reason of low seroprevalance of this infection in Hubei province.
In the present study, a low seroprevalence (5.1%) of
T. gondii infection was tested in wild rabbits, which is significantly lower that the seroprevalence of
T. gondii infection as manifested in Mexican regions [
18,
20,
21]. The differences are likely to be associated with different investigative methods, ecological and geographical factors, and climates [
3]. As chickens have direct feeding habit from the ground, the seroprevalence of
T. gondii infection can be considered a reflection of environmental contamination [
12]. This might be the reason that the prevalence of
T. gondii in wild chickens in our study was significant higher than other species in this region. Moreover, the prevalence of this parasitic infection in chickens in our study (12.6%) was also lower than that of the prevalence as reported previously in the same host species in Henan province of China (18.9%) and other parts of the world, i.e., Ghana (64.0%), Indonesia (24.4%), and Poland (24.2%) [
22,
23].
Demand for the meat of wild animals, including pigs, rabbits, and chickens for human consumption is increasing because of the leanness of their meat [
4], low fat and rich nutrition, and of course increasing human population. Additionally, like other countries, there are no regulations concerning sale and slaughter of these animals. Therefore, infection in wild animals could be of importance in the epidemiology of toxoplasmosis. Especially, wild boars, rabbits, and chickens are hunted and consumed by humans. The consumption of meat and meat-derived products containing cysts of
T. gondii can be an important source of infection for humans. Moreover, the personnel dealing with such type of meat coupled with poor hygienic measures may also become infected during evisceration and handling of the carcass [
2].
In conclusion, the current study reported for the first time the prevalence of T. gondii infection in wild animals in Hubei province of China. As a zoonotic parasite, the infected animals may transmit the infestation to other animals and even human beings in this area. Our results may help in planning the preventive measures against T. gondii infection in wild animals in this province.
Notes
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CONFLICT OF INTEREST
None of the authors have any conflict of interest.
ACKNOWLEDGMENTS
This study was supported by the Wenzhou City Public Welfare Science and Technology Plan Projects (no. N2014004) and Startup Project of Doctor Scientific Research of Wenzhou Vocational College of Science and Technology in 2016 (no. 201604).
Fig. 1Geographical distribution of sample collection.
Table 1Seroprevalence of T. gondii in different animals by indirect agglutination test in Hubei province, China
Table 1
|
Animalsa
|
No. males positive/No. total samples |
Seroprevalence (%) |
No. females positive/No. total samples |
Seroprevalence (%) |
No. total positive/No. total samples |
Seroprevalence (%) |
|
Wild boars |
15/191 |
7.9 |
12/186 |
6.5 |
27/377 |
7.2 |
|
Wild rabbits |
6/107 |
5.6 |
11/224 |
4.9 |
17/331 |
5.1 |
|
Wild chickensb
|
51/299 |
17.1 |
21/272 |
7.7 |
72/571 |
12.6 |
References
- 1. Dubey JP. Toxoplasmosis of Animals and Humans. 2nd ed. Boca Raton, Florida, USA. CRC Press. 2010, pp 1-313.
- 2. Li K, Gao J, Shahzad M, Han Z, Nabi F, Liu M, Zhang D, Li J. Seroprevalence of Toxoplasma gondii infection in yaks (Bos grunniens) on the Qinghai-Tibetan Plateau of China. Vet Parasitol 2014;205:354-356.
- 3. Luo HQ, Li K, Zhang H, Wu B, Wang J, Shahzad M, Tu YQ, Song XZ, Sun SW. Seroepidemiology of Toxoplasma gondii and Neospora caninum infections in goats in Hubei province, China. Trop Biomed 2016;33:285-289.
- 4. Alvarado-Esquivel C, Alvarado-Esquivel D, Villena I, Dubey JP. Seroprevalence of Toxoplasma gondii infection in domestic rabbits in Durango State, Mexico. Prev Vet Med 2013;111:325-328.
- 5. Dubey JP, Passos LM, Rajendran C, Ferreira LR, Gennari SM, Su C. Isolation of viable Toxoplasma gondii from feral guinea fowl (Numida meleagris) and domestic rabbits (Oryctolagus cuniculus) from Brazil. J Parasitol 2011;97:842-845.
- 6. Alvarado-Esquivel C, Torres-Berumen JL, Estrada-Martínez S, Liesenfeld O, Mercado-Suarez MF. Toxoplasma gondii infection and liver disease: a case-control study in a northern Mexican population. Parasit Vectors 2011;4:75.
- 7. Chen XG, Wu K, Lun ZR. Toxoplasmosis researches in China. Chin Med J (Engl) 2005;118:1015-1021.
- 8. Dubey JP. Toxoplasmosis in pigs-the last 20 years. Vet Parasitol 2009;164:89-103.
- 9. Garcia-Bocanegra I, Simon-Grifé M, Dubey JP, Casal J, Martín GE, Cabezón O, Perea A, Almería S. Seroprevalence and risk factors associated with Toxoplasma gondii in domestic pigs from Spain. Parasitol Int 2010;59:421-426.
- 10. Frenkel JK, Lindsay DS, Parker BB. Dogs as potential vectors of Toxoplasma gondii. Am J Trop Med Hyg 1995;53:226.
- 11. Zou J, Huang XX, Yin GW, Ding Y, Liu XY, Wang H, Chen QJ, Suo X. Evaluation of Toxoplasma gondii as a live vaccine vector in susceptible and resistant hosts. Parasit Vectors 2011;4:168.
- 12. Dubey JP. Toxoplasma gondii infections in chickens (Gallus domesticus): prevalence, clinical disease, diagnosis and public health significance. Zoonoses Public Health 2010;57:60-73.
- 13. Cook AJ, Gilbert RE, Buffolano W, Zufferey J, Petersen E, Jenum PA, Foulon W, Semprini AE, Dunn DT. Sources of toxoplasma infection in pregnant women: European multicentre case–control study. BMJ 2000;312:142-147.
- 14. Montoya JG, Liesenfeld O. Toxoplasmosis. Lancet 2004;363:1965-1976.
- 15. Fallahi SH, Kazemi B, Seyyed tabaei SJ, Bandehpour M, Lasjerdi Z, Taghipour N, Zebardast N, Nikmanesh B, Omrani VF, Ebrahimzadeh F. Comparison of the RE and B1 gene for detection of Toxoplasma gondii infection in children with cancer. Parasitol Int 2014;63:37-41.
- 16. Zhou P, Chen Z, Li HL, Zheng H, He S, Lin RQ, Zhu XQ. Toxoplasma gondii infection in humans in China. Parasit Vectors 2011;4:165.
- 17. Hong NN, Qian DX, Zhang DX, Hua Y, Li T, Ran LZ, Tian HR, Liu X, Yu TD. Serological investigation of pig’s toxoplasmosis in Guizhou province, China. J Vet Parasitol 2010;18:68-70. (in Chinese).
- 18. Dubey JP, Alvarado-Esquivel C, Liesenfeld O, Herrera-Flores RG, Ramírez-Sánchez BE, González-Herrera A, Martínez-García SA, Bandini LA, Kwok OC. Neospora caninum and Toxoplasma gondii antibodies in dogs from Durango City, Mexico. J Parasitol 2007;93:1033-1035.
- 19. Li YN, Nie X, Peng QY, Mu XQ, Zhang M, Tian MY, Min SJ. Seroprevalence and genotype of Toxoplasma gondii in pigs, dogs and cats from Guizhou province, Southwest China. Parasit Vectors 2015;8:214.
- 20. Cedillo-Peláez C, Díaz-Figueroa ID, Jiménez-Seres MI, Sánchez-Hernández G, Correa D. Frequency of antibodies to Toxoplasma gondii in stray dogs of Oaxaca, Mexico. J Parasitol 2012;98:871-872.
- 21. Dubey JP, Velmurugan GV, Alvarado-Esquivel C, Alvarado-Esquivel D, Rodríguez-Peña S, Martínez-García S, González-Herrera A, Ferreira LR, Kwok OC, Su C. Isolation of Toxoplasma gondii from animals in Durango, Mexico. J Parasitol 2009;95:319-322.
- 22. Dubey JP, Huong LT, Lawson BW, Subekti DT, Tassi P, Cabaj W, Sundar N, Velmurugan GV, Kwok OC, Su C. Seroprevalence and Isolation of Toxoplasma gondii from free-range chickens in Ghana, Indonesia, Italy, Poland, and Vietnam. J Parasitol 2008;94:68-71.
- 23. Feng Y, Lu Y, Wang Y, Liu J, Zhang L, Yang Y. Toxoplasma gondii and Neospora caninum in free-range chickens in Henan province, China. Biomed Res Int 2016;8290536.
