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Revista Brasileira de Parasitologia Veterinária

Print version ISSN 0103-846XOn-line version ISSN 1984-2961

Rev. Bras. Parasitol. Vet. vol.24 no.3 Jaboticabal July/Sept. 2015  Epub Aug 28, 2015

http://dx.doi.org/10.1590/S1984-29612015050 

Original Article

The prevalence of antibodies to Toxoplasma gondii in horses in Changji Hui Autonomous Prefecture, Xinjiang, northwestern China

Prevalência de anticorpos contra Toxoplasma gondiiem cavalos na Região de Uygur, Xinjiang, Noroeste da China

Jin-Lei Wang 1  

Dong-Hui Zhou 1   *  

Jia Chen 1  

Guang-Xue Liu 1  

Wen-Bing Pu 2  

Ting-Yu Liu 2  

Si-Yuan Qin 1  

Ming-Yang Yin 1  

Xing-Quan Zhu 1  

1State Key Laboratory of Veterinary Etiological Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Gansu Province, Lanzhou, PR China

2Changji Prefecture Animal Disease Control and Prevention Center, Xinjiang Uygur Autonomous Region, PR China


ABSTRACT

Toxoplasmosis is a worldwide zoonosis caused by Toxoplasma gondii, which can infect warm-blooded animals and humans. The present study was performed to investigate the seroprevalence of T. gondii in horses in Xinjiang, northwestern China. A total of 637 blood samples were collected from seven regions in Changji Hui Autonomous Prefecture, Xinjiang in 2011 and assayed for T. gondiiantibodies using the modified agglutination test (MAT). Risk factors (age, gender, and region) related to seroprevalence were determined by a multivariate logistic regression analysis. A total of 200 horses (31.4%, 95% CI 27.79–35.00) were seropositive for T. gondii. Age, gender, and region present no association with seroprevalence (p>0.05) in the logistic regression analysis. The results indicated that T. gondii is widely prevalent in horses in Xinjiang, northwestern China, representing a serious threat to animal and human health. Therefore, more careful measures should be performed to control and prevent T. gondii infection in horses from Xinjiang, northwestern China.

Key words: Toxoplasma gondii ; horse; seroprevalence; modified agglutination test (MAT); China

RESUMO

A toxoplasmose é uma zoonose global causada pelo Toxoplasma gondii, o qual pode infectar animais de sangue quente e seres humanos. Este estudo foi realizado com o objetivo de investigar a soroprevalência em cavalos para T. gondii, na região de Xinjiang, no Noroeste da China. Em 2011, foram recolhidas 637 amostras de sangue em sete distritos da Prefeitura Autônoma de Changji Hui do Xinjiang, as quais foram testadas para a presença de anticorpos, utilizando-se o teste de aglutinação modificado (MAT). Foram estimados fatores de risco relacionados com a soroprevalência (idade, sexo e distrito), através de uma análise de regressão logística multivariada. Um total de 200 equinos (31,4%, 95% IC 27,79 – 35,00) foi positivo para T. gondii. Idade, sexo e região estudada não apresentaram associação com a soroprevalência (p>0,05) na análise de regressão logística. Os resultados revelam que a infecção por T. gondii tem uma prevalência generalizada em todo o território de Xinjiang, no Noroeste da China, constituindo uma séria ameaça à saúde de animais e de humanos. Consequentemente, propõe-se que sejam adotadas medidas reforçadas para o controle e prevenção da infecção de cavalos por T. gondii, no Xinjiang, Noroeste da China.

Palavras-Chave: Toxoplasma gondii ; cavalo; soroprevalência; teste de aglutinação modificado (MAT); China

Introduction

Toxoplasma gondii is an important zoonotic intracellular apicomplexan protozoan that can infect humans and nearly all warm-blooded animals worldwide (Dubey, 2010; Montoya & Liesenfeld, 2004; Tenter et al., 2000; Sousa et al., 2014; Cerro et al., 2014; Barros et al., 2014). Humans and animals can be infected mainly through the ingestion of tissue cysts from undercooked or raw meat or through the consumption of food or water contaminated with sporulated oocysts shed by infected felids (Kijlstra & Jongert, 2008). Around the world, approximately one-third of the human population has been infected with T. gondii, and it is estimated that nearly 7.88% of the population in China has been exposed to T. gondii (Dubey, 2010; Zhou et al., 2011). Toxoplasmosis is typically asymptomatic in healthy individuals but can cause mortality and morbidity in congenitally infected and immunocompromised patients, such as individuals with AIDS (Montoya & Liesenfeld, 2004; Belanger et al., 1999).

Felids are the only recognised definitive hosts of T. gondii, but humans and virtually all warm-blooded species, including horses, can be intermediate hosts (Elmore et al., 2010). Horses are widely distributed in the Xinjiang Uygur Autonomous Region, serving as an important means of transportation for the local population. Humans may acquire T. gondii infections by consuming improperly cooked horse meat containing tissue cysts (Pomares et al., 2011). In horses, T. gondii infection is generally subclinical; however, atypical clinical symptoms, including fever, ataxia, retinal degeneration and encephalomyelitis, sometimes appear (Dubey et al., 1999). In China, although there are several serological surveys for T. gondii infection in horses and some Chinese reports were recently summarised (Miao et al., 2013; Yang et al., 2013), information on horses remains limited in northwestern China. To the best of our knowledge, there has been only one survey performed in Xinjiang, northwestern China, and it took place more than 10 years ago. In that survey, T. gondii antibodies were assayed by IHA, and no positive sample was observed in the 60 serum samples. The aim of the present survey was to examine the prevalence of antibodies against T. gondii in horses in Xinjiang, northwestern China, providing fundamental data for understanding the main transmission routes between animals and humans, as well as preventing and controlling this disease.

Materials and Methods

Region and samples

Xinjiang Uygur Autonomous Region is located in northwest China, covering an area of approximately 1,660,000Km2 and occupying approximately one-sixth of the area of China. The climate in this region is typically temperate and monsoonal continental with an annual precipitation of 150 mm, temperature differences between day and night, and abundant sunshine (yearly sunlight exposure of 2500–35000 h). A total of 637 blood samples were collected from August to December in 2011 in Changji Hui Autonomous Prefecture, Xinjiang. In total, 84, 103, 80, 91, 94, 93 and 92 blood samples were obtained from Miao’ergou, Jimusa’er, Hutubi, Qitai, Manasi, Fukang, and Mulei Kazakh Autonomous County, respectively. Information regarding the age, gender and geographic origin of each horse were obtained. The ages of the horses were classified into four groups: foal (0<age≤1, 129 samples), adolescent (1<age≤5, 118 samples), middle-aged (5<age≤10, 326 samples) and elderly (age>10, 64 samples). In total, 248 of the sampled animals were male, and 389 were female. Blood samples were centrifuged at 3000 × g for 5 min. The separated serum samples were stored at –20°C until use.

Serological assay

T. gondii antibodies were detected in serum samples by the modified agglutination test (MAT) as described previously (Dubey & Desmonts, 1987). In brief, serum samples were added to 96-well “U” bottomed polystyrene plates and then diluted twofold from 1:25 to 1:3200. Positive and negative control serums were included in each test, and controversial serums were re-tested. Horse sera with MAT titres of 1:25 or higher were considered positive for T. gondii antibodies based on previous studies (Yang et al., 2013; García-Bocanegra et al., 2012; Alvarado-Esquivel et al., 2012).

Statistical analysis

Statistical analysis was performed using SAS [Version 8.0] and SPSS [Release 18.0 standard version]. The risk factors (age, gender and region) were analysed using multivariable logistic regression models in SPSS. Differences in the seroprevalence of T. gondii-infected male and female horses, among various age groups and regions, were analysed using a Chi square test with SPSS. A value of P<0.05 was considered statistically significant.

Results

A total of 637 horses from seven regions in Changji Hui Autonomous Prefecture, Xinjiang, were assayed by MAT for T. gondii antibodies. In total, 200 of 637 horses (31.4%, 95% CI 27.79–35.00) were seropositive for T. gondii with titres of 1:25 in 86 individuals, 1:50 in 55, 1:100 in 37, 1:200 in 11, 1:400 in 2, 1:800 in 3, and 1:1600 or higher in 6. The seroprevalence of T. gondii infection from seven regions ranged from 27.7% in Manasi to 37.5% in Hutubi. Infected horses were observed in all age groups, ranging from 26.6–35.7%. Prevalence in female was 33.1% and in male horses 28.9% (Table 1).

Table 1 Seroprevalence of Toxoplasma gondii infection in horses in Changji, Xinjiang Uygur Autonomous Region, northwestern China. 

Factor Category No. tested No. positive Prevalence (%) 95% CI OR (95%) p-value
Gender Male 248 71 28.6 23.1–34.7 Reference P = 0.255
Female 389 129 33.2 28.5–38.1 1.24 (0.87–1.75)
Age 0<age≤1 129 46 35.7 27.4–44.6 Reference P = 0.587
0<age≤5 118 35 29.7 21.6–38.8 0.76 (0.45–1.30)
5<age≤10 326 102 31.3 26.4–36.7 0.82 (0.53–1.26)
age>10 64 17 26.6 16.3–39.1 0.65 (0.34–1.26)
Region Fukang 93 28 30.1 21.0–40.5 Reference P = 0.829
Jimusa’er 103 34 33.0 24.1–43.0 1.14 (0.63–2.10)
Hutubi 80 30 37.5 26.9–49.0 1.39 (0.74–2.62)
Qitai 91 27 29.7 20.5–40.2 0.98 (0.52–1.84)
Mulei 92 31 33.7 24.2–44.3 1.17 (0.63–2.20)
Manasi 94 26 27.7 18.9–37.8 0.89 (0.47–1.67)
Miao’ergou 84 24 28.6 19.2–39.5 0.93 (0.49–1.78)
Total 637 200 31.4 27.8–35.3

No. represents Number; CI is confidence intervals; OR is Odds-ratios.

Discussion

Age, gender and region were not significant in the logistic regression analysis (P > 0.05), suggesting that age, gender and region were not crucial factors for T. gondii infection, a finding that was consistent with the results of previous studies (Miao et al., 2013; Yang et al., 2013). The present study showed that all the regions had T. gondii positive horses, and there were no significant differences among the various regions in Changji Hui Autonomous Prefecture, Xinjiang (P > 0.05). Seroprevalence to T. gondii in male horses (28.6%, 95% CI 23.00–34.26) was lower than that in female horses (33.1%, 95% CI 28.48–37.84). Difference was not significant (p>0.05). Similar findings were reportedin a previous study in Portugal (Lopes et al., 2013). Regarding age group, also no association was observed, however the highest prevalence (35.7%, 95% CI 27.39–43.93) was observed in foals. A relatively lower prevalence was observed in older horses (26.6%, 95% CI 15.74–37.38), which was contrary to the result reported in a previous survey in Tunisia (Boughattas et al., 2011).

Globally, a few surveys have previously reported the prevalence of T. gondii in horses (Table 2). In the present study, the overall average T. gondii seroprevalence in Changji Hui Autonomous Prefecture, Xinjiang was 31.4%, which was similar to that observed in Yunnan Province (30.5%) but higher than that in Liaoning province (25.0%) (Miao et al., 2013; Yang et al., 2013). Horses are considered clinically resistant to T. gondii, and the prevalence of T. gondii in horses was generally lower in most countries, such as 1% in Sweden (Jakubek et al., 2006); 1.8% in Greece (Kouam et al., 2010); 2.6% in Jeju Island, South Korea (Gupta et al., 2002); 6.1% in Mexico (Alvarado-Esquivel et al., 2012); 6.9% in North America (Dubey et al., 1999); 7.2% in Turkey (Karatepe et al., 2010); 10.8% in southern Spain (García-Bocanegra et al., 2012); and 13.3% in Portugal (Lopes et al., 2013). However, higher prevalences included 31.6% in Saudi Arabia (Alanazi & Alyousif, 2011); 34% in Costa Rica (Dangoudoubiyam et al., 2011); 52.6% in Egypt (Shaapan & Ghazy, 2007); and 71.2% in Iran (Hajialilo et al., 2010). These differences in seroprevalence are most likely caused by differences in ecological and geographical factors, serological test methods, living styles and the number of infected cats.

Table 2 The seroprevalence of Toxoplasma gondii infection in horses globally. 

Region Sample size Prevalence (%) Serological test Cut off Reference
Ankara Province ,Turkey 100 28.0 SFDT 1:16 (Güçlü et al., 2007)
Curitiba, Paraná, Brazil 100 17.0 IFAT 1:64 (Finger et al., 2013)
Costa Rica 315 34.0 MAT 1:25 (Dangoudoubiyam et al., 2011)
Czech Republic 522 22.6 LAT / (Bártová et al., 2010)
Durango State, Mexico 495 6.1 MAT 1:25 (Alvarado-Esquivel et al., 2012)
Fernando de Noronha, Brazil 16 43.7 MAT 1:25 (Costa et al., 2012)
Giza-Zoo Egypt 150 52.6 Bioassays in mice / (Shaapan & Ghazy, 2007)
Greater Cairo, Egypt 100 25.0 ELISA / (Haridy et al., 2009)
Greece 753 1.8 ELISA / (Kouam et al., 2010)
Jeju Island, South Korea 191 2.6 IFAT 1:100 (Gupta et al., 2002)
Liaoning Province, China 711 25.0 MAT 1:25 (Yang et al., 2013)
New Caledonia 25 16.0 ELISA / (Roqueplo et al., 2011)
Niğde Province, Turkey 125 7.2 SFDT 1:16 (Karatepe et al., 2010)
North America 1788 6.9 MAT 1:20 (Dubey et al., 1999)
Portugal 173 13.3 MAT 1:20 (Lopes et al., 2013)
Qazvin, Iran 52 71.2 MAT 1:20 (Hajialilo et al., 2010)
Riyadh Province, Saudi Arabia 266 31.6 SFDT 1:16 (Alanazi & Alyousif, 2011)
Southern Spain 454 10.8 MAT 1:25 (García-Bocanegra et al., 2012)
Swedish 414 1.0 DAT 1:40 (Jakubek et al., 2006)
Tunisia 158 17.7 MAT 1:20 (Boughattas et al., 2011)
Urmia, Northwest Iran 26 11.5 MAT 1:20 (Raeghi et al., 2011)
Yunnan Province, China 266 30.5 IHA 1:64 (Miao et al., 2013)

MAT: modified agglutination test; IHA: indirect hemagglutination test; ELISA: enzyme-linked immunoabsorbent assay; SFDT: Sabin Feldman dye test; LAT: latex agglutination test; DAT: direct agglutination test; IFAT: indirect fluorescence antibody test.

The results of the present study indicated a high prevalence of T. gondii in horses in Changji Hui Autonomous Prefecture, Xinjiang, which may represent a potential source of human infection with T. gondii. Therefore, a more targeted approach to address this problem should be executed to control and prevent T. gondii infection in horses from Xinjiang, northwestern China.

Acknowledgements

This study was funded by the National Natural Science Foundation of China (Grant No. 31302085) and the Science Fund for Creative Research Groups of Gansu Province (Grant No. 1210RJIA006).

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Received: February 06, 2015; Accepted: May 14, 2015

*Corresponding author: Dong-Hui Zhou. State Key Laboratory of Veterinary Etiological Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Gansu Province 730046, Lanzhou, PR China. e-mail: zhoudonghui@caas.cn

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