Seroprevalence of Toxoplasma gondii infection in food-producing animals in Northwest China

WANG Meng, YE Qiang, ZHANG Nian-zhang, ZHANG De-lin

(State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of VeterinaryParasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academyof Agricultural Sciences, Gansu Province 730046, China)



Seroprevalence of Toxoplasma gondii infection in food-producing animals in Northwest China

WANG Meng, YE Qiang, ZHANG Nian-zhang, ZHANG De-lin

(StateKeyLaboratoryofVeterinaryEtiologicalBiology,KeyLaboratoryofVeterinaryParasitologyofGansuProvince,LanzhouVeterinaryResearchInstitute,ChineseAcademyofAgriculturalSciences,GansuProvince730046,China)

The obligate intracellularToxoplasmagondiican infect humans through ingestion of raw or undercooked meat containing tissue cysts. The objectives of the present study were to determine theT.gondiiseroprevalence in pigs, cattle, sheep and chickens in Liangzhou, Tianzhu, Minqin and Gulang counties in Hexi Corridor, northwest China. The 1 112 serum samples including 428 pigs, 275 cattle, 130 sheep and 279 chickens were assayed forT.gondiiantibodies by an indirect hemagglutination test (IHAT). A total of 134 serum samples (12.1%, 95% confidence interval, 10.1-14.0) were seropositive withT.gondii. The seroprevalence in pigs (22.7%, 95% CI, 18.7-26.6) was significantly higher (P<0.05) than that in cattle (5.1%, 95% CI, 2.5-7.7), sheep (6.2%, 95% CI, 2.0-10.3) and chickens (5.4%, 95% CI, 27-8.0). Animals from Liangzhou were at a higher risk of infection as compared to all other regions, of which, the difference in pigs was statistically significant (P<0.05). The prevalence in caged chickens and free-range chickens were 3.2% and 9.8% respectively, and the difference was statistically significant (P<0.05). This survey revealed theT.gondiiseroprevalence in pigs, cattle, sheep and chickens in Hexi Corridor, which indicated the potential risk of these animals as a source ofT.gondiiinfection in humans and other animals in this region.

Toxoplasmagondii; seroprevalence; food-producing animals; Hexi Corridor; indirect hemagglutination test

Supported by the grants from the National Special Research Fund for Public Welfare (Agriculture) of China (Grant No. 200903036-06), the NBCITS, MOA (Grant No. CARS-38) and was also provided by the National Science and Technology Support Program of Gansu Province (Grant No. 1504NKCA054-6)

Toxoplasmagondiiis an obligate intracellular apicomplexan parasite that can cause severe and life-threatening diseases in humans and animals[1]. Nearly one third of the global human population has been reported withT.gondiiinfection, which is perhaps the most prevalent parasitic infection in humans all over the world[2-3].T.gondiiinfection in humans often manifests as asymptomatic diseases[3], but primary infection in pregnant women can result in abnormal pregnant outcomes, including abortion, encephalitis, mental retardation and blindness in fetus[4].

In China, approximately 7.9% population has been exposed toT.gondii, and the number was increasing in these years[5]. The incidence of toxoplasmosis was closely relevant to dietary habits[3,5]; consumption of raw or undercooked meat containing tissue cysts, in particular the meat of pig and sheep, has been regarded as a major route ofT.gondiitransmission to humans[2]. The aim of the present survey was to determine the seroprevalence ofT.gondiiinfection in pigs, cattle, sheep and chickens in Hexi Corridor of China where data onT.gondiiinfection in food-producing animals are scarce.

Materials and methodsThe study area

The survey was conducted in Liangzhou, Tianzhu, Minqin and Gulang counties in Hexi Corridor, which are situated in the center of Gansu Province (32°11′-42°57′N, 92°13′-108°46′E), covering approximately 89 000 km2. Hexi Corridor is an important part of the Silk Road, which is a vital trade line connecting East Asia, Central Asia and Europe. The average altitude is about 1 300 meters and average annual temperature is 5.8 ℃-9.3 ℃. The surveyed regions belong to temperate desert climate with the characteristic of large daily temperature difference and the low annual precipitation (60 mm). Tianzhu and Minqin counties belong to Tibetan autonomous county prairie and semi-desert regions, respectively. The ecological and geographical conditions of Gulang County are similar to that in Liangzhou County which is situated in the eastern of Hexi Corridor.

Serum samples

A total of 1 112 serum samples from 428 pigs, 275 cattle, 130 sheep and 279 chickens were collected from four counties by local veterinary practitioners in 2011. Each blood sample was then centrifuged (3 000 rpm) and sera were stored at -20 ℃ until further analysis.

Serological examination

Antibodies toT.gondiiwere identified by the indirect hemagglutination test (IHAT) using a commercially available kit (Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu Province, China). The detection procedures were performed according to the manufacturer’s recommendations. Briefly, sera were added to 96-well V-bottomed polystyrene plates and diluted 4-fold up to 1: 4 096, starting at 1: 4. Antibodies titers of 1: 64 or higher were considered positive forT.gondiiantibodies. Positive and negative controls were included in each test and assayed at the same dilutions of the serum samples.

Statistical analyses

The differences in the prevalence rates ofT.gondiiamong different species and regions as well as between caged and free-range chickens were analyzed by Chi-square analysis in SAS (Statistical Analysis System, Version 8.0). The differences were considered statistically significant whenP<0.05.

Results

One hundred and thirty-three out of 1 112 (12.1%, 95% CI, 10.1-14.0) serum samples were positive forT.gondii. The seroprevalence ofT.gondiiinfection in the four kinds of animals among original areas were shown in Table 1. TheT.gondiiprevalence in chickens ranged from 2.8% in Minqin County to 7.9% in Liangzhou County, but the difference was not statistically significant (P>0.05). As shown in Table 2, the seroprevalence ofT.gondiiin caged chickens (9.8%) was statistically significant higher than that in free-range chickens (3.2%). The variation ofT.gondiiseroprevalence in pigs in different areas ranged from 15.0% (Minqin) to 31.0% (Liangzhou), and the difference was statistically significant (P<0.05). The seroprevalence ofT.gondiiin cattle was the lowest in the four animals (P<0.01), which was found lower in Minqin County (1.4%) and higher in Liangzhou County (10.5%,P>0.05). The difference ofT.gondiiseroprevalence in sheep was not statistically significant among different areas (P>0.05).

Discussion

Toxoplasmosis is one of the most common parasitic zoonoses worldwide caused byT.gondii[3,6-7]. The parasite can be transmitted through variety of routes, and consumption of raw or undercooked meat has been considered the most significantly one[3,6]. In the present study, the overallT.gondiiseroprevalence in meat animals was 12.1% (95% CI, 10.1-14.0), which is lower than that in most other countries[8-10]and most areas in China using the same method[11-13]. The different seroprevalence among areas could be resulted from the difference in temperature, climate conditions, ecological and geographical factors, the protection and management of stray cats as well as difference in the management and animal welfareT.gondiioocysts are more prone to become infectious

Tab.1Seroprevalence of Toxoplasma gondii infection in different species and regions in Hexi Corridor, China

SpeciesRegionNo.ofexaminedIHATPositive1∶641∶2561∶10241∶4096No.(%)PigsLiangzhou129248714031.0Tianzhu80125332320.2Minqin11483101215.0Gulang105114432221.0Total42855201579722.7CattleLiangzhou765300810.5Tianzhu72210034.8Minqin63100011.4Gulang64200023.1Total27510400145.1SheepLiangzhou301101310.0Tianzhu28110025.9Minqin34100013.6Gulang38101025.3Total130421186.2ChickensLiangzhou76321067.9Tianzhu71110023.1Minqin64101022.8Gulang68221057.4Total2797530155.4Totalsamples1112763119813412.1

Tab.2Seroprevalence of Toxoplasma gondii infection in chickens in Hexi Corridor, China

HostNo.ofexaminedIHATPositive1∶641∶2561∶10241∶4096No.(%)Caged187411063.2Free-range92342099.8Total2797530155.4

and survivable in warm and humid environments[3]. The low average annual temperature and dry climate in Hexi Corridor may also be an important reason for the low seroprevalence in this region.

The seroprevalence ofT.gondiiinfection in pigs, cattle, sheep and chickens was 22.7%, 5.1%, 6.2% and 5.4%, respectively. Pigs were > 5X more likely than other animals to be seropositive (OR 5.46, 95% CI 3.05-9.79), which is corresponding to the previous studies that pig is one of the most animals as per the sensitivity toT.gondii[3]. In addition to the different immunity to the parasite, feeding system also contributes to the high seroprevalence. Pigs in the surveyed area are usually bred in free-production system, where the pigs are easy to expose to the food or water contaminated withT.gondiioocysts excreted by infected cats. However, the lowT.gondiiseropositive in cattle, sheep and chickens are due to that these animals are usually raised in intensively or semi-intensively large farms. The results of the present survey coincide with the previous investigation that prevalence ofT.gondiiin animals in intensive-farm is lower than that in free-range animals[14].

In this investigation, seroprevalence ofT.gondiiinfection in cattle was 5.1%, which was lower than that in Guangdong (5.7%), Liaoning (6.0%) and Qinghai (8.3%) province, but higher than that in Yunnan province, China(1.4%)[12,15-16]. Our study showed that the serum positivity in cattle was the lowest in four meat animals (P<0.05), and none of the animal was positive above titers of 1∶256. The lower seroprevalence ofT.gondiiin cattle compared to that in pigs, sheep and chicken may result from the different feeding regime and environment, as well as the different resistance to the parasite.

Our study showed the seroprevalence ofT.gondiiin sheep was 6.2%, which is lower than that in most other countries[14,17]and many other areas in China[18]except Heilongjiang (3.0%) and Tibet (5.7%)[14,19].T.gondiiseroprevalence in sheep from Tianzhu (5.9%) was significant lower (P<0.05) than that in the same region in 1996 (28.6%)[20]. Development of sheep breed-system, management and animal welfare are likely the main reason for the reduction in seroprevalence at the surveyed area.

The total seroprevalence ofT.gondiiinfection in chickens was 5.4%, which was lower than that observed in most other countries, and in most parts of China[10,21-22]. The seroprevalence in caged chickens and free-range chickens were 3.2% and 9.8%, respectively, and the difference was statistically significant (P<0.05). Consumption of sporulated oocysts from the environment is one of important transmission routes ofT.gondiiinfection in chickens[23], the difference of seroprevalence between free-range chickens and caged chickens may be mainly caused by the opportunity to ingest oocysts ofT.gondiiexcreted by infected cats.

Liangzhou (18.3%) was found to have the highestT.gondiiseropositivity compared to other regions (P<0.05), and Minqin, the lowest. In urban region, there is usually a very high prevalence of stray cats[24], which usually eat waste food and drink untreated water withT.gondiioocysts, and those cats also have more potential contacts with livestock. Liangzhou is close to Wuwei City that the high seropositivity may be resulted from the high number of stray cats. However, Minqin belongs to semi-desert region that severely lacks water and the arid and rainless climate is deleterious for the oocysts[3].

Conclusion

The present survey firstly revealed the seroprevalence ofT.gondiiin the common food-producing animals in Hexi Corridor, which indicated the potential risk of these animals as a source ofT.gondiiinfection in humans and other animals in this region. It is necessary to carry out measures to prevent and controlT.gondiiinfection in meat animals in Gansu Province, China.

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10.3969/j.issn.1002-2694.2016.07.004

张念章，Email：nianzhang919@163.com

家畜疫病病原学国家重点实验室，甘肃省动物寄生虫病重点实验室，中国农业科学院兰州兽医研究所，兰州730046

中国西北地区肉用动物弓形虫血清学调查

王萌，叶强，张念章，张德林

目的调查中国西北河西走廊地区的猪、牛、羊和鸡等肉用动物的弓形虫血清阳性率。方法采用间接血凝的检测方法，共调查了1 112份血清样本，包括428头猪、275头牛、130只羊和279只鸡。结果共检测到弓形虫阳性血清样本134份(12.1%, 95% CI, 10.1-14.0)。其中，猪弓形虫血清阳性率(22.7%, 95% CI, 18.7-26.6)显著高于牛(5.1%, 95% CI, 2.5-7.7)、羊(6.2%, 95% CI, 2.0-10.3)和鸡(5.4%, 95% CI, 27-8.0) (P<0.05)。凉州地区的猪弓形虫血清阳性率高于其他地区，且差异有统计学意义(P<0.05)。笼养鸡的弓形虫血清阳性率明显低于放养鸡分别为3.2%和9.8%(P<0.05)。结论河西走廊地区的肉用动物的弓形虫感染率较高，增加了当地人和其他动物感染弓形虫的风险。

弓形虫；血清阳性率；肉用动物；河西走廊；间接血凝

R382.5

A

1002-2694(2016)07-0608-05

Zhang Nian-zhang, Email: nianzhang919@163.com

2016-04-22;Revision accepted:2016-05-11

国家公益性农业行业(Grant No. 200903036-06)，国家肉牛牦牛产业技术体系(Grant No. CARS-38)，甘肃省科技支撑计划 (Grant No.1504NKCA054-6)