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Seroprevalence and Risk Factors of Bluetongue Virus Infection in Tibetan Sheep and Yaks in Tibetan Plateau, China.

1. Introduction

Bluetongue virus (BTV), a member of the genus Orbivirus, family Reoviridae, is the causative agent of bluetongue (BT), an infectious, noncontagious, arthropod-borne viral disease, which can infect a wide range of wild and domestic ruminants [1]. The first case of BT in sheep in India was reported in 1964 [1]. This pathogen was firstly recorded in sheep in China in 1979 [2]. Because BTV can cause a severe hemorrhagic disease with high morbidity, it is listed as a notifiable disease by Office International des Epizootics (OIE) [1]. Transmission of BTV is mainly through biting of blood-feeding insect vectors of the genus Culicoides (Diptera: Ceratopogonidae). BTV infection in sheep and wild ruminants usually presents as symptoms of fever, nasal discharge, drooling of saliva, oral lesion, facial edema, depression, anorexia, and muscle weakness. In contrast, goats and cattle may be asymptomatic [3].

Recently, a large number of BTV surveys have been conducted worldwide. In China, research focused on sheep, goats, and cattle [4, 5]. According to the literature published in a Chinese journal, the abortion rates of yaks were 21.39% based on an investigation of 104 farms in Qinghai Province, which could be caused by BTV and other pathogens [6]. However, no such data concerning BTV in Tibetan sheep are available, and only one case of BTV infection in yak was reported in Qinghai Province [7]. Tibetan sheep (Ovis aries) and black and white yaks(Bos grunniens) are important semiwild animals in China, and they mainly live in Tibetan Plateau which has low air pressure, lower temperature, and oxygen content. The white yaks (~49,400) is a unique yak breed living only in Tianzhu Tibetan Autonomous County, Gansu Province, northwestern China. More importantly, Tibetan sheep and black and white yaks have become the most important income source for local Tibetans. Therefore, seroprevalence of BTV infection in Tibetan sheep and black and white yaks in Tibetan Plateau, China, was conducted in this study.

2. Materials and Methods

2.1. Study Area. The study was conducted in two provinces in western China, namely, Gansu (32[degrees]31"-42[degrees]57"N, 92[degrees]13"-108[degrees]46"E) and Tibet (26[degrees]50"-36[degrees]53"N, 78[degrees]25"-99[degrees]06"E), the Tibetan Plateau, with an average elevation of 4000 metres (Figure 1). These regions have plateau continental climate, with short summer and long winter, and the average annual temperature is only 0[degrees]C.

2.2. Sample Collection. This study was approved by the Animal Ethics Committee of Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences. A total of 3771 blood samples from 2187 Tibetan sheep (962 from Tianzhu with the elevation above 2,000 metres, 182 from Luqu with an average elevation of 3,500 metres, 588 from Maqu with an average elevation of 3,700 metres, and 455 from Nyingchi with an average elevation of 3,000 metres) and 1584 yaks (974 from Tianzhu, 146 from Luqu, and 464 from Maqu) were randomly collected between April 2013 and March 2014. All the blood samples were transported directly to the laboratory in Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu Province, China. Serum was obtained through centrifugation at 1000g for 5 min. The serum was separated and stored at -20[degrees]C until analysis. Information about breed, geographic origin, gender, age, and season was obtained from local farmers and is listed in Table 1.

2.3. Serological Assay. Serum samples were examined using a commercially available c-ELISA kit (Veterinary Medical Research and Development (VMRD) Inc., Pullman, Washington, USA) to screen for BTV-specific IgG antibodies following the manufacturer's instructions [8]. The samples were considered positive when the optical density is less than or equal to 50% of the mean of the negative controls. Then the serum samples with positive or doubtful results were retested.

2.4. Data Analysis. The variation in seroprevalence of BTV-infected Tibetan Sheep and Yaks of different variables including breed, geographic origin, gender, age, and season was analyzed by [chi square] test using SAS version 9.1 (SAS Institute Inc., USA). P value < 0.05 was considered as statistically significant. Odds ratios (ORs) and their 95% confidence intervals (95% CIs) were also calculated.

3. Results

Six hundred and fifty-four (17.3%) out of 3771 serum samples were seropositive for BTV infection using an indirect ELISA test. The seroprevalence ranged from a minimum of 12.6% among the white yaks to a maximum of 20.3% among the Tibetan sheep. In the Tibetan sheep group, the seroprevalence of BTV in Luqu, Maqu, Tianzhu, and Nyingchi was 20.3%, 20.8%, 20.5%, and 19.1%, respectively, and the detailed information about each group is shown in Table 1. In the yak group, BTV seroprevalence was 12.6%, 15.5%, and 11.0% in Tianzhu, Maqu, and Luqu counties, respectively, and the detailed information about each group is shown in Table 1.

According to conditional forward stepwise logistic regression, a significant difference was found between Tibetan sheep and yak groups (P < 0.05), for which the OR was 1.653 (95% CI 1.383-1.976) (Table 2). For the Tibetan sheep group, logistic regression analysis has shown that the season, gender, age, and region were not the significant risk factors (P > 0.05). For the yak group, logistic regression analysis showed that only season was significantly associated with BTV infection (P < 0.05) (Table 2).

4. Discussion

In the present study, the overall BTV seroprevalence in the examined Tibetan sheep and yaks was 17.3%. This rate is higher than the 3.53% reported in yaks in Qinghai Province, China [7], and 9.3% among the domestic ruminants in Northern Kerala, India [3]. However, it is lower than the 27.9% prevalence reported in small ruminants in Nepal [2], 33.13% in sheep and goat in South Bengal [9], 43.68% in ruminants in Jharkhand, India [10], 45.20% among domestic ruminants in the highlands of Nepal [11], and 96.7% in buffaloes and cattle in selected provinces in Lao People's Democratic Republic [12]. Many factors, including the diagnostic methods, climatic conditions, geographical conditions, species/breeds, sample sizes, and sanitation, may contribute to such differences.

In the present survey, Tibetan sheep showed a higher BTV seroprevalence than yaks, and the difference was statistically significant (P < 0.05). This result is consistent with a previous study which demonstrated that sheep are more susceptible to BTV [3]. It is well known that Culicoides midges are the most important transmitting vector for BTV. Moreover, the Culicoides midges are seasonal; they began to be active in spring and are most active in summer in these regions [13]. This seasonal exposure fits with the seroprevalence data in yaks in this study. Hence, the seasons were undoubtedly the risk factor for BTV infection in yaks.

The present study has shown that seasons are highly related to BTV infection in yaks (P < 0.05). Yaks had a 1.87 times higher risk for infection with BTV in summer compared to winter (OR = 1.87, 95% CI = 1.17-3.00) and a 1.85 times higher risk for infection with BTV in autumn compared to winter (OR = 1.85, 95% CI = 1.18-2.91), but it was not different significantly between spring and winter using multivariable analysis (Table 2). Such difference may be due to the fact that the Tibetan sheep and yaks were slaughtered during September and November every year, and the unhealthy and adult animals would be slaughtered first. Hence, the seroprevalence was lower in winter than in other seasons. However, the Culicoides midges would breed when the winter is passed, and they could spread the virus again. Although the season was not considered as the risk factor for Tibetan sheep, the seroprevalence in summer was higher than other seasons. These findings suggest that seasons should be considered when carrying out control programs in the investigation areas.

In the present investigation, no significant difference in BTV seroprevalence was observed among Tibetan sheep and yaks of different ages. This might be because these animals stayed in the same location.

In summary, the present study revealed that BTV infection is widespread in Tibetan sheep (20.3%) and yaks (13.3%) in Gansu and Tibet, western China. This is also the first report of BTV seroprevalence and risk factors in Tibetan sheep in China. The logistic regression analysis showed that the species was the risk factor concerning BTV infection. Season is considered as the risk factor of BTV infection in yaks. Hence, we should pay more attention to controlling Culicoides midges in warm seasons, especially in summer and autumn. These data provide baseline information for the control of BTV infection in Tibetan sheep and yaks.

Competing Interests

The authors declare that there is no conflict of interests regarding the publication of this paper.


This work was supported by the "Special Fund for Agro-Scientific Research in the Public Interest" (Grant no. 2013-03037).


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Jian-Gang Ma, (1,2) Xiao-Xuan Zhang, (1,2) Wen-Bin Zheng, (1,2) Ying-Tian Xu, (3) Xing-Quan Zhu, (1,4) Gui-Xue Hu, (2) and Dong-Hui Zhou (1)

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

(2) College of Animal Science and Technology, Jilin Agricultural University, Changchun, Jilin 130118, China

(3) College of Agriculture, Yanbian University, Yanji, Jilin 133002, China

(4) Jiangsu Co-Innovation Center for the Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University College of Veterinary Medicine, Yangzhou, Jiangsu 225009, China

Correspondence should be addressed to Gui-Xue Hu; and Dong-Hui Zhou;

Received 22 October 2016; Revised 23 January 2017; Accepted 21 February 2017; Published 23 April 2017

Academic Editor: Heather Simpson

Caption: Figure 1: A map of China showing the geographical regions in Tibet and Gansu Provinces where farmed Tibetan sheep and yaks were sampled.
Table 1: Seroprevalence and risk factors of bluetongue virus
(BTV) infection in Tibetan sheep and yaks in Tibetan Plateau,
western China, by enzyme-linked immunosorbent assay (ELISA).

                             Tibetan sheep

                    Number    Number
Variable            Tested   Positive    %     P value

Age group (years)
  1 or less          447        82      18.3
  1-2                413        90      21.8   0.6418
  2-4                1116      229      20.5
  >4                 211        42      19.9
  Male               638       140      21.9   0.2076
  Female             1549      303      19.6
  Tianzhu            962       197      20.5
  Luqu               182        37      20.3   0.9230
  Maqu               588       122      20.8
  Nyingchi           455        87      19.1
  Spring             480       103      21.5
  Summer             398        93      23.4
  Autumn             479        98      20.5   0.1708
  Winter             375        62      16.5
  No information     455        87      19.1
  White yak           --        --       --    --
  Black yak           --        --       --    --
  Total              2187      443      20.3   --


                    Number    Number
Variable            Tested   Positive    %     P value

Age group (years)
  1 or less          286        38      13.3
  1-2                292        38      13.0   0.1148
  2-4                521        83      15.9
  >4                 485        52      10.7
  Male               471        70      14.9   0.2402
  Female             1113      141      12.7
  Tianzhu            974       123      12.6
  Luqu               146        16      11.0   0.2178
  Maqu               464        72      15.5
  Spring             428        54      12.6
  Summer             354        55      15.5
  Autumn             467        72      15.4   0.0293
  Winter             335        30      9.0
  No information      --        --       --
  White yak          974       123      12.6   0.3055
  Black yak          610        88      14.4
  Total              1584      211      13.3     --

Table 2: Odds ratios of the risk factors for bluetongue virus (BTV)
seroprevalence in Tibetan sheep and yaks (n = 3771).

Factor          Group       Prevalence (%)      OR         95% CI

Breed            Yak             13.3        Reference
            Tibetan sheep        20.3          1.653     1.383-1.976

Season         Winter            9.0         Reference
(in yaks)      Spring            12.6          1.468     0.916-2.352
               Summer            15.5          1.870     1.166-3.000
               Autumn            15.4          1.853     1.180-2.910

                                     P value

                            Univariable   Multivariable
Factor          Group        analysis       analysis

Breed            Yak                        Reference
            Tibetan sheep     <0.0001        <0.0001

Season         Winter                       Reference
(in yaks)      Spring         0.0293         0.1088
               Summer                        0.0086
               Autumn                        0.0067
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Article Details
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Title Annotation:Research Article
Author:Ma, Jian-Gang; Zhang, Xiao-Xuan; Zheng, Wen-Bin; Xu, Ying-Tian; Zhu, Xing-Quan; Hu, Gui-Xue; Zhou, D
Publication:BioMed Research International
Article Type:Report
Geographic Code:9CHIN
Date:Jan 1, 2017
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