Skip to main content
PMC home page
Infectious Diseases of Poverty logoLink to Infectious Diseases of Poverty
. 2022 May 26;11:59. doi: 10.1186/s40249-022-00987-9

Assessment of echinococcosis control in Tibet Autonomous Region, China

Liying Wang 1,2,3,4,✉,#, Quzhen Gongsang 2,#, Huasheng Pang 2, Min Qin 1, Ying Wang 1, Jingzhong Li 2,✉, Roger Frutos 3, Laurent Gavotte 4
PMCID: PMC9137097  PMID: 35619124

Abstract

Background

In China the highest prevalence of echinococcosis is in Tibet Autonomous Region (TAR). The government has issued documents and implemented comprehensive prevention and control measures focusing on controlling the source of infection of echinococcosis. It was very important to understand the implementation and effect of infectious source control measures. The purpose of this study was to examine the implementation of measures to control infectious source (domestic and stray dogs) in TAR and to assess their effectiveness.

Methods

We collected data on domestic dog registration and deworming and stray dog sheltering in 74 counties/districts in the TAR from 2017 to 2019. Fecal samples from domestic dogs were collected from randomly selected towns to determine Echinococcus infection in dogs using coproantigen ELISA. We analyzed the data to compare the canine rate of infection between 2016 and 2019. The data analysis was performed by SPSS statistical to compare dog infection rate in 2016 and 2019 by chi-square test, and ArcGIS was used for mapping.

Results

From 2017 to 2019, 84 stray dog shelters were built in TAR, and accumulatively 446,660 stray or infected dogs were arrested, sheltered, or disposed of. The number of domestic dogs went downward, with an increased registration management rate of 78.4% (2017), 88.8% (2018), and 99.0% (2019). Dogs were dewormed 5 times in 2017, 12 times in 2018, and 12 times in 2019. The dog infection rate was 1.7% (252/14,584) in 2019, significantly lower than 7.3% (552/7564) from the survey of echinococcosis prevalence in Tibet in 2016 (P < 0.05).

Conclusion

Between 2017 and 2019, the number of stray dogs and infection rate of Echinococcus spp. in domestic dogs decreased significantly, indicating that dogs were effectively controlled as a source of infection in TAR and reflecting a significant decrease in the risk of echinococcosis transmission.

Graphical Abstract

graphic file with name 40249_2022_987_Figa_HTML.jpg

Keywords: Echinococcosis, Hydatidosis, Source of infection, Control measure, Effect assessment, China

Background

Echinococcosis, which is a zoonotic parasitic disease, caused by the larvae of Echinococcus. In China, two major types of echinococcosis are prevalent: cystic echinococcosis (CE) which is caused by the larvae of E. granulosus and alveolar echinococcosis (AE) which is caused by the larvae of E. multilocularis [1]. It is estimated that there are at least 188,000 new CE cases worldwide every year, resulting in 1,097,000 disability-adjusted life years (DALYs), and China accounts for 40% of the world [2]. The disease burden of AE is 666,434 DALYs per year in the world, and 91% of cases and 95% of DALYs occur in China every year [3]. Echinococcosis is highly endemic in western and northern China. Tibet Autonomous Region (TAR), also simply referred to as Tibet, located in the Qinghai-Tibet Plateau, which is one of the most infected regions. A national survey of echinococcosis, which conducted between 2012 and 2016, showed that echinococcosis prevalence in humans was 1.66% and estimated that nearly 50,000 patients experienced echinococcosis [4]. In the survey, the prevalence of echinococcosis was found to be highest in TAR [4]. Echinococcosis prevailed in all 74 counties of TAR. In animals, the disease prevalence was 7.30 and 13.21%, in dogs and livestock respectively [5]. As definitive hosts, dogs may significantly impact transmission and dissemination of E. granulosus [6]. Dogs, together with small mammals, are also involved in the transmission of E. multilocularis [7]. When dogs prey on small mammals, they can carry E. multilocularis into a synanthropic transmission ecosystem [8]. In addition, domestic dogs are identified as the most important definitive host of both E. granulosus and E. multilocularis with the highest risk of transmitting CE and AE to humans due to their ability to wander freely in pastoral areas and prey on slaughtered livestock [9]. Few people pass scores from echinococcosis prevention questionnaire [10]. These factors make TAR the region with the most severe prevalence worldwide. Echinococcosis has become a major public health issue that seriously restricts economic development, ethnic unity and social stability of TAR, and seriously endangers health and safety of people. It is also a major obstacle to the development of TAR [11].

In March 2017, in response to the severe echinococcosis situation, the General Office of the People’s Government of the Tibet Autonomous Region issued the “Work Plan for Comprehensive Control of Echinococcosis in the Tibet Autonomous Region (2017–2020) (ZZBF [2017] No. 29)”, hereinafter referred to as “the Plan”, to speed up and strengthen echinococcosis control in TAR. The Plan requires complete screening on all populations and implementation of various control measures (focusing on infection source control). This work was conducted in order to assess the implementation of measures to control infectious source (domestic dogs and stray dogs) for echinococcosis in TAR. Our findings will provide reference for the implementation of further prevention and control measures.

Methods

Study area

TAR is located in the southwest of Qinghai Tibet Plateau, with an average altitude of more than 4000 m. TAR has 74 endemic counties (districts) in 6 prefecture-level cities (Lhasa City, Changdu city, Shannan city, Shigatse city, Naqu city, Linzhi city) and one prefecture (Ali Prefecture). Among these counties 47counties are endemic counties for mixed CE and AE, and all the 74 counties are endemic counties for CE.

Source of data

The Center for Disease Control and Prevention of the Tibet Autonomous Region (TAR CDC), guided by the National Institute of Parasitic Diseases (NIPD), Chinese Center for Disease Control and Prevention (China CDC), prepared a questionnaire for identifying the infection sources − dogs from 2017 to 2019. Data on dog infection rates of Echinococcus spp. were collected from endemic counties in 2019 in conjunction with the Annual Task of Central Government's Transfer Payment Project for Echinococcosis Control.

Implementation of control measures

The TAR government made the prevention and control of echinococcosis a priority and thus incorporated echinococcosis control into government's performance evaluation. Leadership groups for echinococcosis control have been established at provincial, regional, and county levels. Comprehensive measures were implemented to prevent and control echinococcosis in all 74 endemic counties (districts) in six prefecture-level cities and one prefecture in TAR. In endemic counties, relevant departments actively functioned according to requirements of prevention and control programs, implemented comprehensive control strategies and measures focusing on infection source control and promoted dog registration and management. To ensure effective dog management, the public security bureau of each county of each city (prefecture) established a leadership group for dog management according to specific requirements from the Opinions on Regulating Dog Management in TAR and the Plan. Based on dog statistics, township (town) police stations, convenient police posts, and village resident policemen implemented dog management requirements, such as restriction, tethering and permit application, into each household in each village. The public security department collaborated with agriculture and animal husbandry department to collect and record basic dog information. Registered dog owners and dogs were photographed and put on record for dynamic and standardized management. A proactive campaign was launched to educate farmers and herders about the importance of limiting the number of dogs and tethering dogs. Currently, all dogs in cities (prefectures) are tethered. For many stray dogs, the measures focused on territorial centralized accommodation and management and disposal of infected dogs. The situation in the Linzhi Prefecture has previously been studied by Wang et al. [12] and data were added to the results of this study.

Dog registration and management

According to the “Opinions on Regulating Dog Management in TAR”, each household should have no more than two dogs, and these dogs should be tethered. Shepherd dogs should also be tethered immediately upon arrival at the temporary settlement, and dog feces should be buried. Dog deworming registration cards were established to register all domestic (herd) dogs in endemic areas and register ownerless dogs by village. Contents of the registration were: name of the head of household, dog’s sex, age, fur color, and date of each deworming. These tasks were completed by local public security departments and agricultural departments.

Dog deworming

Efforts have been made to ensure that each dog is dewormed monthly following relevant requirements from the Technical Plan for Echinococcosis Control (2008 Edition) issued by the Central Government. The local agriculture and husbandry department sent down deworming drugs and provided instructions on conducting operations. Dog owners embedded praziquantel into food such as zanba to feed dogs and recorded it on a logbook every month. Praziquantel (specification: 0.2 g/tablet) was used to deworm all dogs, at 1 to 2 tablets/dose/dog (2 tablets for dogs > 15 kg). The dose was delivered once a month. Dogs were fed with food-coated drugs. The drug was ensured to be swallowed and the treatment was recorded on a dog deworming registration card.

Disposal of dog feces after deworming

Dog feces were collected and disposed (buried in-depth or incinerated) within five days after deworming to prevent Echinococcus eggs from contaminating the environment.

Reduction of dog populations

Various measures were taken to control the number of dogs, stray dogs were accommodated where conditions allow, and infected dogs were hunted down. The public security bureau of each county (district), under unified instructions of comprehensive echinococcosis control leadership group at each level, invited third-party capture teams to cooperate with public security and armed police to make joint efforts in stray dog capture and sheltering. Farmers and herders were informed about the restrictions on dog breeding. Number of domestic and stray dogs collected by local veterinarian.

Monitoring of dog infection

One administrative village in each endemic township was randomly selected each year. According to dog deworming registration cards, 20 households in the village were identified using a systematic random sampling method. One sample of feces from each household was collected to obtain 20 samples. Whenever the number of samples was less than 20, samples from a nearby village were used to supplement up to 20. The collected samples were frozen a – 80 °C for at least 72 h and sandwich ELISA (Dog Echinococcus coproantigens ELISA kit, Combined, Shenzhen, China) was used to detect infection states of dogs.

Data collection and analysis

Data on dog registration, management and deworming, and stray dog accommodation were collected through retrospective surveys and field study. The results of the 2016 TAR echinococcosis prevalence survey were used as a baseline data for dog infection rate. The dog infection rate in 2019 was based on data from the Central Government's Transfer Payment Project for Echinococcosis Control. The collected data were firstly systematized and checked before being entered and analyzed using SPSS 20.0 (IBM, Armonk, USA). A chi-square test was used to compare the dog infection rate in two cross-sections. Geographic information maps were mapped using ArcGIS version 10.1 (ESRI, Redlands, USA).

Results

Control measures for domestic dogs

Registration and management of domestic dogs

The registration rate of domestic dogs increased annually from 78.4% in 2017 to 88.8% in 2018 and 99.0% in 2019 (Table 1 and Fig. 1). Currently, all domestic dogs in each region have been registered for management and are tethered. The number of domestic dogs decreased from 184,564 to 175,561 between 2017 and 2018, and then to 171,754 in 2019 (Table 1). The 2018 surveys of domestic dogs revealed that TAR had 670,838 households and an average of 1 dog for four households.

Table 1.

Registration and management of domestic dogs by prefecture/city in Tibet Autonomous Region during 2017–2019

Prefecture/City 2017 2018 2019
Endemic county Total domestic dogs Registered domestic dogs Registration rate of domestic dogs (%) Total domestic dogs Registered domestic dogs Registration rate of domestic dogs (%) Total domestic dogs Registered domestic dogs Registration rate of domestic dogs (%)
Lhasa 24,744 24,743 100.0 23,807 23,807 100.0 26,883 26,883 100.0
Chengguan 7885 7885 100.0 10,091 10,091 100.0 11,734 11,734 100.0
Linzhou 3158 3158 100.0 1327 1327 100.0 4485 4485 100.0
Dangxiong 2193 2193 100.0 3827 3827 100.0 1186 1186 100.0
Nimu 1776 1776 100.0 1625 1625 100.0 1535 1535 100.0
Qushui 3130 3130 100.0 1650 1650 100.0 2895 2895 100.0
Duilong Deqing 1205 1205 100.0 661 661 100.0 716 716 100.0
Dazi 3892 3892 100.0 3458 3458 100.0 3219 3219 100.0
Mozhu Gongka 1505 1504 100.0 1168 1168 100.0 1113 1113 100.0
Changdu 28,033 20,208 72.1 28,033 23,244 82.9 28,033 27,962 99.8
Karuo 3985 2897 72.7 3985 3285 82.4 3985 3892 97.7
Jiangda 5085 3645 71.7 5085 4146 81.5 5085 4984 98.0
Gongjue 956 756 79.1 956 817 85.5 956 949 99.3
Leiwuqi 846 609 72.0 846 696 82.3 846 829 98.0
Dingqing 3528 2563 72.6 3528 2846 80.7 3528 3877 100.0
Chaya 2236 1617 72.3 2236 1887 84.4 2236 2237 100.0
Basu 2220 1598 72.0 2220 1846 83.2 2220 2152 96.9
Zuogong 1800 1309 72.7 1800 1522 84.6 1800 1743 96.8
Mangkang 4150 2914 70.2 4150 3527 85.0 4150 4088 98.5
Luolong 1129 799 70.8 1129 946 83.8 1129 1135 100.0
Bianba 2098 1501 71.5 2098 1726 82.3 2098 2076 99.0
Shannan 12,434 3858 31.0 12,787 9844 77.0 12,988 12,988 100.0
Naidong 3700 988 26.7 3081 2,467 80.1 3081 3081 100.0
Zanang 1088 540 49.6 1595 990 62.1 1599 1599 100.0
Gongga 1941 344 17.7 2402 1606 66.9 2475 2475 100.0
Sangri 401 184 45.9 543 412 75.9 557 557 100.0
Qiongjie 1120 379 33.8 548 454 82.9 548 548 100.0
Qusong 390 142 36.4 428 425 99.3 428 428 100.0
Cuomei 264 162 61.4 307 264 86.0 308 308 100.0
Luoza 362 354 97.8 427 419 98.1 433 433 100.0
Jiacha 1316 295 22.4 1698 1313 77.3 1713 1713 100.0
Longzi 538 127 23.6 593 541 91.2 680 680 100.0
Cuona 352 98 27.8 222 197 88.7 223 223 100.0
Langkazi 962 245 25.5 943 756 80.2 943 943 100.0
Shigatse 50,067 31,678 63.3 42,703 31,678 74.2 41,074 39,495 96.2
Sangzhuzi 8898 3123 35.1 4542 3123 68.8 4268 3548 100.0
Nanmulin 3373 1127 33.4 3558 3558 100.0 3360 3360 100.0
Jiangzi 3473 499 14.4 4299 499 11.6 4299 4299 100.0
Dingri 1957 931 47.6 6662 6662 100.0 6662 6662 100.0
Sajia 3181 1327 41.7 3450 3450 100.0 3450 3450 100.0
Lazi 1673 100 6.0 1747 1747 100.0 1747 1747 100.0
Angren 1701 1008 59.3 1701 1008 59.3 1008 1008 100.0
Xietongmen 1384 617 44.6 1617 1617 100.0 1617 1617 100.0
Bailang 3038 1914 63.0 2823 1914 67.8 2823 2225 100.0
Renbu 1339 1136 84.8 1472 1136 77.2 1393 1236 100.0
Kangma 1936 1708 88.2 1708 1708 100.0 1708 1708 100.0
Dingjie 1648 284 17.2 1116 284 25.5 1239 1239 100.0
Zhongba 6924 1,450 20.9 1537 1,537 100.0 1537 1537 100.0
Yadong 655 487 74.4 483 487 100.0 495 495 98.0
Jilong 1071 488 45.6 670 448 66.9 573 481 100.0
Nielamu 5979 1080 18.1 3400 1,080 31.8 3400 3388 100.0
Saga 1248 750 60.1 1248 750 60.1 825 825 100.0
Gangba 589 313 53.1 670 670 100.0 670 670 100.0
Naqu 43,629 42,767 98.0 43,364 43,183 99.6 40,590 40,590 100.0
Naqu County 11,064 11,064 100.0 6707 6707 100.0 6157 6157 100.0
Jiali 1032 1032 100.0 3101 3101 100.0 2962 2962 100.0
Biru 5754 4892 85.0 6592 6592 100.0 6261 6261 100.0
Nierong 4377 4377 100.0 4838 4838 100.0 4850 4850 100.0
Anduo 2480 2480 100.0 2493 2493 100.0 2507 2507 100.0
Shenza 1027 1027 100.0 1054 873 82.8 224 224 100.0
Suoxian 3451 3451 100.0 405 3405 100.0 3410 3410 100.0
Bange 2829 2829 100.0 2875 2875 100.0 1787 1787 100.0
Baqing 7384 7384 100.0 6360 6360 100.0 6567 6567 100.0
Nima 3660 3660 100.0 4616 4616 100.0 4634 4634 100.0
Shuanghu 571 571 100.0 1323 1323 100.0 1231 1231 100.0
Ali 8250 8250 100.0 8355 8355 100.0 9523 9523 100.0
Pulan 330 330 100.0 117 117 100.0 1,681 1681 100.0
Zhada 323 323 100.0 234 234 100.0 278 278 100.0
Gaer 213 213 100.0 1323 1323 100.0 1056 1056 100.0
Ritu 1438 1438 100.0 1206 1206 100.0 953 953 100.0
Geji 3386 3386 100.0 3363 3363 100.0 2485 2485 100.0
Gaize 1740 1740 100.0 1495 1495 100.0 1596 1596 100.0
Cuoqin 820 820 100.0 617 617 100.0 1474 1474 100.0
Linzhi [12] 17,407 13,216 75.9 16,512 15,766 95.5 12,663 12,491 98.6
Linzhi County 3759 2722 72.4 2820 2679 95.0 2669 2643 99.0
Gongbu Jiangda 3759 3759 100.0 3310 3310 100.0 2305 2259 98.0
Milin 3287 1446 44.0 2651 2545 96.0 2168 2147 99.0
Motuo 1193 453 38.0 1054 1011 95.9 401 397 99.0
Bomi 2863 2863 100.0 2771 2660 96.0 2661 26,08 98.0
Chayu 1912 1339 70.0 2126 1781 83.8 2048 2028 99.0
Langxian 634 634 100.0 1780 1780 100.0 411 409 99.5
Total 74 counties 184,564 144,720 78.4 175,561 155,877 88.8 171,754 169,932 99.0
Open in a new tab
Fig. 1.

Fig. 1

Open in a new tab

Dog populations' evolution in Tibet Autonomous Region during 2017–2019

Deworming of domestic dogs

In 2017, dogs were dewormed at an average of five times a year. In 2018 and 2019, this number was increased to 12, ensuring that every dog was dewormed monthly as required by the Plan. As by December 31, 2019, there have been more than 5.09 million deworming doses for domestic dogs in the past three years (Table 2).

Table 2.

Deworming of domestic dogs by prefecture/city in Tibet Autonomous Region during 2017–2019

Prefecture/City 2017 2018 2019
Total domestic dogs Dog deworming doses Annual average dog deworming doses Total domestic dogs Dog deworming doses Annual average dog deworming doses Total domestic dogs Dog deworming doses Annual average dog deworming doses
Lhasa 24,744 149,969 6 23,807 304,494 13 26,883 322,588 12
Changdu 28,033 118,354 4 28,033 353,743 13 28,033 331,566 12
Shannan 12,434 10,759 1 12,787 122,928 10 12,988 155,856 12
Shigatse 50,067 74,770 1 42,703 492,613 12 41,074 533,962 13
Naqu 43,629 377,711 9 43,364 498,437 11 40,590 489,901 12
Ali 8250 99,000 12 8355 100,260 12 9523 114,276 12
Linzhi [12] 17,407 67,352 4 16,512 204,375 12 12,663 171,315 14
Total 184,564 897,915 5 175,561 2,076,850 12 171,754 2,119,464 12
Open in a new tab

Control measures for stray dogs

From 2017 to 2019, 69.6%, 86.8%, and 98.1% of stray dogs were sheltered, respectively (Table 3). The sharp reduction of the number of stray dogs (Figs. 1 and 2), resulted in an overall reduction of the number of infection sources. Assessment teams reported that stray dog sheltering management made remarkable achievements, and stray dogs were rarely observed in endemic villages. No dog feces were found on the roadside or around settlements during the visits.

Table 3.

Stray dog sheltering by prefecture/city in Tibet Autonomous Region during 2017–2019

Prefecture/City 2017 2018 2019
No. of stray dogs No. of sheltered dogs No. of stray dogs at end of year Sheltering rate (%) No. of stray dogs No. of sheltered dogs No. of stray dogs at end of year Sheltering rate (%) No. of stray dogs No. of sheltered dogs No. of stray dogs at end of year Sheltering rate (%)
Lhasa 52,571 44,811 7760 85.2 30,764 27,727 3037 90.1 24,995 24,659 336 98.7
Changdu 17,200 10,706 6494 62.2 16,081 11,820 4261 73.5 16,420 16,256 164 99.0
Shannan 20,254 14,676 5578 72.5 14,324 12,004 2320 83.8 9370 8612 758 91.9
Shigatse 76,687 38,651 38,036 50.4 71,569 72,649 9617 86.6 58,822 58,040 782 98.7
Naqu 33,234 27,474 5760 82.7 22,208 20,228 1980 91.1 18,536 18,383 153 99.2
Ali 7913 6201 1712 78.4 5680 5023 657 88.4 3937 3804 133 96.6
Linzhi [12] 14,336 12,132 2204 84.6 13,067 12,063 1004 92.3 11,837 11,438 399 96.6
Total 222,195 154,651 67,544 69.6 173,693 150,817 22,876 86.8 143,917 141,192 2725 98.1
Open in a new tab

Fig. 2.

Fig. 2

Open in a new tab

Distribution of changes in the number of stray dogs in each city (prefecture) of Tibet Autonomous Region. Map approval No. GS (2022) 2437

Status of dogs as sources of infection

The assessments revealed that in 2019 the dog infection rate in TAR was 1.7% (252/14,584). At present, out of 74 endemic counties in TAR, 3 reported a dog infection rate higher than 5%, 16 reported a rate of between 1 and 5%, and 55 reported a rate of < 1%, including 32 counties with no reported positive dog feces (Table 4) (Fig. 3).

Table 4.

Comparison of domestic dog infections in prefecture/cities of Tibet Autonomous Region in 2016 vs 2019

Prefecture/City 2016 2019 Test result
No. of dog feces tested No. of dog feces positive Positive rate of dog feces (%) [95% CI] No. of dog feces tested No. of dog feces positive Positive rate of dog feces (%) [95% CI] χ2 P Result
Lhasa 1047 66 6.3 [4.8, 7.8] 2,620 0 0.0 168.19  < 0.01 ↓
Changdu 1358 78 5.74 [4.5, 7.0] 1,669 56 3.4 [2.5, 4.2] 10.10  < 0.01 ↓
Shannan 1046 107 10.2 [8.4, 12.1] 1,741 0 0.0 185.21  < 0.01 ↓
Shigatse 1945 94 4.8 [3.9, 5.8] 1,803 41 2.3 [1.6, 3.0] 17.65  < 0.01 ↓
Naqu 1127 128 11.4 [9.5, 13.2] 2,941 67 2.3 [1.7, 2.8] 147.18  < 0.01 ↓
Ali 423 34 8.04 [5.4, 10.6] 1,095 11 1.0 [0.4, 1.6] 52.47  < 0.01 ↓
Linzhi [12] 618 45 7.3 [5.2, 9.3] 2,715 77 2.8 [2.2, 3.5] 28.21  < 0.01 ↓
Total 7564 552 7.3 [6.7, 7.9] 14,584 252 1.7 [1.5, 1.9] 441.68  < 0.01 ↓
Open in a new tab

This table represents changes in the infection rate of domestic dogs. Due to the large number of stray dogs sheltered and effective management in endemic counties, the number of infection sources has decreased significantly, and the weighted dog infection rate, which represents the prevalence of endemic counties, has been significantly reduced. CI Confidence interval

Fig. 3.

Fig. 3

Open in a new tab

Dog infection distribution of comprehensive control effect of echinococcosis in Tibet Autonomous Region in 2019. Map approval No. GS (2022) 2437

Assessment of the effect of infection source control

In 2016, 43 Class I counties were identified with a dog infection rate ≥ 5% (Fig. 4), 26 Class II counties with a dog infection rate of < 5% and ≥ 1%, and 5 Class III counties with a dog infection rate of < 1%. In 2019, the numbers of Class I, II, and III counties were 3, 16, and 55, respectively (Fig. 4).

Fig. 4.

Fig. 4

Open in a new tab

Distribution of dog infections in echinococcosis prevalence surveys in Tibet Autonomous Region in 2016. Map approval No. GS (2022) 2437

The dog infection rate was 1.7% (252/14,584) in 2019, significantly lower (P < 0.05) than in 2016 when it was 7.3%, representing a 76.3% decrease. County-level dog infection rates ranged from 41.3% in 2016 (Baqing County) to 6.2% in 2019. The dog infection rate of the seven cities or prefectures under the jurisdiction of TAR all declined significantly (P < 0.05), as shown in Table 4. Given the important role of decreased infection sources in lowering the risk of local transmission, the dog infection rate in 2019 was weighed and compared to that of 2016. The number of dogs were different in the same endemic county in 2016 and 2019. Therefore, the positive rates of dog were weighted adjusted based on the number of domestic dogs in 2016 and 2019. The results are presented in Table 5 and Fig. 5. The weighted overall infection rate in 2019 was 0.7%, with a decrease of 90.0% compared to that of 2016 (Fig. 5). Rates were compared for each endemic county, and each county experienced a reduction in the rate to varying degrees. The decrease was significant in 32 counties (P < 0.05) and insignificant in 40 counties (P > 0.05). The dog infection rate has always been null in two counties, Zanda County of Ali Prefecture and Lhozhag County of Shannan City.

Table 5.

Comparison of dog infections in 74 endemic counties of Tibet Autonomous Region in 2016 vs 2019

Region/Prefecture/League/City Endemic county 2016 2019 Weighted adjusted positive rate Test results of two rates
Total dogs No. of dog feces tested No. of dog feces positive Positive rate of dog feces (%) [95% CI] Total dogs No. of dog feces tested No. of dog feces positive Positive rate of dog feces (%) [95% CI]
Lhasa Chengguan 25,186 324 29 9.0 [5.8, 12.1] 11,754 1060 0 0.0 0.0 P < 0.05
Linzhou 10,664 159 15 9.4 [4.8, 14.0] 4536 100 0 0.0 0.0 P < 0.05
Dangxiong 6209 80 6 7.5 [1.6, 13.4] 1239 500 0 0.0 0.0 P < 0.05
Nimu 4562 80 4 5.0 [0.1, 9.9] 1568 80 0 0.0 0.0 P > 0.05
Qushui 8146 80 2 2.5 [− 1.0, 6.0] 2922 200 0 0.0 0.0 P > 0.05
Duilong Deqing 8221 163 1 0.6 [− 0.6, 1.8] 757 100 0 0.0 0.0 P > 0.05
Dazi 6738 80 3 3.8 [− 0.5, 8.0] 3258 300 0 0.0 0.0 P > 0.05
Mozhu Gongka 7589 81 6 7.4 [1.6, 13.2] 1185 280 0 0.0 0.0 P < 0.05
Changdu Karuo 5928 319 5 1.6 [0.2, 2.9] 4008 120 0 0.0 0.0 P > 0.05
Jiangdaa 7468 160 8 5.0 [1.6, 8.4] 5105 108 10 9.3 [3.7, 14.8] 6.3 P > 0.05
Gongjue 1910 80 2 2.5 [− 1.0, 6.0] 972 100 3 3.0 [− 0.4, 6.4] 1.5 P > 0.05
Leiwuqia 1406 80 7 8.8 [2.4, 15.1] 856 100 4 4.0 [0.1, 7.9] 2.4 P > 0.05
Dingqinga 3972 160 11 6.9 [2.9, 10.8] 3,548 280 18 6.4 [3.5, 9.3] 5.7 P > 0.05
Chaya 4575 80 2 2.5 [− 1.0,6.0] 2246 100 7 7.0 [1.9, 12.1] 3.4 P > 0.05
Basu 4484 79 6 7.6 [1.6, 13.6] 2230 280 3 1.1 [− 0.1, 2.3] 0.5 P < 0.05
Zuogonga 3476 80 20 25.0 [15.3, 34.7] 1820 101 4 4.0 [0.1, 7.8] 2.1 P < 0.05
Mangkang 5654 160 15 9.4 [4.8, 13.9] 4168 280 5 1.8 [0.2, 3.3] 1.3 P < 0.05
Luolong 3997 80 0 0.0 1139 100 2 2.0 [− 0.8, 4.8] 0.6 P > 0.05
Bianba 2363 80 2 2.5 [− 1.0, 6.0] 2105 100 0 0.0 0.0 P > 0.05
Shannan Naidong 7195 140 9 6.4 [2.3, 10.5] 3149 101 0 0.0 0.0 P < 0.05
Zanang 3034 80 3 3.8 [− 0.5, 8.0] 1641 100 0 0.0 0.0 P > 0.05
Gongga 4422 80 3 3.8 [− 0.5, 8.0] 2548 100 0 0.0 0.0 P > 0.05
Sangri 1457 72 3 4.2 [− 0.6, 8.9] 590 100 0 0.0 0.0 P > 0.05
Qiongjie 2666 80 4 5.0 [0.1, 9.9] 589 100 0 0.0 0.0 P > 0.05
Qusong 876 80 1 1.3 [− 1.2, 3.7] 476 280 0 0.0 0.0 P > 0.05
Cuomei 1240 114 43 37.7 [28.7, 46.8] 365 100 0 0.0 0.0 P < 0.05
Luozab 2226 80 0 0.0 547 100 0 0.0 0.0 /
Jiacha 2534 80 2 2.5 [− 1.0, 6.0] 1783 280 0 0.0 0.0 P > 0.05
Longzi 2646 80 6 7.5 [1.6, 13.4] 763 280 0 0.0 0.0 P < 0.05
Cuona 902 80 11 13.8 [6.0, 21.5] 259 100 0 0.0 0.0 P < 0.05
Langkazi 3490 80 22 27.5 [17.5, 37.5] 1036 100 0 0.0 0.0 P < 0.05
Shigatse Sangzhuzi 20,679 320 8 2.5 [0.8, 4.2] 4308 100 0 0.0 0.0 P > 0.05
Nanmulin 12,132 160 13 8.1 [3.8, 12.4] 415 100 0 0.0 0.0 P < 0.05
Jiangzi 11,312 160 8 5.0 [1.6, 8.4] 4334 100 0 0.0 0.0 P > 0.05
Dingri 6081 154 4 2.6 [0.1, 5.1] 6706 101 1 1.0 [− 1.0, 3.0] 1.1 P > 0.05
Sajia 4445 80 3 3.8 [− 0.5, 8.0] 3489 100 0 0.0 0.0 P > 0.05
Lazi 4805 80 5 6.3 [0.8, 11.7] 1802 101 8 7.9 [2.6, 13.3] 3.0 P > 0.05
Angren 11,470 160 6 3.8 [0.8, 6.7] 1053 100 3 3.0 [− 0.4, 6.4] 0.3 P > 0.05
Xietongmen 7168 80 3 3.8 [− 0.5, 8.0] 1662 100 7 7.0 [1.9, 12.1] 1.6 P > 0.05
Bailang 5954 80 5 6.3 [0.8, 11.7] 2868 101 2 2.0 [0.8, 4.7] 1.0 P > 0.05
Renbu 2154 83 1 1.2 [− 1.2, 3.6] 1443 100 1 1.0 [− 1.0, 3.0] 0.7 P > 0.05
Kangma 5060 80 6 7.5 [1.6, 13.4] 1748 100 0 0.0 0.0 P < 0.05
Dingjie 3327 80 2 2.5 [− 1.0, 6.0] 1279 100 2 2.0 [− 0.8, 4.8] 0.8 P > 0.05
Zhongba 8597 80 8 10.0 [3.3, 16.7] 1587 100 3 3.0 [− 0.4, 6.4] 0.6 P < 0.05
Yadong 2551 28 5 17.9 [2.7, 33.0] 530 100 8 8.0 [2.6, 13.4] 1.7 P < 0.05
Jilong 2836 80 6 7.5 [1.6, 13.4] 613 100 1 1.0 [− 1.0, 3.0] 0.2 P < 0.05
Nielamu 11,162 80 5 6.3 [0.8, 11.7] 3445 100 1 1.0 [− 1.0, 3.0] 0.3 P < 0.05
Saga 4445 80 6 7.5 [1.6, 13.4] 863 100 1 1.0 [− 1.0, 3.0] 0.2 P < 0.05
Gangba 2576 80 0 0.0 711 100 3 3.0 [− 0.4, 6.4] 0.8 P > 0.05
Naqu City Naqu County 15,011 322 23 7.1 [4.3, 10.0] 6170 101 5 5.0 [0.6, 9.3] 2.0 P > 0.05
Jiali 2979 80 10 12.5 [5.1, 19.9] 2999 950 0 0.0 0.0 P < 0.05
Biru 9927 160 4 2.5 [0.1, 4.9] 6275 100 6 6.0 [1.3, 10.7] 3.8 P > 0.05
Nierong 7500 80 3 3.8 [− 0.5, 8.0] 4873 214 25 11.7 [7.3, 16.0] 7.6 P > 0.05
Anduo 4015 79 10 12.7 [5.2, 20.2] 2515 500 4 0.8 [0, 1.6] 0.5 P < 0.05
Shenza 1900 80 11 13.8 [6.0, 21.5] 237 100 0 0.0 0.0 P < 0.05
Suoxian 11,138 80 4 5.0 [0.1, 9.9] 3423 100 0 0.0 0.0 P > 0.05
Bange 4737 80 14 17.5 [9.0, 26.0] 1793 220 10 4.6 [1.8, 7.3] 1.7 P < 0.05
Baqing 12,530 46 19 41.3 [26.5, 56.1] 6578 276 17 6.2 [3.3, 9.0] 3.2 P < 0.05
Nima 5196 80 16 20.0 [11.0, 29.0] 4640 100 0 0.0 0.0 P < 0.05
Shuanghua 1930 40 14 35.0 [19.6, 50.4] 1240 280 0 0.0 0.0 P < 0.05
Ali Pulan 1188 40 4 10.0 [0.3, 19.7] 1696 100 0 0.0 0.0 P < 0.05
Zhadab 550 25 0 0.0 288 100 0 0.0 0.0 /
Gaer 1165 80 6 7.5 [1.6, 13.4] 1076 200 1 0.5 [− 0.5, 1.5] 0.5 P < 0.05
Ritu 1897 40 2 5.0 [− 2.1, 12.1] 962 180 1 0.6 [− 0.5, 1.7] 0.3 P > 0.05
Geji 5266 79 2 2.5 [− 1.0, 6.1] 2510 115 3 2.6 [− 0.3, 5.6] 1.2 P > 0.05
Gaize 4539 79 15 19.0 [10.1, 27.8] 1632 200 5 2.5 [0.3, 4.7] 0.9 P < 0.05
Cuoqin 1558 80 5 6.3 [0.8, 11.7] 1492 200 1 0.5 [− 0.5, 1.5] 0.5 P < 0.05
Linzhi City [12] Linzhi Countya 6775 117 27 23.1 [15.3, 30.8] 2783 1, 058 40 3.8 [2.6, 4.9] 1.6 P < 0.05
Gongbu Jiangda 6673 81 4 4.9 [0.1, 9.8] 2393 166 2 1.2 [− 0.5, 2.9] 0.4 P > 0.05
Milin 5351 80 1 1.3 [− 1.2, 3.7] 2229 192 5 2.6 [0.3, 4.9] 1.1 P > 0.05
Motuo 2988 80 6 7.5 [1.6, 13.4] 432 120 2 1.7 [− 0.7, 4.0] 0.2 P < 0.05
Bomi 5578 80 1 1.3 [− 1.2, 3.7] 2721 205 2 1.0 [− 0.4, 2.3] 0.5 P > 0.05
Chayua 2898 100 3 3.0 [− 0.4, 6.4] 2078 200 0 0.0 0.0 P > 0.05
Langxian 1480 80 3 3.8 [− 0.5, 8.0] 426 774 26 3.4 [2.1, 4.6] 1.0 P > 0.05
Total 74 counties 406,759 7,564 552 7.3 [6.7, 7.9] 171, 479 14, 584 252 1.7 [1.5, 1.9] 0.7 P < 0.05
Open in a new tab

In the process of testing the two rates, different methods were selected according to data characteristics, and Fisher's exact test was used in most cases

CI Confidence interval

aChi-square test

bBoth rates were 0, and therefore no test was performed

Fig. 5.

Fig. 5

Open in a new tab

The number of dogs and positive rate of dogs with Echinococcus spp. in Tibet Autonomous Region

Discussion

China displays the highest echinococcosis prevalence worldwide, and TAR displays the highest echinococcosis prevalence in China [4, 5]. Echinococcosis has developed into a major public health issue, severely impeding economic development, ethnic unity, and social stability of TAR and endangering health and safety of people. TAR has a large pastoral area. Animal husbandry is the main way of production and life for local residents. Tibetan herdsmen families have a traditional habit of keeping dogs to protect their livestock, while pastoralists and Buddhist monks are easily tolerating stray dogs. These habits have been linked to an increased risk of human echinococcosis [13]. Experimental studies have demonstrated that dogs can keep an independent E. multilocularis transmission cycle [6]. There is evidence confirming the hypothesis that wild dogs serve as a reservoir of E. granulosus transmission due to transmission between wild and domestic hosts [14, 15]. While infection rates would decline if dogs cannot wander freely [16], dogs still represent the greatest risk to people [17–19]. Therefore, it is crucial to reduce the incidence of human parasitic infection rates by implementing control measures in animal hosts, namely dogs in this case [20]. Feasible intervention measures of wild hosts and domestic dogs are critical for reducing transmission risks of E. granulosus and E. multilocularis [21]. Control measures for E. granulosus are theoretically more governable in domestic animals [22]. Generally, humans infected with echinococcosis do not cause active transmission of Cystic echinococcosis unless a dog ingests hydatid cysts [23]. Deworming dogs is an effective measure to quickly reduce active transmission [23]. In addition, the density of dog feces is higher around villages with frequent human activities [19]. The positive rate of E. granulosus antigen in dog feces was not related to the density of livestock within its range, but the positive rate of fecal E. multilocularis antigen of domestic dogs was positively correlated with the number of stray dogs visible within 200 m of the activity diameter of domestic dogs [24, 25].

The central finance transfer payment local echinococcosis control project has been launched in 2005. Since 2008, TAR has been included in two counties to carry out epidemiological investigation. Due to the limitations of local conditions, other counties have carried out epidemiological investigation one after another, but the process was slow. In response to the severe situation of echinococcosis prevalence, TAR established a comprehensive echinococcosis control headquarters in February 2017 to coordinate and implement various control measures of stray dogs, limit domestic dogs, and communicate the need to reduce the number of untethered dogs and keep dogs. These measures included population investigation and treatment, domestic dog registration and deworming, stray dog sheltering, livestock immunization, and quality of drinking water. Specifically, the government enforced the control of infection sources by limiting the number of dogs, registering them, and issuing domestic dog certificates via an electronic registration system. Stray dogs were captured and sent to the nearest shelters for management. The population of domestic dogs did not decline significantly but remained relatively stable, implying that public awareness of stray dog sheltering and tethering led to an absence of increase. Before 2016, TAR had a substantially large number of dogs, with almost every family owing at least one dog. However, although no statistics on dog breeding are available. As echinococcosis control programs, health education, and people awareness advanced, people have become aware of animal hazards, have reduced the number of dogs in their families, or have even completely stopped feeding dogs. After three years of control practices, the number of stray dogs was effectively reduced. Up to now, TAR has spent CNY 37 million on building 84 stray dog shelters, and 446,660 stray or infected dogs were captured, sheltered or euthanized. The drastic reduction in stray dogs played a vital role in controlling infection sources and significantly reducing the risk of echinococcosis transmission. The dog infection rate has always been a sensitive indicator of the local prevalence and risk of cystic echinococcosis transmission.

To ensure that every dog is dewormed monthly, government departments supervised the deworming practices of domestic dogs in each village. Simultaneously, a multi-dimensional, multi-index assessment and evaluation system for echinococcosis control measures was established. In TAR, the number of stray dogs has decreased sharply, and domestic dogs have been tethered and incorporated into standardized management. On-site sampling surveys confirmed that dog deworming drugs were properly distributed. Although most dogs have achieved deworming monthly, the infection rate of dogs was still very high. Contradictions in dog feces test results indicate the presence of loopholes in the deworming process. This may result from false records in some areas or improperly implemented deworming measures (the dog did not swallow praziquantel, or the tablets were not mashed, and dogs ate the zanba and spit out the tablets). Low infection rates are also associated with sensitivity, specificity, and cross-reactivity of the test kits. A study estimated that the minimal burden of worms for assessing sensitivity might be 500, and had a suggestion for improving the sensitivity of the test kits that using parallel detection with two different kits at the same time or multiple sampling from one dog [26]. In a sample survey in TAR 93.4% of the villagers expressed their willingness to cooperate with free deworming for dogs [10]. These strategic measures are well-suited to the situation of lack of local professionals. They significantly reduce the risk of echinococcosis in the environment by focusing on the top concern, i.e., controlling the source of infection. Additionally, it provides a successful experience for other endemic counties in TAR. The measures are consistent with national control strategies and international experience with echinococcosis control [27].

The quasi eradication of stray dogs and the drastic reduction in the infection rate with Echinococcus spp. of domestic dogs seems to result from the TAR's efforts to control dogs as an infection source. Seven dog-targeted control programs were successfully implemented in islands states/nations, resulting in parasite elimination [28]. Iceland, New Zealand, Falkland Islands, or Tasmania have successfully eliminated CE from dogs and livestock by undertaking dog-targeted, including culling, purgation and/or anthelmintic treatments and control measures, and improving husbandry and slaughter practices [29]. However, the island is a limited geographical area, which is easier to achieve than the mainland. Additionally, some countries in South America, Europe, and East Africa have experienced success [22]. Dogs deworming successfully reduced the prevalence of E. multilocularis in commensal vole populations in Alaska, confirming that taking measures to protect owned dogs can reduce the risk of zoonotic transmission [30]. Iceland once released a national law stating that the effects of controlling dogs were achieved through taxation and forceful deworming, and it has been in effect since 1890 [23]. The main target of control is the definitive hosts dogs, and the aim is to reduce or eliminate the adult worm burden, which will reduce the transmission to livestock with the greatest and quickest effect [23]. TAR is expected to maintain the current mode and trend of infection source control, identify any deficiencies in control practices, strengthen supervision and quality control, improve the implementation of the computational data system with the objective of eliminating echinococcosis.

This study only assessed the management and control measures of dogs, and did not evaluate the control measures of intermediate hosts. At the same time, there was no assessment of health education in the population. In addition, the fecal sample size of some counties was a little less, and only a few villages were collected, which was difficult to represent the results of a county. Moreover, it was only tested once a year, indicating that the transmission risk in the environment had some limitations.

Conclusions

TAR now has taken comprehensive measures to control the number of domestic and stray dogs, and achieved good results. The management and control of infectious source dogs can reduce the rate of dogs by dog registration and management, dog deworming, disposal of dog feces after deworming, reduction of dog populations, monitoring of dog infection. Comprehensive measures to control infectious source dogs were feasible and effective, and needed continuous implementation.

Acknowledgements

The authors express thanks to the workshops for echinococcosis prevention and control in TAR for provided data.

Abbreviations

AE

Alveolar echinococcosis

CE

Cystic echinococcosis

TAR

Tibet Autonomous Region

DALYs

Disability-adjusted life years

TAR CDC

Tibet Autonomous Region

NIPD

National Institute of Parasitic Diseases

China CDC

Chinese Center for Disease Control and Prevention

Author contributions

LW designed the study, contributed to conceptualization, data collection and screening, verification and analysis, charting and writing, funding acquisition, investigation and resources. GQ participated in data collection, investigation and resources. HP and YW contributed to data collection. MQ participated in data analysis. JL contributed to conceptualization and project administration. RF and LG participated in analysis, review and supervised the study. RF and LG revised the manuscript. All authors read and approved the final manuscript.

Funding

The study was financially supported by the National Natural Science Foundation of China (Grant No. 81703281) and NHC Key Laboratory of Echinococcosis Prevention and Control, China (No.2021WZK1006).

Availability of data and materials

The relevant materials and data in this study are inaccessible to peers.

Declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

Roger Frutos is an editorial board member of the journal Infectious Diseases of Poverty. He was not involved in the peer-review or handling of the manuscript. The authors have no other competing interests to disclose.

Footnotes

Liying Wang and Quzhen Gongsang co-first authors.

Contributor Information

Liying Wang, Email: wangliyingcdc@163.com.

Quzhen Gongsang, Email: gongsang1212@126.com.

Huasheng Pang, Email: 478310952@qq.com.

Min Qin, Email: qmkx0106@163.com.

Ying Wang, Email: wangying1162@163.com.

Jingzhong Li, Email: 13908996200@139.com.

Roger Frutos, Email: roger.frutos@cirad.fr.

Laurent Gavotte, Email: laurent.gavotte@umontpellier.fr.

References

  • 1.Budke CM, Jiamin Q, Zinsstag J, Qian W, Torgerson PR. Use of disability adjusted life years in the estimation of the disease burden of echinococcosis for a high endemic region of the Tibetan plateau. Am J Trop Med Hyg. 2004;71(1):56–64. doi: 10.4269/ajtmh.2004.71.56. [DOI] [PubMed] [Google Scholar]
  • 2.Budke CM, Deplazes P, Torgerson PR. Global socioeconomic impact of cystic echinococcosis. Emerg Infect Dis. 2006;12(2):296–303. doi: 10.3201/eid1202.050499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Torgerson PR, Keller K, Magnotta M, Ragland N. The global burden of alveolar echinococcosis. PLoS Negl Trop Dis. 2010;4(6):e722. doi: 10.1371/journal.pntd.0000722. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Wu WP, Wang H, Wang Q, Zhou XN, Wang LY, Zheng CJ, et al. A nationwide sampling survey on echinococcosis in China during 2012–2016. Chin J Parasitol Parasit. 2018;36:1–14. [Google Scholar]
  • 5.Li B, Quzhen G, Xue CZ, Han S, Chen WQ, Yan XL, et al. Epidemiological survey of echinococcosis in Tibet Autonomous Region of China. Infect Dis Poverty. 2019;8(1):29. doi: 10.1186/s40249-019-0537-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Moss JE, Chen X, Li T, Qiu J, Wang Q, Giraudoux P, et al. Reinfection studies of canine echinococcosis and role of dogs in transmission of Echinococcus multilocularis in Tibetan communities, Sichuan, China. Parasitology. 2013;140(13):1685–1692. doi: 10.1017/S0031182013001200. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Wang X, Liu J, Zuo Q, Mu Z, Weng X, Sun X, et al. Echinococcus multilocularis and Echinococcus shiquicus in a small mammal community on the eastern Tibetan Plateau: host species composition, molecular prevalence, and epidemiological implications. Parasit Vectors. 2018;11(1):302. doi: 10.1186/s13071-018-2873-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Craig PS. Echinococcosis Working Group in China. Epidemiology of human alveolar echinococcosis in China. Parasitol Int. 2006;55:S221–S225. doi: 10.1016/j.parint.2005.11.034. [DOI] [PubMed] [Google Scholar]
  • 9.Wang Z, Wang X, Liu X. Echinococcosis in China, a review of the epidemiology of Echinococcus spp. EcoHealth. 2008;5(2):115–126. doi: 10.1007/s10393-008-0174-0. [DOI] [PubMed] [Google Scholar]
  • 10.Yan XL, Gong S, Wu WP, Zheng CJ, Xue CZ, Chen WQ, et al. Survey on knowledge, attitude and behaviors toward hydatid disease among villagers and students in Tibet Autonomous Region. Chin J Parasitol Parasit Dis. 2018;1:38–42 (In Chinese).
  • 11.Craig PS, Giraudoux P, Wang ZH, Wang Q. Echinococcosis transmission on the Tibetan Plateau. Adv Parasitol. 2019;104:165–246. doi: 10.1016/bs.apar.2019.03.001. [DOI] [PubMed] [Google Scholar]
  • 12.Wang Y, Ma BC, Wang LY, Quzhen G, Pang HS. Effects of management of infection source of echinococcosis in Linzhi, Tibet Autonomous Region of China. Infect Dis Poverty. 2021;10(1):25. doi: 10.1186/s40249-021-00805-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Craig PS, Li T, Qiu J, Zhen R, Wang Q, Giraudoux P, et al. Echinococcosis and Tibetan communities. Emerg Infect Dis. 2008;14(10):1674–1675. doi: 10.3201/eid1410.071636. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Grainger HJ, Jenkins DJ. Transmission of hydatid disease to sheep from wild dogs in Victoria. Australia Int J Parasitol. 1996;26:1263–1270. doi: 10.1016/S0020-7519(96)00109-9. [DOI] [PubMed] [Google Scholar]
  • 15.Jenkins DJ, Macpherson CN. Transmission ecology of Echinococcus in wild-life in Australia and Africa. Parasitology. 2003;127(Suppl):S63–S72. doi: 10.1017/S0031182003003871. [DOI] [PubMed] [Google Scholar]
  • 16.Buishi IE, Njoroge EM, Bouamra O, Craig PS. Canine echinococcosis in northwest Libya: assessment of coproantigen ELISA, and a survey of infection with analysis of risk-factors. Vet Parasitol. 2005;130:223–232. doi: 10.1016/j.vetpar.2005.03.004. [DOI] [PubMed] [Google Scholar]
  • 17.Budke CM, Jiamin Q, Craig PS, Torgerson PR. Modeling the transmission of Echinococcus granulosus and Echinococcus multilocularis in dogs for a high endemic region of the Tibetan plateau. Int J Parasitol. 2005;35(2):163–170. doi: 10.1016/j.ijpara.2004.10.026. [DOI] [PubMed] [Google Scholar]
  • 18.Li TY, Qiu JM, Wen Y, Craig PS, Chen XW, Xiao N, et al. Echinococcosis in Tibetan populations, western Sichuan Province. China Emerg Infect Dis. 2005;11(12):1866–1873. doi: 10.3201/eid1112.051041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Vaniscotte A, Raoul F, Poulle ML, Romig T, Dinkel A, Takahashi K, et al. Role of dog behaviour and environmental fecal contamination in transmission of Echinococcus multilocularis in Tibetan communities. Parasitology. 2011;138(10):1316–1329. doi: 10.1017/S0031182011000874. [DOI] [PubMed] [Google Scholar]
  • 20.Otero-Abad B, Torgerson PR. A systematic review of the epidemiology of echinococcosis in domestic and wild animals. PLoS Negl Trop Dis. 2013;7(6):e2249. doi: 10.1371/journal.pntd.0002249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Deplazes P, van Knapen F, Schweiger A, Overgaauw PA. Role of pet dogs and cats in the transmission of helminthic zoonoses in Europe, with a focus on echinococcosis and toxocarosis. Vet Parasitol. 2011;182:41–53. doi: 10.1016/j.vetpar.2011.07.014. [DOI] [PubMed] [Google Scholar]
  • 22.Craig PS, Larrieu E. Control of cystic echinococcosis/hydatidosis: 1863–2002. Adv Parasitol. 2006;61:443–508. doi: 10.1016/S0065-308X(05)61011-1. [DOI] [PubMed] [Google Scholar]
  • 23.Craig PS, Hegglin D, Lightowlers MW, Torgerson PR, Wang Q. Echinococcosis: control and prevention. Adv Parasitol. 2017;96:55–158. doi: 10.1016/bs.apar.2016.09.002. [DOI] [PubMed] [Google Scholar]
  • 24.Chaâbane-Banaoues R, Oudni-M'rad M, Cabaret J, M'rad S, Mezhoud H, Babba H. Infection of dogs with Echinococcus granulosus: causes and consequences in an hyperendemic area. Parasit Vectors. 2015;8:231. doi: 10.1186/s13071-015-0832-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Wang Q, Raoul F, Budke C, Craig PS, Xiao YF, Vuitton DA, et al. Grass height and transmission ecology of Echinococcus multilocularis in Tibetan communities, China. Chin Med J (Engl) 2010;123(1):61–67. [PubMed] [Google Scholar]
  • 26.Wang L, Wang Q, Cai H, Wang H, Huang Y, Feng Y, et al. Evaluation of fecal immunoassays for canine Echinococcus infection in China. PLoS Negl Trop Dis. 2021;15:e0008690. doi: 10.1371/journal.pntd.0008690. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Gong S, Wang LY, Niu YL, Baima YJ, Ciren LM, Xiao D, et al. Analysis of the characteristics of the spatial distribution of human echinococcosis in the Tibet Autonomous Region. J Pathog Biol. 2018;13(1):64–67. [Google Scholar]
  • 28.Craig PS, McManus DP, Lightowlers MW, Chabalgoity JA, Garcia HH, Gavidia CM, et al. Prevention and control of cystic echinococcosis. Lancet Infect Dis. 2007;7(6):385–394. doi: 10.1016/S1473-3099(07)70134-2. [DOI] [PubMed] [Google Scholar]
  • 29.Irabedra P, Ferreira C, Sayes J, Elola S, Rodríguez M, Morel N, et al. Control programme for cystic echinococcosis in Uruguay. Mem Inst Oswaldo Cruz. 2016;111(6):372–377. doi: 10.1590/0074-02760160070. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Rausch RL, Wilson JF, Schantz PM. A programme to reduce the risk of infection by Echinococcus multilocularis: the use of praziquantel to control the cestode in a village in the hyperendemic region of Alaska. Ann Trop Med Parasitol. 1990;84(3):239–250. doi: 10.1080/00034983.1990.11812463. [DOI] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The relevant materials and data in this study are inaccessible to peers.

Articles from Infectious Diseases of Poverty are provided here courtesy of BMC

RESOURCES