Endemic echinococcosis is still a serious challenge in northwestern China. We employed smart deworming collars controlled by remote management system (RMS) to deliver baits containing praziquantel (PZQ), a medication used to treat parasitic worm infections, for dogs. Compared with existing manual deworming techniques, the deworming coverage increased from 57.7% (173/300) to 85.7% (945/1,103) following the smart collars implementation, and the monthly deworming rate increased from 40.3% (121/300) to 91.4% (1,008/1,103). The positive rates of Echinococcus antigen in canine feces were reduced to zero, which suggests that this may be a novel effective alternative to reduce the transmission of echinococcosis.
Echinococcosis is a severe cross-species transmitted parasitic disease (1), and cystic echinococcosis (CE) caused by Echinococcus granulosus and alveolar echinococcosis (AE) caused by Echinococcus. multilocularis are the two main forms in human. In China, CE is widely endemic in at least 368 counties of 9 provincial-level administrative divisions (PLADs) and AE is co-endemic with CE in 115 of these counties (2). China remains the region with the most serious endemic disease burden, which comprised 40% of the world’s CE disability-adjusted life years (DALYs) and 91% of new cases of AE per year globally (3–4).
Existing studies demonstrated that dogs were the most definitive host for Echinococcus spp. and its role in transmission of both CE and AE was significant (5). Periodic deworming of dogs is a highly effective measure against echinococcosis recommended by the World Health Organization (WHO) and Office International Des Epizooties (OIE) (6). In China from 2006, a monthly deworming program was employed to control the transmission of canine echinococcosis to livestock and humans (7–8), and significant progress has taken place to reduce the population prevalence of echinococcosis and the infection rate of Echinococcus spp. in dogs(2). However, in harsh climate and high altitude areas such as the Qinghai-Tibet Plateau, the unique humanistic values and nomadic production methods caused the implementation of manual monthly deworming for every dog encountered to become difficult and challenging, and the real data on the deworming coverage and frequency was difficult to obtain. Even in a county where the National Control Program struggled to achieve monthly deworming from 2010, the deworming coverage for dogs was not higher than 63.2% (9). In another county earmarked for the comprehensive control of echinococcosis in 2016–2017, only 21.7% (30/138) of dog owners performed deworming once a month (10). The low deworming frequency and coverage was responsible for the high prevalence of echinococcus among dogs, including 2.96% in Sichuan, 3.03% in Ningxia, 4.91% in Gansu, 7.3% in Xizang (Tibet), 13.0% in Qinghai, and 41.3% in Hobukesar County, Xinjiang, China (2,9).
In this study, we employed a smart deworming collar controlled by RMS, a platform specially developed for managing and controlling smart deworming devices, to deliver bait containing PZQ (100 mg per bait; Beijing Zhongnong Warwick Pharmaceutical Co., Ltd., Beijing, China. batch: 20190613) for dogs automatically, regularly, and quantitatively to increase the deworming frequency and coverage, reduce the dogs’ infection rate of Echinococcus spp., further reduce the abundance of parasitic eggs in the environment, and ultimately prevent the transmission of echinococcosis from dogs to humans and livestock.
From June to November, 2020, a six-month field evaluation was performed in Kangma County, Shigatse City, Tibet Autonomous Region of China, which is a semi-agricultural and semi-pastoral border county with a severe epidemic of echinococcosis, an average altitude of >4,300 m, and an annual average temperature of about 4 °C. The population is around 34,000, of which >99% are ethnic Tibetans, the population prevalence of echinococcosis is 1.74%, and the overall positive rates of Echinococcus antigen in canine feces is 7.5%. Based on the production style, the population prevalence of echinococcosis, the number of dogs, and the positive rates of Echinococcus antigen in canine feces, a stratified cluster sampling method was conducted, and 5 townships were identified as smart collar group with 1,103 registered dogs and the other 4 townships as manual deworming group with 605 registered dogs. Local staff attached the smart deworming collars to all the dogs in the smart collar group according to the product specifications. The steps for attaching the smart collar to the dogs were as follows: 1) matching the information of the dogs, the owners, and the smart collars and uploading the information to the RMS; 2) set deworming frequency such as once a month, once a quarter, even once every six months according to the local prevalence of echinococcosis; 3) set the PZQ baits dose for each dog according to the dog’s weight and size; and 4) set deworming time (8:00 or 18:00 on the deworming date), and then the smart deworming collar will run according to the set procedure. The dogs in the manual deworming group remained to be dewormed by the existing manual deworming methods.
In the smart deworming group, the deworming coverage and frequency of the smart collars were counted by the RMS. In the manual deworming group, due to remote locations of nomadic settlements, 300 dog owners (their dogs were randomly selected to collect dog feces once a quarter) were surveyed through questionnaires to obtain the information of monthly deworming. The total fecal sample size was estimated by the Walters normal approximation method and determined to be 600 (300∶300). Each quarter, 300 dogs were randomly selected from the 1,103-dog category and the other 300 dogs from 605-dog category by an accurate random sampling method followed by collection of the fecal samples from each of the chosen dogs. The fecal samples were tested once a quarter with the coproantigen ELISA Kit for Canines (produced by Shenzhen Combined Biotech Co., Ltd., Shenzhen, China) in the National Health Commission (NHC) Key Laboratory of Echinococcosis Prevention and Control. IBM SPSS (version 20.00; International Business Machines Corporation, New York, USA) was used to analyze the data.
Over 85.7% (945/1,103) deworming coverage was achieved with the smart collars, and 91.4% (1,008/1,103) of dogs in smart deworming group were dewormed 6 times during the 6 months. The smart deworming collar increased the deworming coverage and frequency (Tables 1 and 2). The positive rate of Echinococcus antigen in canine feces decreased from 5.7% (17/300) to 0 after six months of smart-collar deworming (Table 3).
Group Number of dogs (n) Beginning deworming Three months later Six months later Actual number covered (n) Rate (%) Actual number covered (n) Rate (%) Actual number covered (n) Rate (%) Smart collar deworming group 1,103 1,103 100.0 1,032 93.6 945 85.7 Manual deworming group 300 129 43.0 158 52.7 173 57.7
Table 1. Deworming coverage between the two groups in Kangma County, Shigatse City, Tibet from June to November 2020.
Deworming frequency Smart collar deworming group Manual deworming group Number of dogs (n) Constituent ratio (%) Number of dogs (n) Constituent ratio (%) 0 0 0.0 19 6.3 1 9 0.8 43 14.3 2 16 1.5 29 9.7 3 23 2.1 25 8.3 4 21 1.9 30 10.0 5 26 2.5 33 11.0 6 1,008* 91.4 121 40.3 Total 1,103 100.0 300 100.0 * The number 1,008 sums 945 and 63, where 945 is the number of the dogs with smart deworming collars still attached after six months, and 63 is the number of the dogs which although the smart deworming collars were removed by their owners, the smart deworming collars still ran well to deliver the bait containing praziquantel once a month, and the owners fed the baits to the dogs.
Table 2. Deworming frequencies between the two groups in Kangma County, Shigatse City, Tibet from June to November 2020.
Deworming time Smart deworming group Manual deworming group χ2 p Test numbers (n) Positive numbers (n) Positive rate (%) Test numbers (n) Positive numbers (n) Positive rate (%) Before deworming 300 17 5.7 300 15 5.0 0.132 >0.05 Three months later 300 1 0.3 300 13 4.3 10.531 <0.05 Six months later 300 0 0.0 300 14 4.7 14.334 <0.05
Table 3. Positive rates of Echinococcus antigen in canine feces between the two groups in Kangma County, Shigatse City, Tibet, from June to November 2020.