The impact of reducing stray dog density on the prevalence of Echinococcus spp. in small mammals

doi:10.12140/j.issn.1000-7423.2021.02.005

Abstract

Abstract:

Objective To investigate the impact of reducing stray dog population on the prevalence of Echinococcus spp. in small mammals. Methods From April 2016 to June 2020, stray dogs were captured and euthanized by professional dog catchers or by the public service department, in Shiqu County of Ganzi Tibetan Autonomous Prefecture throughout the year. During 2015 to 2020, investigators drove along the highway from State-owned livestock farm to Niga Township (130.5 km) in Shiqu County, and recorded the number of stray dogs within the sight distance on both sides of the highway. The density of stray dogs in Shiqu County was calculated by dividing the number of stray dogs by the driving distance. Small mammals were captured in Edoma, Wenbo, Yiniu, Xiazha, Niga, Mengyi and Gemeng Townships of Shiqu County and dissected on-site in July 2016 and July-August 2020. Organs of small mammals were stored in 95% ethanol and transferred back to laboratory. Hydatid lesion-like tissues were sampled from the organs for extraction of genomic DNA for PCR to amplify cytochrome c oxidase subunit 1 (cox1). The amplified products of PCR were sequenced and then compared with the known sequences in GenBank through BLAST to determine the species of Echinococcus. The infection rate of Echinococcus in small mammals was calculated according to the sequencing and alignment results. The 95% confidence interval of the rate was calculated using the Clopper & Pearson exact method. The difference in the prevalence of Echinococcus in small mammals was analyzed by chi-square test or Fisher exact test. Results From April 2016 to June 2020, 41 446 stray dogs were captured and euthanized in Shiqu County, including 26 570, 4 377, 5 656, 4 100, and 743 in each year, respectively. The density of stray dogs in Shiqu from 2015 to 2020 was 0.80, 0.04, 0.06, 0.04, 0.05 and 0.05 per kilometer, respectively. In July 2016, a total of 261 small mammals were captured, including 192 pikas (Lagomorpha : Ochotonidae) and 69 voles (Rodentia : Cricetidae). There were 14 small mammals infected with Echinococcus, of which 8 were voles and 6 pikas. The infection rate of E. multilocularis metacestodes in voles in 2016 was 11.6% (8/69, 95% CI: 5.1%-21.6%). The infection rate of E. multilocularis metacestodes and E. shiquicus metacestodes in pikas in 2016 were both 1.6% (3/192, 95% CI: 0.3%-4.5%). From July to August of 2020, a total of 270 small mammals were captured, of which 223 were voles and 47 pikas. The infection rate of E. multilocularis metacestodes in voles in 2020 was 0.5% (1/223, 95%CI: 0-2.5%). No pikas were found to be infected with Echinococcus spp.. The prevalence of E. multilocularis metacestodes in voles in 2020 was significantly reduced compared with that in 2016 (P < 0.01). The infection rate of E. multilocularis metacestodes and E. shiquicus metacestodes in pikas in 2020 were both lower than that in 2016, but the difference was not statistically significant (P > 0.05). Conclusion In endemic areas where stray dogs play an important role in the transmission of E. multilocularis, measures to reduce the density of stray dogs can significantly lower the infection rate of E. multilocularis metacestodes in voles.

Key words: Alveolar echinococcosis, Density of stray dogs, Small mammals, Shiqu County

CLC Number:

532.32

YANG Liu, HE Wei, WANG Qi, YU Wen-jie, ZHONG Bo, LIU Yang, XIAO Tong-guang, XIE Fei, YAO Ren-xin, HUANG Yan, LI Rui-rui, LIAO Sha, ZHANG Guang-jia, WANG Qian. The impact of reducing stray dog density on the prevalence of Echinococcus spp. in small mammals[J]. CHINESE JOURNAL OF PARASITOLOGY AND PARASITIC DISEASES, 2021, 39(2): 156-160.

Figures/Tables 2

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References 20

[1]	Deplazes P, Rinaldi L, Alvarez Rojas CA, et al. Global distribution of alveolar and cystic echinococcosis[J]. Adv Parasitol, 2017,95:315-493.
[2]	Wu WP, Wang H, Wang Q, et al. A nationwide sampling survey on echinococcosis in China during 2012—2016[J]. Chin J Parasitol Parasit Dis, 2018,36(1):1-14. (in Chinese)
	( 伍卫平, 王虎, 王谦, 等. 2012—2016年中国棘球蚴病抽样调查分析[J]. 中国寄生虫学与寄生虫病杂志, 2018,36(1):1-14.)
[3]	Huang Y, Wang Q, Yi DY, et al. Prevelance investigation and evaluation of human echinococcosis in Sichuan Province[J]. J Prev Med Inf, 2012,28(8):594-597. (in Chinese)
	( 黄燕, 王谦, 易德友, 等. 四川省棘球蚴病患病情况调查及评估[J]. 预防医学情报杂志, 2012,28(8):594-597.)
[4]	Wang Q, Yang L, Wang YF, et al. Disease burden of echinococcosis in Tibetan communities: a significant public health issue in an underdeveloped region of Western China[J]. Acta Trop, 2020,203:105283. doi: 10.1016/j.actatropica.2019.105283
[5]	Ailiyali·A, Sun L, Li BL, et al. The economic burden of echinococcosis in China: a systematic review[J]. Chin J Evid-Based Med, 2019,19(12):1416-1422. (in Chinese)
	( 艾力亚力·艾力, 孙立, 李波霖, 等. 中国包虫病患者经济负担研究的系统评价[J]. 中国循证医学杂志, 2019,19(12):1416-1422.)
[6]	Wang Q, Zhong B, Yu WJ, et al. Assessment of a 10-year dog deworming programme on the transmission of Echinococcus multilocularis in Tibetan communities in Sichuan Province, China[J]. Int J Parasitol, 2021,51(2/3):159-166. doi: 10.1016/j.ijpara.2020.08.010
[7]	He W, Shang JY, Yu WJ, et al. Study on the current status investigation of epidemiology of echinococcosis(hydatidosis) in Shiqu County of Sichuan Province[J]. J Prev Med Inf, 2017,33(9):850-854. (in Chinese)
	( 何伟, 尚婧晔, 喻文杰, 等. 四川省石渠县包虫病流行病学现状调查[J]. 预防医学情报杂志, 2017,33(9):850-854.)
[8]	Wang Q, Qiu JM, Schantz P, et al. Investigation of risk factors for development of human hydatidosis among households raising livestock in Tibetan areas of western Sichuan Province[J]. Chin J Parasitol Parasit Dis, 2001,19(2):93-96. (in Chinese)
	( 王谦, 邱加闽, Schantz P, 等. 四川省西部藏区家庭饲养牲畜人群包虫病风险因素的调查[J]. 中国寄生虫学与寄生虫病杂志, 2001,19(2):93-96.)
[9]	Nakao M, Sako Y, Yokoyama N, et al. Mitochondrial genetic code in cestodes[J]. Mol Biochem Parasitol, 2000,111(2):415-424. doi: 10.1016/S0166-6851(00)00334-0
[10]	Romig T, Kratzer W, Kimmig P, et al. An epidemiologic survey of human alveolar echinococcosis in southwestern Germany. Römerstein Study Group[J]. Am J Trop Med Hyg, 1999,61(4):566-573. pmid: 10548290
[11]	Guislain MH, Raoul F, Giraudoux P, et al. Ecological and biological factors involved in the transmission of Echinococcus multilocularis in the French Ardennes[J]. J Helminthol, 2008,82(2):143-151. doi: 10.1017/S0022149X08912384
[12]	Morishima Y, Tsukada H, Nonaka N, et al. Coproantigen survey for Echinococcus multilocularis prevalence of red foxes in Hokkaido, Japan[J]. Parasitol Int, 1999,48(2):121-134. pmid: 11269273
[13]	Craig PS, Echinococcosis Working Group in China. Epidemiology of human alveolar echinococcosis in China[J]. Parasitol Int, 2006,55(Suppl):221-225.
[14]	Stehr-Green JK, Stehr-Green PA, Schantz PM, et al. Risk factors for infection with Echinococcus multilocularis in Alaska[J]. Am J Trop Med Hyg, 1988,38(2):380-385. pmid: 3354771
[15]	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[J]. Ann Trop Med Parasitol, 1990,84(3):239-250. doi: 10.1080/00034983.1990.11812463
[16]	Kapel CM, Torgerson PR, Thompson RC, et al. Reproductive potential of Echinococcus multilocularis in experimentally infected foxes, dogs, raccoon dogs and cats[J]. Int J Parasitol, 2006,36(1):79-86. pmid: 16199043
[17]	Ziadinov I, Mathis A, Trachsel D, et al. Canine echinococcosis in Kyrgyzstan: using prevalence data adjusted for measurement error to develop transmission dynamics models[J]. Int J Parasitol, 2008,38(10):1179-1190. doi: 10.1016/j.ijpara.2008.01.009 pmid: 18371969
[18]	Takahashi K, Uraguchi K, Hatakeyama H, et al. Efficacy of anthelmintic baiting of foxes against Echinococcus multilocularis in northern Japan[J]. Vet Parasitol, 2013,198(1/2):122-126. doi: 10.1016/j.vetpar.2013.08.006
[19]	König A, Romig T, Holzhofer E. Effective long-term control of Echinococcus multilocularis in a mixed rural-urban area in southern Germany[J]. PLoS One, 2019,14(4):e0214993. doi: 10.1371/journal.pone.0214993
[20]	Yu Q, Xiao N, Yang SJ, et al. Deworming of stray dogs and wild canines with praziquantel-laced baits delivered by an unmanned aerial vehicle in areas highly endemic for echinococcosis in China[J]. Infect Dis Poverty, 2017,6:117. doi: 10.1186/s40249-017-0329-8

乡（镇）Townships	田鼠 Voles				鼠兔 Pika
	多房棘球蚴 E. multilocularis metacestodes		石渠棘球蚴 E. shiquicus metacestodes		多房棘球蚴 E. multilocularis metacestodes		石渠棘球蚴 E. shiquicus metacestodes
	感染率/% Infection rate/%	95%CI	感染率/% Infection rate/%	95%CI	感染率/% Infection rate/%	95%CI	感染率/% Infection rate/%	95%CI
2016
宜牛Yiniu	-	-	-	-	0/5	0~52.2	0/5	0~52.2
虾扎Xiazha	2/11	2.3~51.8	0/11	0~28.5	0 (0/37)	0~9.5	0 (0/37)	0~9.5
温波 Wenbo	2/8	3.2~65.1	0/8	0~36.9	1/17	0.2~28.7	0/17	0~19.5
呢呷 Niga	-	-	-	-	3.6 (2/56)	0.4~12.3	5.4 (3/56)	1.1~14.9
蒙宜Mengyi	3/10	6.7~65.3	0/10	0~30.9	0 (0/39)	0~9.0	0 (0/39)	0~9.0
格孟Gemeng	1/14	0.2~33.9	0/14	0~23.2	0/8	0~36.9	0/8	0~36.9
俄多玛Eduoma	0(0/26)	0~13.2	0 (0/26)	0~13.2	0 (0/30)	0~11.6	0 (0/30)	0~11.6
小计 Subtotal	11.6 (8/69)	5.1~21.6	0 (0/69)	0~5.2	1.6 (3/192)	0.3~4.5	1.6 (3/192)	0.3~4.5
2020
宜牛Yiniu	0 (0/20)	0~16.8	0 (0/20)	0~16.8	0/2	0~84.2	0/2	0~84.2
虾扎Xiazha	0 (0/62)	0~5.8	0 (0/62)	0~5.8	0/2	0~84.2	0/2	0~84.2
温波Wenbo	0/16	0~20.6	0/16	0~20.6	0/9	0~33.6	0/9	0~33.6
呢呷Niga	2.6 (1/39)	0.1~13.5	0 (0/39)	0~9.0	0/15	0~21.8	0/15	0~21.8
蒙宜Mengyi	0 (0/56)	0~6.4	0 (0/56)	0~6.4	0/7	0~41.0	0/7	0~41.0
格孟Gemeng	0/8	0~36.9	0/8	0~36.9	0/7	0~41.0	0/7	0~41.0
俄多玛Eduoma	0 (0/22)	0~15.4	0 (0/22)	0~15.4	0/5	0~52.2	0/5	0~52.2
小计 Subtotal	0.5 (1/223)	0~2.5	0 (0/223)	0~1.6	0 (0/47)	0~7.6	0/47	0~7.6