Volume 25, Number 7—July 2019
Research Letter
Echinococcus canadensis G8 Tapeworm Infection in a Sheep, China, 2018
Abstract
We report a sheep infected with Echinococcus canadensis G8 tapeworm in China in 2018. This pathogen was previously detected in moose, elk, muskox, and mule deer in Europe and North America; our findings suggest a wider host range and geographic distribution. Surveillance for the G8 tapeworm should be conducted in China.
Cystic echinococcosis (CE) is a zoonotic disease of worldwide distribution that causes disease, death, and economic loss in many domestic and wildlife ungulates and carnivore species, as well as in humans. Animals and humans can become infected through the accidental ingestion of Echinococcus tapeworm eggs (1,2). Echinococcus granulosus sensu stricto (G1, G3) tapeworms are considered the major cause of CE globally; however, cases attributable to E. canadensis genotypes within the E. granulosus tapeworm complex are increasingly being recognized (3). Overall, E. canadensis tapeworms comprise 4 genotypes (G6, G7, G8, G10), although the taxonomy is still being debated (4). E. canadensis G8 tapeworms were initially identified in 1994 in a moose (Alces alces) in Minnesota, USA (Appendix Table). Then, in 2002, two infections were reported in humans in Alaska. G8 tapeworms have also been found in elk (Cervus canadensis, 2006) and muskox (Ovibos moschatus, 2013) in Canada. Updated epidemiologic data show infections have also occurred in Estonia moose (2008), Russia moose (2013), and a US mule deer (Odocoileus hemionus, 2018). As of April 2019, at least 4 species (moose, elk, muskox, and mule deer) have been proven to serve as intermediate hosts of G8 tapeworms in Europe and North America. We report a potential new public health threat regarding sheep (Ovis aries) infected with E. canadensis G8 tapeworms in China and highlight the potential wider host range and geographic distribution of this species.
During 2017, we conducted a molecular epidemiologic survey of CE in northwestern China and collected 277 hydatid cysts from sheep (78 from Qinghai-Tibet Plateau, 60 from Xinjiang Autonomous Region) and yaks (Bos mutus; 139 from Qinghai-Tibet Plateau) at local slaughterhouses. During sampling, we handled all animals in strict accordance with the animal welfare laws of China. We genotyped the hydatid cysts using the partial mitochondrial cox1 gene sequence, as described previously (5), and found that most cyst specimens were represented by E. granulosus G1 and G3 tapeworms (data not shown), and 1 sheep cyst was diagnosed as an E. canadensis G8–like tapeworm infection (herein designated sheep-XN) (Appendix Figure 1, panel A). To further investigate the genotype of tapeworm sheep-XN, we amplified the full-length cox1 gene (1,608 bp) and the mitochondrial nad1 gene (894 bp), a method proven effective for Echinococcus tapeworm genotyping (4). This analysis verified that sheep-XN clustered with E. canadensis G8 tapeworms (Appendix Figure 1, panel B). However, given that partial mitochondrial DNA (mtDNA) sequences are insufficient to identify genotype (because of limited loci information) (6), we amplified the complete mtDNA of sheep-XN and compared it with Echinococcus mtDNA sequences from GenBank. The resulting phylogenetic tree showed the same topologic structure as that acquired when using the cox1 and nad1 genes, suggesting that sheep-XN was an E. canadensis G8 tapeworm (Figure).
We confirmed that the sheep-origin hydatid cyst was E. canadensis G8 tapeworm (Appendix Figure 1, panel C) and suggest that this pathogen potentially poses a new public health threat on the Qinghai-Tibet Plateau of China, where human echinococcosis is prevalent. Previous research has shown that sterile cysts usually result when Echinococcus spp. infect species not commonly infected (7). However, for the sheep-origin cyst, we found numerous protoscoleces in the hydatid fluid, indicating the cyst was fertile. Thus, sheep might serve as another intermediate host of the E. canadensis G8 tapeworm in nature and spread protoscoleces to definitive hosts, posing a threat to local herdsmen and livestock.
G6 and G7 tapeworms can circulate through the domestic cycle (in animals such as camels, pigs, and dogs) or the sylvatic cycle (in animals such as reindeer and wolves), and G8 and G10 tapeworms are generally believed to be restricted to the sylvatic cycle in circumpolar regions (Appendix Table) (2,8). Our finding of an E. canadensis G8 tapeworm in a sheep in China should not only alert the local population to be aware of this pathogen but also contributes to the discussion concerning E. canadensis tapeworm taxonomy. Further research is required to determine the transmission dynamics of this pathogen and determine whether the domestic life cycle of E. canadensis G8 tapeworm (circulation through sheep and dogs) has been or is present.
Since 2017, a mandatory vaccination campaign of sheep and goats with the CE vaccine EG95 has been sponsored in high-prevalence areas of China because of China’s policy, the National Medium- and Long-Term Plan for Animal Disease Control (2012–2020) (9). However, EG95 was developed against the E. granulosus G1 tapeworm (10) and might not provide effective protection against the E. canadensis G8 tapeworm. Our findings indicate the G8 tapeworm might be prevalent in sheep in China, suggesting a wider host range and geographic distribution (Appendix Table, Figure 2). Thus, we propose the need for increased surveillance of the E. canadensis G8 tapeworm in China and that integration of this pathogen into ongoing echinococcosis programs is essential for tapeworm prevention and control.
Mr. Hua is a graduate student studying at the Department of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China. His primary research interest is parasite genomics.
Acknowledgment
This work was supported by grants from the Key Technology Research and Development Program of Sichuan Province in China (grant no. 2015NZ0041) and the National Natural Science Foundation of China (grant no. 31672547).
References
- Cardona GA, Carmena D. A review of the global prevalence, molecular epidemiology and economics of cystic echinococcosis in production animals. Vet Parasitol. 2013;192:10–32. DOIPubMedGoogle Scholar
- Cerda JR, Buttke DE, Ballweber LR. Echinococcus spp. tapeworms in North America. Emerg Infect Dis. 2018;24:230–5. DOIPubMedGoogle Scholar
- Alvarez Rojas CA, Romig T, Lightowlers MW. Echinococcus granulosus sensu lato genotypes infecting humans—review of current knowledge. Int J Parasitol. 2014;44:9–18. DOIPubMedGoogle Scholar
- Davidson RK, Lavikainen A, Konyaev S, Schurer J, Miller AL, Oksanen A, et al. Echinococcus across the north: current knowledge, future challenges. Food Waterborn Parasitol. 2016;4:39–53. DOIGoogle Scholar
- Bowles J, Blair D, McManus DP. Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol Biochem Parasitol. 1992;54:165–73. DOIPubMedGoogle Scholar
- Laurimäe T, Kinkar L, Romig T, Omer RA, Casulli A, Umhang G, et al. The benefits of analysing complete mitochondrial genomes: Deep insights into the phylogeny and population structure of Echinococcus granulosus sensu lato genotypes G6 and G7. Infect Genet Evol. 2018;64:85–94. DOIPubMedGoogle Scholar
- Bružinskaitė R, Sarkūnas M, Torgerson PR, Mathis A, Deplazes P. Echinococcosis in pigs and intestinal infection with Echinococcus spp. in dogs in southwestern Lithuania. Vet Parasitol. 2009;160:237–41. DOIPubMedGoogle Scholar
- Oksanen A, Lavikainen A. Echinococcus canadensis transmission in the North. Vet Parasitol. 2015;213:182–6. DOIPubMedGoogle Scholar
- Zhong Z. The national medium- and long-term plan for animal disease control (2012–2020). 2014 Nov 4 [cited 2018 Nov 11]. http://ap.fftc.agnet.org/ap_db.php?id=308
- Alvarez Rojas CA, Gauci CG, Lightowlers MW. Antigenic differences between the EG95-related proteins from Echinococcus granulosus G1 and G6 genotypes: implications for vaccination. Parasite Immunol. 2013;35:99–102. DOIPubMedGoogle Scholar
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Cite This ArticleOriginal Publication Date: June 10, 2019
1These authors contributed equally to this article.
Table of Contents – Volume 25, Number 7—July 2019
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Please use the form below to submit correspondence to the authors or contact them at the following address:
Guangyou Yang, Department of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, 211 Huimin Rd, Chengdu, Sichuan, 611130, China
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