Hostname: page-component-848d4c4894-x5gtn Total loading time: 0 Render date: 2024-05-25T08:44:38.043Z Has data issue: false hasContentIssue false

Investigation of giardiasis in captive animals in zoological gardens with strain typing of assemblages in China

Published online by Cambridge University Press:  08 June 2021

Hua Liu*
Affiliation:
National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention (Chinese Center for Tropical Diseases Research), NHC Key Laboratory of Parasite and Vector Biology, WHO Collaborating Centre for Tropical Diseases, National Center for International Research on Tropical Diseases, Shanghai200025, China
Bin Wang
Affiliation:
Department of Parasitology, Zunyi Medical University, Zunyi563000, China Guizhou Center for Disease Control and Prevention, Guiyan550000, China
Jianhai Yin
Affiliation:
National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention (Chinese Center for Tropical Diseases Research), NHC Key Laboratory of Parasite and Vector Biology, WHO Collaborating Centre for Tropical Diseases, National Center for International Research on Tropical Diseases, Shanghai200025, China
Zhongying Yuan
Affiliation:
National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention (Chinese Center for Tropical Diseases Research), NHC Key Laboratory of Parasite and Vector Biology, WHO Collaborating Centre for Tropical Diseases, National Center for International Research on Tropical Diseases, Shanghai200025, China
Yanyan Jiang
Affiliation:
National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention (Chinese Center for Tropical Diseases Research), NHC Key Laboratory of Parasite and Vector Biology, WHO Collaborating Centre for Tropical Diseases, National Center for International Research on Tropical Diseases, Shanghai200025, China
Jing Zhang
Affiliation:
National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention (Chinese Center for Tropical Diseases Research), NHC Key Laboratory of Parasite and Vector Biology, WHO Collaborating Centre for Tropical Diseases, National Center for International Research on Tropical Diseases, Shanghai200025, China
Jianping Cao
Affiliation:
National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention (Chinese Center for Tropical Diseases Research), NHC Key Laboratory of Parasite and Vector Biology, WHO Collaborating Centre for Tropical Diseases, National Center for International Research on Tropical Diseases, Shanghai200025, China
Yujuan Shen*
Affiliation:
National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention (Chinese Center for Tropical Diseases Research), NHC Key Laboratory of Parasite and Vector Biology, WHO Collaborating Centre for Tropical Diseases, National Center for International Research on Tropical Diseases, Shanghai200025, China
Hui Liu*
Affiliation:
Department of Parasitology, Zunyi Medical University, Zunyi563000, China
*
Authors for correspondence: Yujuan Shen, E-mail: shenyj@nipd.chinacdc.cn; Hui Liu, E-mail: liuhui6032@sina.com
Authors for correspondence: Yujuan Shen, E-mail: shenyj@nipd.chinacdc.cn; Hui Liu, E-mail: liuhui6032@sina.com
Authors for correspondence: Yujuan Shen, E-mail: shenyj@nipd.chinacdc.cn; Hui Liu, E-mail: liuhui6032@sina.com

Abstract

Giardia duodenalis is a common zoonotic intestinal pathogen. It has been increasingly reported in humans and animals; however, genotyping information for G. duodenalis in captive animals is still limited. This study was conducted to assess the prevalence and multilocus genotyping of G. duodenalis in captive animals in zoological gardens in Shanghai, China. A total of 678 fresh fecal samples were randomly collected from captive animals including non-human primates (NHPs) (n = 190), herbivores (n = 190), carnivores (n = 151), birds (n = 138) and reptiles (n = 9) in a zoo and were examined for the presence of G. duodenalis using nested polymerase chain reaction (nested PCR). All G. duodenalis positive samples were assayed with PCR followed by sequencing at β-giardin (bg), glutamate dehydrogenase (gdh) and triose phosphate isomerase (tpi) genes. In this study, 42 specimens (6.2%) were tested G. duodenalis-positive of the 678 fecal samples examined based on a single locus. A total of 30 (4.4%), 30 (4.4%) and 22 (3.2%) specimens were successfully amplified and sequenced at gdh, tpi and bg loci, respectively. Assemblages A and B were identified with assemblage B dominating in NHPs. Sequence analysis demonstrated that one, two and five new isolates were identified at bg, gdh and tpi loci. DNA sequences and new assemblage-subtypes of zoonotic G. duodenalis assemblages A and B were identified in the current study. Our data indicate the occurrence and molecular diversity of G. duodenalis and the potential zoonotic transmission in captive animals in China.

Type
Research Article
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

These authors contributed equally to this work.

References

Abeywardena, H, Jex, AR and Gasser, RB (2015) A perspective on Cryptosporidium and Giardia, with an emphasis on bovines and recent epidemiological findings. Advances in Parasitology 88, 243301.CrossRefGoogle ScholarPubMed
Beck, R, Sprong, H, Bata, I, Lucinger, S, Pozio, E and Cacciò, SM (2011) Prevalence and molecular typing of Giardia spp. in captive mammals at the zoo of Zagreb, Croatia. Veterinary Parasitology 175, 4046.CrossRefGoogle Scholar
Berrilli, F, Prisco, C, Friedrich, KG, Cerbo, PD, Cave, DD and Liberato, CD (2011) Giardia duodenalis assemblages and Entamoeba species infecting non-human primates in an Italian zoological garden: zoonotic potential and management traits. Parasites & Vectors 4, 199.CrossRefGoogle Scholar
Brearley, G, Rhodes, J, Bradley, A, Baxter, G, Seabrook, L, Lunney, D, Liu, Y and McAlpine, C (2013) Wildlife disease prevalence in human-modified landscapes. Biological Reviews of the Cambridge Philosophical Society 88, 427442.CrossRefGoogle ScholarPubMed
Cacciò, SM and Ryan, U (2008) Molecular epidemiology of giardiasis. Molecular and Biochemical Parasitology 160, 7580.CrossRefGoogle ScholarPubMed
Cacciò, SM, Beck, R, Lalle, M, Marinculic, A and Pozio, E (2008) Multilocus genotyping of Giardia duodenalis reveals striking differences between assemblages A and B. International Journal for Parasitology 38, 15231531.CrossRefGoogle ScholarPubMed
Daszak, P, Cunningham, AA and Hyatt, AD (2000) Emerging infectious diseases of wildlife – threats to biodiversity and human health. Science (New York, N.Y.) 287, 443449.CrossRefGoogle ScholarPubMed
Du, S, Zhao, G, Shao, J, Fang, Y, Tian, G, Zhang, L, Wang, R, Wang, H, Qi, M and Yu, S (2015) Cryptosporidium spp., Giardia intestinalis, and Enterocytozoon bieneusi in captive non-human primates in Qinling Mountains. Korean Journal of Parasitology 53, 395402.CrossRefGoogle ScholarPubMed
Fayer, R, Trout, JM, Graczyk, TK and Lewis, EJ (2000) Prevalence of Cryptosporidium, Giardia and Eimeria infections in post-weaned and adult cattle on three Maryland farms. Veterinary Parasitology 93, 103112.CrossRefGoogle ScholarPubMed
Feng, Y and Xiao, L (2011) Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clinical Microbiology Reviews 24, 110140.CrossRefGoogle ScholarPubMed
Halliez, MC and Buret, AG (2013) Extra-intestinal and long term consequences of Giardia duodenalis infections. World Journal of Gastroenterology 19, 89748985.CrossRefGoogle ScholarPubMed
Johnston, AR, Gillespie, TR, Rwego, IB, McLachlan, TL, Kent, AD and Goldberg, TL (2010) Molecular epidemiology of cross-species Giardia duodenalis transmission in western Uganda. PLoS Neglected Tropical Diseases 4, e683.CrossRefGoogle ScholarPubMed
Karim, MR, Zhang, S, Jian, F, Li, J, Zhou, C, Zhang, L, Sun, M, Yang, G, Zou, F, Dong, H, Li, J, Rume, FI, Qi, M, Wang, R, Ning, C and Xiao, L (2014) Multilocus typing of Cryptosporidium spp. and Giardia duodenalis from non-human primates in China. International Journal for Parasitology 44, 10391047.CrossRefGoogle ScholarPubMed
Karim, MR, Wang, R, Yu, F, Li, T, Dong, H, Li, D, Zhang, L, Li, J, Jian, F, Zhang, S, Rume, I, Ning, C and Xiao, L (2015) Multi-locus analysis of Giardia duodenalis from nonhuman primates kept in zoos in China: geographical segregation and host-adaptation of assemblage B isolates. Infection Genetics and Evolution 30, 8288.CrossRefGoogle ScholarPubMed
Lalle, M, Pozio, E, Capelli, G, Bruschi, F, Crotti, D and Cacciò, SM (2005) Genetic heterogeneity at the beta-giardin locus among human and animal isolates of Giardia duodenalis and identification of potentially zoonotic subgenotypes. International Journal for Parasitology 35, 207213.CrossRefGoogle Scholar
Li, J, Dong, H, Wang, R, Yu, F, Wu, Y, Chang, Y, Wang, C, Qi, M and Zhang, L (2017) An investigation of parasitic infections and review of molecular characterization of the intestinal protozoa in nonhuman primates in China from 2009 to 2015. International Journal for Parasitology. Parasites and Wildlife 6, 815.CrossRefGoogle ScholarPubMed
Liu, A, Yang, F, Shen, Y, Zhang, W, Wang, R, Zhao, W, Zhang, L, Ling, H and Cao, J (2014) Genetic analysis of the Gdh and Bg genes of animal-derived Giardia duodenalis isolates in Northeastern China and evaluation of zoonotic transmission potential. PLoS One 9, e95291.CrossRefGoogle ScholarPubMed
Liu, H, Shen, Y, Liu, A, Yin, J, Yuan, Z, Jiang, Y, Pan, W, Zhang, Y, Zhao, W and Cao, J (2017) Occurrence and multilocus genotyping of Giardia duodenalis in pets and zoo animals in Shanghai, China. Journal of Infection in Developing Countries 11, 479486.CrossRefGoogle ScholarPubMed
Long, K, Cai, L and He, L (2018) DNA sequencing data analysis. Methods in Molecular Biology 1754, 113.CrossRefGoogle ScholarPubMed
Mynářová, A, Foitová, I, Kváč, M, Květoňová, D, Rost, M, Morrogh-Bernard, H, Nurcahyo, W, Nguyen, C, Supriyadi, S and Sak, B (2016) Prevalence of Cryptosporidium spp., Enterocytozoon bieneusi, Encephalitozoon spp. and Giardia intestinalis in wild, semi-wild and captive orangutans (Pongo abelii and Pongo pygmaeus) on Sumatra and Borneo, Indonesia. PLoS One 11, e152771.CrossRefGoogle ScholarPubMed
Oates, SC, Miller, MA, Hardin, D, Conrad, PA, Melli, A, Jessup, DA, Dominik, C, Roug, A, Tinker, MT and Miller, WA (2012) Prevalence, environmental loading, and molecular characterization of Cryptosporidium and Giardia isolates from domestic and wild animals along the Central California Coast. Applied and Environmental Microbiology 78, 87628772.CrossRefGoogle ScholarPubMed
Qi, M, Wang, H, Jing, B, Wang, R, Jian, F, Ning, C and Zhang, L (2016) Prevalence and multilocus genotyping of Giardia duodenalis in dairy calves in Xinjiang, Northwestern China. Parasites & Vectors 9, 546.CrossRefGoogle ScholarPubMed
Reboredo-Fernández, A, Ares-Mazás, E, Cacciò, SM and Gómez-Couso, H (2015) Occurrence of Giardia and Cryptosporidium in wild birds in Galicia (Northwest Spain). Parasitology 142, 917925.CrossRefGoogle Scholar
Ryan, U and Cacciò, SM (2013) Zoonotic potential of Giardia. International Journal for Parasitology 43, 943956.CrossRefGoogle ScholarPubMed
Sricharern, W, Inpankaew, T, Keawmongkol, S, Supanam, J, Stich, RW and Jittapalapong, S (2016) Molecular detection and prevalence of Giardia duodenalis and Cryptosporidium spp. among long-tailed macaques (Macaca fascicularis) in Thailand. Infection Genetics and Evolution 40, 310314.CrossRefGoogle Scholar
Sulaiman, IM, Fayer, R, Bern, C, Gilman, RH, Trout, JM, Schantz, PM, Das, P, Lal, AA and Xiao, L (2003) Triosephosphate isomerase gene characterization and potential zoonotic transmission of Giardia duodenalis. Emerging Infectious Diseases 9, 14441452.CrossRefGoogle ScholarPubMed
Thompson, RC (2013) Parasite zoonoses and wildlife: one health, spillover and human activity. International Journal for Parasitology 43, 10791088.CrossRefGoogle ScholarPubMed
Thompson, RC, Lymbery, AJ and Smith, A (2010) Parasites, emerging disease and wildlife conservation. International Journal for Parasitology 40, 11631170.CrossRefGoogle ScholarPubMed
Wegayehu, T, Karim, R, Li, J, Adamu, H, Erko, B, Zhang, L and Tilahun, G (2016) Multilocus genotyping of Giardia duodenalis isolates from children in Oromia Special Zone, central Ethiopia. BMC Microbiology 16, 89.CrossRefGoogle ScholarPubMed
Ye, J, Xiao, L, Ma, J, Guo, M, Liu, L and Feng, Y (2012) Anthroponotic enteric parasites in monkeys in public park, China. Emerging Infectious Diseases 18, 16401643.CrossRefGoogle ScholarPubMed
Ye, J, Xiao, L, Li, J, Huang, W, Amer, SE, Guo, Y, Roellig, D and Feng, Y (2014) Occurrence of human-pathogenic Enterocytozoon bieneusi, Giardia duodenalis and Cryptosporidium genotypes in laboratory macaques in Guangxi, China. Parasitology International 63, 132137.CrossRefGoogle ScholarPubMed
Zhang, X, Wang, L, Lan, X, Dan, J, Ren, Z, Cao, S, Shen, L, Deng, J, Zuo, Z, Yu, S, Wang, Y, Ma, X, Liu, H, Zhou, Z, Hu, Y, Fu, H, He, C, Geng, Y, Gu, X, Peng, G, Wang, Y and Zhong, Z (2020) Occurrence and multilocus genotyping of Giardia duodenalis in captive non-human primates from 12 zoos in China. PLoS ONE 15, e0228673.CrossRefGoogle ScholarPubMed
Zhong, Z, Tian, Y, Li, W, Huang, X, Deng, L, Cao, S, Geng, Y, Fu, H, Shen, L, Liu, H and Peng, G (2017) Multilocus genotyping of Giardia duodenalis in captive non-human primates in Sichuan and Guizhou provinces, Southwestern China. PLoS One 12, e184913.CrossRefGoogle ScholarPubMed
Supplementary material: File

Liu et al. supplementary material

Tables S1-S2

Download Liu et al. supplementary material(File)
File 19.8 KB