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A relatively high zoonotic trematode prevalence in Orientogalba ollula and the developmental characteristics of isolated trematodes by experimental infection in the animal model

BACKGROUND: Food-borne parasitic diseases decrease food safety and threaten public health. The snail species is an intermediate host for numerous human parasitic trematodes. Orientogalba ollula has been reported as intermediate hosts of many zoonotic trematodes. Here, we investigated the prevalence...

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Autores principales: Li, Jian, Ren, Yijing, Yang, Lei, Guo, Jiani, Chen, Haiying, Liu, Jiani, Tian, Haoqiang, Zhou, Qingan, Huang, Weiyi, Hu, Wei, Feng, Xinyu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9389801/
https://www.ncbi.nlm.nih.gov/pubmed/35986411
http://dx.doi.org/10.1186/s40249-022-01014-7
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author Li, Jian
Ren, Yijing
Yang, Lei
Guo, Jiani
Chen, Haiying
Liu, Jiani
Tian, Haoqiang
Zhou, Qingan
Huang, Weiyi
Hu, Wei
Feng, Xinyu
author_facet Li, Jian
Ren, Yijing
Yang, Lei
Guo, Jiani
Chen, Haiying
Liu, Jiani
Tian, Haoqiang
Zhou, Qingan
Huang, Weiyi
Hu, Wei
Feng, Xinyu
author_sort Li, Jian
collection PubMed
description BACKGROUND: Food-borne parasitic diseases decrease food safety and threaten public health. The snail species is an intermediate host for numerous human parasitic trematodes. Orientogalba ollula has been reported as intermediate hosts of many zoonotic trematodes. Here, we investigated the prevalence of zoonotic trematodes within O. ollula in Guangxi, China, and assessed their zoonotic potential. METHODS: Snails were collected from 54 sites in 9 cities throughout Guangxi. The snail and trematode larvae species were determined by combining morphological characteristics and molecular markers. The trematodes prevalence and constituent ratio were calculated and compared among different habitat environments. Phylogenetic trees of the trematode species were constructed using the neighbor-joining method with nuclear internal transcribed spacer 2 (ITS2) sequences. The developmental cycles of the isolated trematodes were examined by experimental infection in ducks. The developmental characteristics of Echinostoma revolutum was recorded by dissecting infected ducklings from 1-day post infection (dpi) to 10 dpi. RESULTS: The overall prevalence of trematode larvae was 22.1% (1818/8238) in O. ollula from 11 sample sites. Morphological together with molecular identification, showed that E. revolutum, Australapatemon sp., Hypoderaeum conoideum, Pharyngostomum cordatum, and Echinostoma sp. parasitized O. ollula, with the highest infection rate of E. revolutum (13.0%). However, no Fasciola larvae were detected. The trematodes prevalence and constituent ratio varied in two sub-biotypes (P < 0.01). A neighbor-joining tree analysis of ITS2 sequences resulted in distinct monophyletic clades supported by sequences from isolated larvae with high bootstrap values. Ducklings exposed to O. ollula infected with Echinostoma sp., E. revolutum, and H. conoideum larvae were successfully infected. The animal model for Echinostoma revolutum was successfully established. E. revolutum matured from larvae to adult at 10 dpi in the intestine of the duck, and the developmental characteristics of E. revolutum were characterized by the maturation of the reproductive and digestive organs at 6–8 dpi. CONCLUSIONS: This study revealed a high prevalence of zoonotic trematodes in O. ollula from Guangxi, China. Existing trematodes infection in animals and human clinical cases, coupled with the wide geographical distribution of O. ollula, necessitate further evaluations of the potential risk of spillover of zoonotic infection from animal to human and vice versa. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40249-022-01014-7.
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spelling pubmed-93898012022-08-20 A relatively high zoonotic trematode prevalence in Orientogalba ollula and the developmental characteristics of isolated trematodes by experimental infection in the animal model Li, Jian Ren, Yijing Yang, Lei Guo, Jiani Chen, Haiying Liu, Jiani Tian, Haoqiang Zhou, Qingan Huang, Weiyi Hu, Wei Feng, Xinyu Infect Dis Poverty Research Article BACKGROUND: Food-borne parasitic diseases decrease food safety and threaten public health. The snail species is an intermediate host for numerous human parasitic trematodes. Orientogalba ollula has been reported as intermediate hosts of many zoonotic trematodes. Here, we investigated the prevalence of zoonotic trematodes within O. ollula in Guangxi, China, and assessed their zoonotic potential. METHODS: Snails were collected from 54 sites in 9 cities throughout Guangxi. The snail and trematode larvae species were determined by combining morphological characteristics and molecular markers. The trematodes prevalence and constituent ratio were calculated and compared among different habitat environments. Phylogenetic trees of the trematode species were constructed using the neighbor-joining method with nuclear internal transcribed spacer 2 (ITS2) sequences. The developmental cycles of the isolated trematodes were examined by experimental infection in ducks. The developmental characteristics of Echinostoma revolutum was recorded by dissecting infected ducklings from 1-day post infection (dpi) to 10 dpi. RESULTS: The overall prevalence of trematode larvae was 22.1% (1818/8238) in O. ollula from 11 sample sites. Morphological together with molecular identification, showed that E. revolutum, Australapatemon sp., Hypoderaeum conoideum, Pharyngostomum cordatum, and Echinostoma sp. parasitized O. ollula, with the highest infection rate of E. revolutum (13.0%). However, no Fasciola larvae were detected. The trematodes prevalence and constituent ratio varied in two sub-biotypes (P < 0.01). A neighbor-joining tree analysis of ITS2 sequences resulted in distinct monophyletic clades supported by sequences from isolated larvae with high bootstrap values. Ducklings exposed to O. ollula infected with Echinostoma sp., E. revolutum, and H. conoideum larvae were successfully infected. The animal model for Echinostoma revolutum was successfully established. E. revolutum matured from larvae to adult at 10 dpi in the intestine of the duck, and the developmental characteristics of E. revolutum were characterized by the maturation of the reproductive and digestive organs at 6–8 dpi. CONCLUSIONS: This study revealed a high prevalence of zoonotic trematodes in O. ollula from Guangxi, China. Existing trematodes infection in animals and human clinical cases, coupled with the wide geographical distribution of O. ollula, necessitate further evaluations of the potential risk of spillover of zoonotic infection from animal to human and vice versa. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40249-022-01014-7. BioMed Central 2022-08-19 /pmc/articles/PMC9389801/ /pubmed/35986411 http://dx.doi.org/10.1186/s40249-022-01014-7 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Li, Jian
Ren, Yijing
Yang, Lei
Guo, Jiani
Chen, Haiying
Liu, Jiani
Tian, Haoqiang
Zhou, Qingan
Huang, Weiyi
Hu, Wei
Feng, Xinyu
A relatively high zoonotic trematode prevalence in Orientogalba ollula and the developmental characteristics of isolated trematodes by experimental infection in the animal model
title A relatively high zoonotic trematode prevalence in Orientogalba ollula and the developmental characteristics of isolated trematodes by experimental infection in the animal model
title_full A relatively high zoonotic trematode prevalence in Orientogalba ollula and the developmental characteristics of isolated trematodes by experimental infection in the animal model
title_fullStr A relatively high zoonotic trematode prevalence in Orientogalba ollula and the developmental characteristics of isolated trematodes by experimental infection in the animal model
title_full_unstemmed A relatively high zoonotic trematode prevalence in Orientogalba ollula and the developmental characteristics of isolated trematodes by experimental infection in the animal model
title_short A relatively high zoonotic trematode prevalence in Orientogalba ollula and the developmental characteristics of isolated trematodes by experimental infection in the animal model
title_sort relatively high zoonotic trematode prevalence in orientogalba ollula and the developmental characteristics of isolated trematodes by experimental infection in the animal model
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9389801/
https://www.ncbi.nlm.nih.gov/pubmed/35986411
http://dx.doi.org/10.1186/s40249-022-01014-7
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