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Public health implications of Yersinia enterocolitica investigation: an ecological modeling and molecular epidemiology study

BACKGROUND: Yersinia enterocolitica has been sporadically recovered from animals, foods, and human clinical samples in various regions of Ningxia, China. However, the ecological and molecular characteristics of Y. enterocolitica, as well as public health concerns about infection in the Ningxia Hui A...

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Autores principales: Yue, Yuan, Zheng, Jinxin, Sheng, Mei, Liu, Xiang, Hao, Qiong, Zhang, Shunxian, Xu, Shuai, Liu, Zhiguo, Hou, Xuexin, Jing, Huaiqi, Liu, Yang, Zhou, Xuezhang, Li, Zhenjun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10120104/
https://www.ncbi.nlm.nih.gov/pubmed/37085902
http://dx.doi.org/10.1186/s40249-023-01063-6
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author Yue, Yuan
Zheng, Jinxin
Sheng, Mei
Liu, Xiang
Hao, Qiong
Zhang, Shunxian
Xu, Shuai
Liu, Zhiguo
Hou, Xuexin
Jing, Huaiqi
Liu, Yang
Zhou, Xuezhang
Li, Zhenjun
author_facet Yue, Yuan
Zheng, Jinxin
Sheng, Mei
Liu, Xiang
Hao, Qiong
Zhang, Shunxian
Xu, Shuai
Liu, Zhiguo
Hou, Xuexin
Jing, Huaiqi
Liu, Yang
Zhou, Xuezhang
Li, Zhenjun
author_sort Yue, Yuan
collection PubMed
description BACKGROUND: Yersinia enterocolitica has been sporadically recovered from animals, foods, and human clinical samples in various regions of Ningxia, China. However, the ecological and molecular characteristics of Y. enterocolitica, as well as public health concerns about infection in the Ningxia Hui Autonomous Region, remain unclear. This study aims to analyze the ecological and molecular epidemiological characteristics of Y. enterocolitis in order to inform the public health intervention strategies for the contains of related diseases. METHODS: A total of 270 samples were collected for isolation [animals (n = 208), food (n = 49), and patients (n = 13)], then suspect colonies were isolated and identified by the API20E biochemical identification system, serological tests, biotyping tests, and 16S rRNA-PCR. Then, we used an ecological epidemiological approach combined with machine learning algorithms (general linear model, random forest model, and eXtreme Gradient Boosting) to explore the associations between ecological factors and the pathogenicity of Y. enterocolitis. Furthermore, average nucleotide identity (ANI) estimation, single nucleotide polymorphism (SNP), and core gene multilocus sequence typing (cgMLST) were applied to characterize the molecular profile of isolates based on whole genome sequencing. The statistical test used single-factor analysis, Chi-square tests, t-tests/ANOVA-tests, Wilcoxon rank-sum tests, and Kruskal–Wallis tests. RESULTS: A total of 270 isolates of Yersinia were identified from poultry and livestock (n = 191), food (n = 49), diarrhoea patients (n = 13), rats (n = 15), and hamsters (n = 2). The detection rates of samples from different hosts were statistically different (χ(2) = 22.636, P < 0.001). According to the relatedness clustering results, 270 isolates were divided into 12 species, and Y. enterocolitica (n = 187) is a predominated species. Pathogenic isolates made up 52.4% (98/187), while non-pathogenic isolates made up 47.6% (89/187). Temperature and precipitation were strongly associated with the pathogenicity of the isolates (P < 0.001). The random forest (RF) prediction model showed the best performance. The prediction result shows a high risk of pathogenicity Y. enterocolitica was located in the northern, northwestern, and southern of the Ningxia Hui Autonomous Region. The Y. enterocolitica isolates were classified into 54 sequence types (STs) and 125 cgMLST types (CTs), with 4/O:3 being the dominant bioserotype in Ningxia. The dominant STs and dominant CTs of pathogenic isolates in Ningxia were ST429 and HC100_2571, respectively. CONCLUSIONS: The data indicated geographical variations in the distribution of STs and CTs of Y. enterocolitica isolates in Ningxia. Our work offered the first evidence that the pathogenicity of isolates was directly related to fluctuations in temperature and precipitation of the environment. CgMLST typing strategies showed that the isolates were transmitted to the population via pigs and food. Therefore, strengthening health surveillance on pig farms in high-risk areas and focusing on testing food of pig origin are optional strategies to prevent disease outbreaks. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40249-023-01063-6.
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spelling pubmed-101201042023-04-22 Public health implications of Yersinia enterocolitica investigation: an ecological modeling and molecular epidemiology study Yue, Yuan Zheng, Jinxin Sheng, Mei Liu, Xiang Hao, Qiong Zhang, Shunxian Xu, Shuai Liu, Zhiguo Hou, Xuexin Jing, Huaiqi Liu, Yang Zhou, Xuezhang Li, Zhenjun Infect Dis Poverty Research Article BACKGROUND: Yersinia enterocolitica has been sporadically recovered from animals, foods, and human clinical samples in various regions of Ningxia, China. However, the ecological and molecular characteristics of Y. enterocolitica, as well as public health concerns about infection in the Ningxia Hui Autonomous Region, remain unclear. This study aims to analyze the ecological and molecular epidemiological characteristics of Y. enterocolitis in order to inform the public health intervention strategies for the contains of related diseases. METHODS: A total of 270 samples were collected for isolation [animals (n = 208), food (n = 49), and patients (n = 13)], then suspect colonies were isolated and identified by the API20E biochemical identification system, serological tests, biotyping tests, and 16S rRNA-PCR. Then, we used an ecological epidemiological approach combined with machine learning algorithms (general linear model, random forest model, and eXtreme Gradient Boosting) to explore the associations between ecological factors and the pathogenicity of Y. enterocolitis. Furthermore, average nucleotide identity (ANI) estimation, single nucleotide polymorphism (SNP), and core gene multilocus sequence typing (cgMLST) were applied to characterize the molecular profile of isolates based on whole genome sequencing. The statistical test used single-factor analysis, Chi-square tests, t-tests/ANOVA-tests, Wilcoxon rank-sum tests, and Kruskal–Wallis tests. RESULTS: A total of 270 isolates of Yersinia were identified from poultry and livestock (n = 191), food (n = 49), diarrhoea patients (n = 13), rats (n = 15), and hamsters (n = 2). The detection rates of samples from different hosts were statistically different (χ(2) = 22.636, P < 0.001). According to the relatedness clustering results, 270 isolates were divided into 12 species, and Y. enterocolitica (n = 187) is a predominated species. Pathogenic isolates made up 52.4% (98/187), while non-pathogenic isolates made up 47.6% (89/187). Temperature and precipitation were strongly associated with the pathogenicity of the isolates (P < 0.001). The random forest (RF) prediction model showed the best performance. The prediction result shows a high risk of pathogenicity Y. enterocolitica was located in the northern, northwestern, and southern of the Ningxia Hui Autonomous Region. The Y. enterocolitica isolates were classified into 54 sequence types (STs) and 125 cgMLST types (CTs), with 4/O:3 being the dominant bioserotype in Ningxia. The dominant STs and dominant CTs of pathogenic isolates in Ningxia were ST429 and HC100_2571, respectively. CONCLUSIONS: The data indicated geographical variations in the distribution of STs and CTs of Y. enterocolitica isolates in Ningxia. Our work offered the first evidence that the pathogenicity of isolates was directly related to fluctuations in temperature and precipitation of the environment. CgMLST typing strategies showed that the isolates were transmitted to the population via pigs and food. Therefore, strengthening health surveillance on pig farms in high-risk areas and focusing on testing food of pig origin are optional strategies to prevent disease outbreaks. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40249-023-01063-6. BioMed Central 2023-04-21 /pmc/articles/PMC10120104/ /pubmed/37085902 http://dx.doi.org/10.1186/s40249-023-01063-6 Text en © The Author(s) 2023 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
Yue, Yuan
Zheng, Jinxin
Sheng, Mei
Liu, Xiang
Hao, Qiong
Zhang, Shunxian
Xu, Shuai
Liu, Zhiguo
Hou, Xuexin
Jing, Huaiqi
Liu, Yang
Zhou, Xuezhang
Li, Zhenjun
Public health implications of Yersinia enterocolitica investigation: an ecological modeling and molecular epidemiology study
title Public health implications of Yersinia enterocolitica investigation: an ecological modeling and molecular epidemiology study
title_full Public health implications of Yersinia enterocolitica investigation: an ecological modeling and molecular epidemiology study
title_fullStr Public health implications of Yersinia enterocolitica investigation: an ecological modeling and molecular epidemiology study
title_full_unstemmed Public health implications of Yersinia enterocolitica investigation: an ecological modeling and molecular epidemiology study
title_short Public health implications of Yersinia enterocolitica investigation: an ecological modeling and molecular epidemiology study
title_sort public health implications of yersinia enterocolitica investigation: an ecological modeling and molecular epidemiology study
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10120104/
https://www.ncbi.nlm.nih.gov/pubmed/37085902
http://dx.doi.org/10.1186/s40249-023-01063-6
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