Host Range-Associated Clustering Based on Multilocus Variable-Number Tandem-Repeat Analysis, Phylotypes, and Virulence Genes of Atypical Enteropathogenic Escherichia coli Strains

Atypical enteropathogenic (aEPEC) strains (36 Japanese and 50 Bangladeshi) obtained from 649 poultry fecal samples were analyzed by molecular epidemiological methods. Clermont's phylogenetic typing showed that group A was more prevalent (58%, 50/86) than B1 (31%, 27/86). Intimin type β1, which...

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Veröffentlicht in:Applied and environmental microbiology 2019-03, Vol.85 (6)
Hauptverfasser: Parvej, Md Shafiullah, Nakamura, Hiromi, Alam, Md Ashraful, Wang, Lili, Zhang, Shaobo, Emura, Kazuo, Kage-Nakadai, Eriko, Wada, Takayuki, Hara-Kudo, Yukiko, Nishikawa, Yoshikazu
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container_title Applied and environmental microbiology
container_volume 85
creator Parvej, Md Shafiullah
Nakamura, Hiromi
Alam, Md Ashraful
Wang, Lili
Zhang, Shaobo
Emura, Kazuo
Kage-Nakadai, Eriko
Wada, Takayuki
Hara-Kudo, Yukiko
Nishikawa, Yoshikazu
description Atypical enteropathogenic (aEPEC) strains (36 Japanese and 50 Bangladeshi) obtained from 649 poultry fecal samples were analyzed by molecular epidemiological methods. Clermont's phylogenetic typing showed that group A was more prevalent (58%, 50/86) than B1 (31%, 27/86). Intimin type β1, which is prevalent among human diarrheal patients, was predominant in both phylogroups B1 (81%, 22/27) and A (70%, 35/50). However, about 95% of B1-β1 strains belonged to virulence group I, and 77% of them were Japanese strains, while 17% (6/35) of A-β1 strains did. Multilocus variable-number tandem-repeat analysis (MLVA) distributed the strains into 52 distinct profiles, with Simpson's index of diversity (D) at 73%. When the data were combined with those of 142 previous strains from different sources, the minimum spanning tree formed five zones for porcine strains, poultry strains (excluding B1-β1), strains from healthy humans, bovine and human patient strains, and the B1-β1 poultry strains. Antimicrobial resistance to nalidixic acid was most common (74%) among the isolates. Sixty-eight percent of them demonstrated resistance to ≥3 antimicrobial agents, and most of them (91%) were from Bangladesh. The strains were assigned into two groups by hierarchical clustering. Correlation matrix analysis revealed that the virulence genes were negatively associated with antimicrobial resistance. The present study suggested that poultry, particularly Japanese poultry, could be another reservoir of aEPEC (phylogroup B1, virulence group I, and intimin type β1); however, poultry strains seem to be apart from patient strains that were closer to bovine strains. Bangladeshi aEPEC may be less virulent for humans but more resistant to antibiotics. Atypical enteropathogenic (aEPEC) is a diarrheagenic type of , as it possesses the intimin gene ( ) for attachment and effacement on epithelium. Since aEPEC is ubiquitous even in developed countries, we previously used molecular epidemiological methods to discriminate aEPEC as a human pathogen. The present study assessed poultry as another source of human diarrheagenic aEPEC. Poultry could be the source of aEPEC (phylogroup B1, virulence group I, and intimin type β1) found among patient strains in Japan. However, the minimum spanning tree (MST) suggested that the strains from Japanese poultry were far from Japanese patient strains compared with the distance between bovine and patient strains. Bangladeshi avian strains seemed to be less diarrheagenic
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Clermont's phylogenetic typing showed that group A was more prevalent (58%, 50/86) than B1 (31%, 27/86). Intimin type β1, which is prevalent among human diarrheal patients, was predominant in both phylogroups B1 (81%, 22/27) and A (70%, 35/50). However, about 95% of B1-β1 strains belonged to virulence group I, and 77% of them were Japanese strains, while 17% (6/35) of A-β1 strains did. Multilocus variable-number tandem-repeat analysis (MLVA) distributed the strains into 52 distinct profiles, with Simpson's index of diversity (D) at 73%. When the data were combined with those of 142 previous strains from different sources, the minimum spanning tree formed five zones for porcine strains, poultry strains (excluding B1-β1), strains from healthy humans, bovine and human patient strains, and the B1-β1 poultry strains. Antimicrobial resistance to nalidixic acid was most common (74%) among the isolates. Sixty-eight percent of them demonstrated resistance to ≥3 antimicrobial agents, and most of them (91%) were from Bangladesh. The strains were assigned into two groups by hierarchical clustering. Correlation matrix analysis revealed that the virulence genes were negatively associated with antimicrobial resistance. The present study suggested that poultry, particularly Japanese poultry, could be another reservoir of aEPEC (phylogroup B1, virulence group I, and intimin type β1); however, poultry strains seem to be apart from patient strains that were closer to bovine strains. Bangladeshi aEPEC may be less virulent for humans but more resistant to antibiotics. Atypical enteropathogenic (aEPEC) is a diarrheagenic type of , as it possesses the intimin gene ( ) for attachment and effacement on epithelium. Since aEPEC is ubiquitous even in developed countries, we previously used molecular epidemiological methods to discriminate aEPEC as a human pathogen. The present study assessed poultry as another source of human diarrheagenic aEPEC. Poultry could be the source of aEPEC (phylogroup B1, virulence group I, and intimin type β1) found among patient strains in Japan. However, the minimum spanning tree (MST) suggested that the strains from Japanese poultry were far from Japanese patient strains compared with the distance between bovine and patient strains. Bangladeshi avian strains seemed to be less diarrheagenic but are hazardous as a source of drug resistance genes.</description><identifier>ISSN: 0099-2240</identifier><identifier>EISSN: 1098-5336</identifier><identifier>DOI: 10.1128/AEM.02796-18</identifier><identifier>PMID: 30658974</identifier><language>eng</language><publisher>United States: American Society for Microbiology</publisher><subject>Acid resistance ; Animals ; Anti-Bacterial Agents - pharmacology ; Antibiotics ; Antiinfectives and antibacterials ; Antimicrobial agents ; Antimicrobial resistance ; Bacteria ; Bangladesh ; Cattle ; Cattle Diseases - microbiology ; Chickens ; Cluster analysis ; Clustering ; Coliforms ; Correlation analysis ; Developed countries ; Diarrhea ; Drug resistance ; Drug Resistance, Bacterial ; E coli ; Enteropathogenic Escherichia coli - classification ; Enteropathogenic Escherichia coli - drug effects ; Enteropathogenic Escherichia coli - genetics ; Enteropathogenic Escherichia coli - physiology ; Epidemiology ; Epithelium ; Escherichia coli ; Escherichia coli Infections - microbiology ; Escherichia coli Infections - veterinary ; Escherichia coli Proteins - genetics ; Escherichia coli Proteins - metabolism ; Genes ; Graph theory ; Host range ; Host Specificity ; Humans ; Intimin ; Japan ; Matrix methods ; Minisatellite Repeats ; Nalidixic acid ; Phylogeny ; Poultry ; Poultry Diseases - microbiology ; Public and Environmental Health Microbiology ; Swine ; Swine Diseases - microbiology ; Trees ; Typing ; Virulence ; Virulence Factors - genetics ; Virulence Factors - metabolism</subject><ispartof>Applied and environmental microbiology, 2019-03, Vol.85 (6)</ispartof><rights>Copyright © 2019 American Society for Microbiology.</rights><rights>Copyright American Society for Microbiology Mar 2019</rights><rights>Copyright © 2019 American Society for Microbiology. 2019 American Society for Microbiology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c478t-1ef949d63b1af868fa49b1af2108c012312c897a2543c93c7d400ec4137bcb613</citedby><cites>FETCH-LOGICAL-c478t-1ef949d63b1af868fa49b1af2108c012312c897a2543c93c7d400ec4137bcb613</cites><orcidid>0000-0002-7562-477X ; 0000-0002-0512-0656 ; 0000-0001-9453-0739</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6414391/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6414391/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,3175,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30658974$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Dudley, Edward G.</contributor><creatorcontrib>Parvej, Md Shafiullah</creatorcontrib><creatorcontrib>Nakamura, Hiromi</creatorcontrib><creatorcontrib>Alam, Md Ashraful</creatorcontrib><creatorcontrib>Wang, Lili</creatorcontrib><creatorcontrib>Zhang, Shaobo</creatorcontrib><creatorcontrib>Emura, Kazuo</creatorcontrib><creatorcontrib>Kage-Nakadai, Eriko</creatorcontrib><creatorcontrib>Wada, Takayuki</creatorcontrib><creatorcontrib>Hara-Kudo, Yukiko</creatorcontrib><creatorcontrib>Nishikawa, Yoshikazu</creatorcontrib><title>Host Range-Associated Clustering Based on Multilocus Variable-Number Tandem-Repeat Analysis, Phylotypes, and Virulence Genes of Atypical Enteropathogenic Escherichia coli Strains</title><title>Applied and environmental microbiology</title><addtitle>Appl Environ Microbiol</addtitle><description>Atypical enteropathogenic (aEPEC) strains (36 Japanese and 50 Bangladeshi) obtained from 649 poultry fecal samples were analyzed by molecular epidemiological methods. Clermont's phylogenetic typing showed that group A was more prevalent (58%, 50/86) than B1 (31%, 27/86). Intimin type β1, which is prevalent among human diarrheal patients, was predominant in both phylogroups B1 (81%, 22/27) and A (70%, 35/50). However, about 95% of B1-β1 strains belonged to virulence group I, and 77% of them were Japanese strains, while 17% (6/35) of A-β1 strains did. Multilocus variable-number tandem-repeat analysis (MLVA) distributed the strains into 52 distinct profiles, with Simpson's index of diversity (D) at 73%. When the data were combined with those of 142 previous strains from different sources, the minimum spanning tree formed five zones for porcine strains, poultry strains (excluding B1-β1), strains from healthy humans, bovine and human patient strains, and the B1-β1 poultry strains. Antimicrobial resistance to nalidixic acid was most common (74%) among the isolates. Sixty-eight percent of them demonstrated resistance to ≥3 antimicrobial agents, and most of them (91%) were from Bangladesh. The strains were assigned into two groups by hierarchical clustering. Correlation matrix analysis revealed that the virulence genes were negatively associated with antimicrobial resistance. The present study suggested that poultry, particularly Japanese poultry, could be another reservoir of aEPEC (phylogroup B1, virulence group I, and intimin type β1); however, poultry strains seem to be apart from patient strains that were closer to bovine strains. Bangladeshi aEPEC may be less virulent for humans but more resistant to antibiotics. Atypical enteropathogenic (aEPEC) is a diarrheagenic type of , as it possesses the intimin gene ( ) for attachment and effacement on epithelium. Since aEPEC is ubiquitous even in developed countries, we previously used molecular epidemiological methods to discriminate aEPEC as a human pathogen. The present study assessed poultry as another source of human diarrheagenic aEPEC. Poultry could be the source of aEPEC (phylogroup B1, virulence group I, and intimin type β1) found among patient strains in Japan. However, the minimum spanning tree (MST) suggested that the strains from Japanese poultry were far from Japanese patient strains compared with the distance between bovine and patient strains. Bangladeshi avian strains seemed to be less diarrheagenic but are hazardous as a source of drug resistance genes.</description><subject>Acid resistance</subject><subject>Animals</subject><subject>Anti-Bacterial Agents - pharmacology</subject><subject>Antibiotics</subject><subject>Antiinfectives and antibacterials</subject><subject>Antimicrobial agents</subject><subject>Antimicrobial resistance</subject><subject>Bacteria</subject><subject>Bangladesh</subject><subject>Cattle</subject><subject>Cattle Diseases - microbiology</subject><subject>Chickens</subject><subject>Cluster analysis</subject><subject>Clustering</subject><subject>Coliforms</subject><subject>Correlation analysis</subject><subject>Developed countries</subject><subject>Diarrhea</subject><subject>Drug resistance</subject><subject>Drug Resistance, Bacterial</subject><subject>E coli</subject><subject>Enteropathogenic Escherichia coli - classification</subject><subject>Enteropathogenic Escherichia coli - drug effects</subject><subject>Enteropathogenic Escherichia coli - genetics</subject><subject>Enteropathogenic Escherichia coli - physiology</subject><subject>Epidemiology</subject><subject>Epithelium</subject><subject>Escherichia coli</subject><subject>Escherichia coli Infections - microbiology</subject><subject>Escherichia coli Infections - veterinary</subject><subject>Escherichia coli Proteins - genetics</subject><subject>Escherichia coli Proteins - metabolism</subject><subject>Genes</subject><subject>Graph theory</subject><subject>Host range</subject><subject>Host Specificity</subject><subject>Humans</subject><subject>Intimin</subject><subject>Japan</subject><subject>Matrix methods</subject><subject>Minisatellite Repeats</subject><subject>Nalidixic acid</subject><subject>Phylogeny</subject><subject>Poultry</subject><subject>Poultry Diseases - microbiology</subject><subject>Public and Environmental Health Microbiology</subject><subject>Swine</subject><subject>Swine Diseases - microbiology</subject><subject>Trees</subject><subject>Typing</subject><subject>Virulence</subject><subject>Virulence Factors - 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pharmacology</topic><topic>Antibiotics</topic><topic>Antiinfectives and antibacterials</topic><topic>Antimicrobial agents</topic><topic>Antimicrobial resistance</topic><topic>Bacteria</topic><topic>Bangladesh</topic><topic>Cattle</topic><topic>Cattle Diseases - microbiology</topic><topic>Chickens</topic><topic>Cluster analysis</topic><topic>Clustering</topic><topic>Coliforms</topic><topic>Correlation analysis</topic><topic>Developed countries</topic><topic>Diarrhea</topic><topic>Drug resistance</topic><topic>Drug Resistance, Bacterial</topic><topic>E coli</topic><topic>Enteropathogenic Escherichia coli - classification</topic><topic>Enteropathogenic Escherichia coli - drug effects</topic><topic>Enteropathogenic Escherichia coli - genetics</topic><topic>Enteropathogenic Escherichia coli - physiology</topic><topic>Epidemiology</topic><topic>Epithelium</topic><topic>Escherichia coli</topic><topic>Escherichia coli Infections - microbiology</topic><topic>Escherichia coli Infections - veterinary</topic><topic>Escherichia coli Proteins - genetics</topic><topic>Escherichia coli Proteins - metabolism</topic><topic>Genes</topic><topic>Graph theory</topic><topic>Host range</topic><topic>Host Specificity</topic><topic>Humans</topic><topic>Intimin</topic><topic>Japan</topic><topic>Matrix methods</topic><topic>Minisatellite Repeats</topic><topic>Nalidixic acid</topic><topic>Phylogeny</topic><topic>Poultry</topic><topic>Poultry Diseases - microbiology</topic><topic>Public and Environmental Health Microbiology</topic><topic>Swine</topic><topic>Swine Diseases - microbiology</topic><topic>Trees</topic><topic>Typing</topic><topic>Virulence</topic><topic>Virulence Factors - genetics</topic><topic>Virulence Factors - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Parvej, Md Shafiullah</creatorcontrib><creatorcontrib>Nakamura, Hiromi</creatorcontrib><creatorcontrib>Alam, Md Ashraful</creatorcontrib><creatorcontrib>Wang, Lili</creatorcontrib><creatorcontrib>Zhang, Shaobo</creatorcontrib><creatorcontrib>Emura, Kazuo</creatorcontrib><creatorcontrib>Kage-Nakadai, Eriko</creatorcontrib><creatorcontrib>Wada, Takayuki</creatorcontrib><creatorcontrib>Hara-Kudo, Yukiko</creatorcontrib><creatorcontrib>Nishikawa, Yoshikazu</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Applied and environmental microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Parvej, Md Shafiullah</au><au>Nakamura, Hiromi</au><au>Alam, Md Ashraful</au><au>Wang, Lili</au><au>Zhang, Shaobo</au><au>Emura, Kazuo</au><au>Kage-Nakadai, Eriko</au><au>Wada, Takayuki</au><au>Hara-Kudo, Yukiko</au><au>Nishikawa, Yoshikazu</au><au>Dudley, Edward G.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Host Range-Associated Clustering Based on Multilocus Variable-Number Tandem-Repeat Analysis, Phylotypes, and Virulence Genes of Atypical Enteropathogenic Escherichia coli Strains</atitle><jtitle>Applied and environmental microbiology</jtitle><addtitle>Appl Environ Microbiol</addtitle><date>2019-03-15</date><risdate>2019</risdate><volume>85</volume><issue>6</issue><issn>0099-2240</issn><eissn>1098-5336</eissn><abstract>Atypical enteropathogenic (aEPEC) strains (36 Japanese and 50 Bangladeshi) obtained from 649 poultry fecal samples were analyzed by molecular epidemiological methods. Clermont's phylogenetic typing showed that group A was more prevalent (58%, 50/86) than B1 (31%, 27/86). Intimin type β1, which is prevalent among human diarrheal patients, was predominant in both phylogroups B1 (81%, 22/27) and A (70%, 35/50). However, about 95% of B1-β1 strains belonged to virulence group I, and 77% of them were Japanese strains, while 17% (6/35) of A-β1 strains did. Multilocus variable-number tandem-repeat analysis (MLVA) distributed the strains into 52 distinct profiles, with Simpson's index of diversity (D) at 73%. When the data were combined with those of 142 previous strains from different sources, the minimum spanning tree formed five zones for porcine strains, poultry strains (excluding B1-β1), strains from healthy humans, bovine and human patient strains, and the B1-β1 poultry strains. Antimicrobial resistance to nalidixic acid was most common (74%) among the isolates. Sixty-eight percent of them demonstrated resistance to ≥3 antimicrobial agents, and most of them (91%) were from Bangladesh. The strains were assigned into two groups by hierarchical clustering. Correlation matrix analysis revealed that the virulence genes were negatively associated with antimicrobial resistance. The present study suggested that poultry, particularly Japanese poultry, could be another reservoir of aEPEC (phylogroup B1, virulence group I, and intimin type β1); however, poultry strains seem to be apart from patient strains that were closer to bovine strains. Bangladeshi aEPEC may be less virulent for humans but more resistant to antibiotics. Atypical enteropathogenic (aEPEC) is a diarrheagenic type of , as it possesses the intimin gene ( ) for attachment and effacement on epithelium. Since aEPEC is ubiquitous even in developed countries, we previously used molecular epidemiological methods to discriminate aEPEC as a human pathogen. The present study assessed poultry as another source of human diarrheagenic aEPEC. Poultry could be the source of aEPEC (phylogroup B1, virulence group I, and intimin type β1) found among patient strains in Japan. However, the minimum spanning tree (MST) suggested that the strains from Japanese poultry were far from Japanese patient strains compared with the distance between bovine and patient strains. Bangladeshi avian strains seemed to be less diarrheagenic but are hazardous as a source of drug resistance genes.</abstract><cop>United States</cop><pub>American Society for Microbiology</pub><pmid>30658974</pmid><doi>10.1128/AEM.02796-18</doi><orcidid>https://orcid.org/0000-0002-7562-477X</orcidid><orcidid>https://orcid.org/0000-0002-0512-0656</orcidid><orcidid>https://orcid.org/0000-0001-9453-0739</orcidid><oa>free_for_read</oa></addata></record>
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source American Society for Microbiology; MEDLINE; PubMed Central; Alma/SFX Local Collection
subjects Acid resistance
Animals
Anti-Bacterial Agents - pharmacology
Antibiotics
Antiinfectives and antibacterials
Antimicrobial agents
Antimicrobial resistance
Bacteria
Bangladesh
Cattle
Cattle Diseases - microbiology
Chickens
Cluster analysis
Clustering
Coliforms
Correlation analysis
Developed countries
Diarrhea
Drug resistance
Drug Resistance, Bacterial
E coli
Enteropathogenic Escherichia coli - classification
Enteropathogenic Escherichia coli - drug effects
Enteropathogenic Escherichia coli - genetics
Enteropathogenic Escherichia coli - physiology
Epidemiology
Epithelium
Escherichia coli
Escherichia coli Infections - microbiology
Escherichia coli Infections - veterinary
Escherichia coli Proteins - genetics
Escherichia coli Proteins - metabolism
Genes
Graph theory
Host range
Host Specificity
Humans
Intimin
Japan
Matrix methods
Minisatellite Repeats
Nalidixic acid
Phylogeny
Poultry
Poultry Diseases - microbiology
Public and Environmental Health Microbiology
Swine
Swine Diseases - microbiology
Trees
Typing
Virulence
Virulence Factors - genetics
Virulence Factors - metabolism
title Host Range-Associated Clustering Based on Multilocus Variable-Number Tandem-Repeat Analysis, Phylotypes, and Virulence Genes of Atypical Enteropathogenic Escherichia coli Strains
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