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Inactivation of mixed Escherichia coli O157:H7 biofilms on lettuce by bacteriophage in combination with slightly acidic hypochlorous water (SAHW) and mild heat treatment
Escherichia coli O157:H7 is one of the most important foodborne pathogens that can persist in leafy green vegetables and subsequently produce biofilms. Biofilm formation is an ongoing concern in the food industry as biofilms are relatively resistant to a variety of antimicrobial treatments. In the p...
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Published in: | Food microbiology 2022-06, Vol.104, p.104010, Article 104010 |
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creator | Zhang, Yu Huang, Hung-Hsin Ma, Luyan Z. Masuda, Yoshimitsu Honjoh, Ken-ichi Miyamoto, Takahisa |
description | Escherichia coli O157:H7 is one of the most important foodborne pathogens that can persist in leafy green vegetables and subsequently produce biofilms. Biofilm formation is an ongoing concern in the food industry as biofilms are relatively resistant to a variety of antimicrobial treatments. In the present study, we evaluated the combined effects of phage FP43 and mild-heated slightly acidic hypochlorous water (SAHW) in reducing established biofilms on lettuce. Prior to the sequential treatments involving phage-SAHW and SAHW-phage for long-term storage, equal inoculum densities of E. coli O157:H7 and E. coli O91:H- were added on iceberg lettuce surfaces and the lettuce samples were stored at 10 °C for 48 h to allow biofilm formation. The sequential treatment with phage FP43 and SAHW significantly decreased the number of adhered cells, especially the combination of phage FP43 at 25 °C for 2 h and mild-heated SAHW, which considerably eliminated E. coli viable biofilm cells to undetectable levels (>3 log CFU/piece). However, the biofilms were not completely removed, as evidenced via SEM observation. Additionally, sequential treatment with SAHW and phage caused continuous reductions in viable counts, decreasing the viability of E. coli O157:H7 and total E. coli to the lower limit of detection after incubation for 5 d. Meanwhile, bacterial regrowth was observed after treatment with SAHW alone. These results indicated that the combination of phage and SAHW could be considered as a promising strategy to control the formation of E. coli O157:H7 biofilms on lettuce.
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•Phage FP43 and SAHW strongly decontaminated mixed E. coli biofilms on lettuce.•Sequential treatment by FP43 and 50 °C-SAHW showed higher antibiofilm activity.•Phage FP43 at 10 °C continuously reduced viability of SAHW-treated biofilm cells. |
doi_str_mv | 10.1016/j.fm.2022.104010 |
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[Display omitted]
•Phage FP43 and SAHW strongly decontaminated mixed E. coli biofilms on lettuce.•Sequential treatment by FP43 and 50 °C-SAHW showed higher antibiofilm activity.•Phage FP43 at 10 °C continuously reduced viability of SAHW-treated biofilm cells.</description><identifier>ISSN: 0740-0020</identifier><identifier>EISSN: 1095-9998</identifier><identifier>DOI: 10.1016/j.fm.2022.104010</identifier><identifier>PMID: 35287798</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>Bacteriophage ; Bacteriophages ; Biofilms ; Colony Count, Microbial ; Escherichia coli O157 ; Escherichia coli O157:H7 ; Food Microbiology ; Hot Temperature ; Lactuca - microbiology ; Lettuce ; Mild heat ; Mixed biofilm ; Slightly acidic hypochlorous water ; Water - pharmacology</subject><ispartof>Food microbiology, 2022-06, Vol.104, p.104010, Article 104010</ispartof><rights>2022 Elsevier Ltd</rights><rights>Copyright © 2022 Elsevier Ltd. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c392t-c02a59a2e197e8437c238f6792ef49d14983adfd4c79943ef23eb181f3a3d4963</citedby><cites>FETCH-LOGICAL-c392t-c02a59a2e197e8437c238f6792ef49d14983adfd4c79943ef23eb181f3a3d4963</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35287798$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhang, Yu</creatorcontrib><creatorcontrib>Huang, Hung-Hsin</creatorcontrib><creatorcontrib>Ma, Luyan Z.</creatorcontrib><creatorcontrib>Masuda, Yoshimitsu</creatorcontrib><creatorcontrib>Honjoh, Ken-ichi</creatorcontrib><creatorcontrib>Miyamoto, Takahisa</creatorcontrib><title>Inactivation of mixed Escherichia coli O157:H7 biofilms on lettuce by bacteriophage in combination with slightly acidic hypochlorous water (SAHW) and mild heat treatment</title><title>Food microbiology</title><addtitle>Food Microbiol</addtitle><description>Escherichia coli O157:H7 is one of the most important foodborne pathogens that can persist in leafy green vegetables and subsequently produce biofilms. Biofilm formation is an ongoing concern in the food industry as biofilms are relatively resistant to a variety of antimicrobial treatments. In the present study, we evaluated the combined effects of phage FP43 and mild-heated slightly acidic hypochlorous water (SAHW) in reducing established biofilms on lettuce. Prior to the sequential treatments involving phage-SAHW and SAHW-phage for long-term storage, equal inoculum densities of E. coli O157:H7 and E. coli O91:H- were added on iceberg lettuce surfaces and the lettuce samples were stored at 10 °C for 48 h to allow biofilm formation. The sequential treatment with phage FP43 and SAHW significantly decreased the number of adhered cells, especially the combination of phage FP43 at 25 °C for 2 h and mild-heated SAHW, which considerably eliminated E. coli viable biofilm cells to undetectable levels (>3 log CFU/piece). However, the biofilms were not completely removed, as evidenced via SEM observation. Additionally, sequential treatment with SAHW and phage caused continuous reductions in viable counts, decreasing the viability of E. coli O157:H7 and total E. coli to the lower limit of detection after incubation for 5 d. Meanwhile, bacterial regrowth was observed after treatment with SAHW alone. These results indicated that the combination of phage and SAHW could be considered as a promising strategy to control the formation of E. coli O157:H7 biofilms on lettuce.
[Display omitted]
•Phage FP43 and SAHW strongly decontaminated mixed E. coli biofilms on lettuce.•Sequential treatment by FP43 and 50 °C-SAHW showed higher antibiofilm activity.•Phage FP43 at 10 °C continuously reduced viability of SAHW-treated biofilm cells.</description><subject>Bacteriophage</subject><subject>Bacteriophages</subject><subject>Biofilms</subject><subject>Colony Count, Microbial</subject><subject>Escherichia coli O157</subject><subject>Escherichia coli O157:H7</subject><subject>Food Microbiology</subject><subject>Hot Temperature</subject><subject>Lactuca - microbiology</subject><subject>Lettuce</subject><subject>Mild heat</subject><subject>Mixed biofilm</subject><subject>Slightly acidic hypochlorous water</subject><subject>Water - pharmacology</subject><issn>0740-0020</issn><issn>1095-9998</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNp1kE1r3DAQhkVpaLZp7z0VHduDN_qwV1ZuIaTdQCCHtvQoZGkUz2Jbi6VNsj-p_zIKbnvLZYaB53kZXkI-cbbmjG_Od-swrgUTopw14-wNWXGmm0pr3b4lK6ZqVjEm2Cl5n9KOMc4bqd-RU9mIVindrsifm8m6jA82Y5xoDHTEJ_D0OrkeZnQ9WurigPSON-piq2iHMeAwJlroAXI-OKDdkXYlpPBx39t7oDgVaexwWlIfMfc0DXjf5-FIrUOPjvbHfXT9EOd4SPTRFpt--XG5_f2V2smXLwZPe7CZ5rnMEab8gZwEOyT4-HefkV_frn9ebavbu-83V5e3lZNa5MoxYRttBXCtoK2lckK2YaO0gFBrz2vdSuuDr53SupYQhISOtzxIK32tN_KMsCXXzTGlGYLZzzja-Wg4My-tm50Jo3lp3SytF-XzouwP3Qj-v_Cv5gJcLACUxx8QZpMcwuTA4wwuGx_x9fRnie-T1g</recordid><startdate>202206</startdate><enddate>202206</enddate><creator>Zhang, Yu</creator><creator>Huang, Hung-Hsin</creator><creator>Ma, Luyan Z.</creator><creator>Masuda, Yoshimitsu</creator><creator>Honjoh, Ken-ichi</creator><creator>Miyamoto, Takahisa</creator><general>Elsevier Ltd</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope></search><sort><creationdate>202206</creationdate><title>Inactivation of mixed Escherichia coli O157:H7 biofilms on lettuce by bacteriophage in combination with slightly acidic hypochlorous water (SAHW) and mild heat treatment</title><author>Zhang, Yu ; Huang, Hung-Hsin ; Ma, Luyan Z. ; Masuda, Yoshimitsu ; Honjoh, Ken-ichi ; Miyamoto, Takahisa</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c392t-c02a59a2e197e8437c238f6792ef49d14983adfd4c79943ef23eb181f3a3d4963</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Bacteriophage</topic><topic>Bacteriophages</topic><topic>Biofilms</topic><topic>Colony Count, Microbial</topic><topic>Escherichia coli O157</topic><topic>Escherichia coli O157:H7</topic><topic>Food Microbiology</topic><topic>Hot Temperature</topic><topic>Lactuca - microbiology</topic><topic>Lettuce</topic><topic>Mild heat</topic><topic>Mixed biofilm</topic><topic>Slightly acidic hypochlorous water</topic><topic>Water - pharmacology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhang, Yu</creatorcontrib><creatorcontrib>Huang, Hung-Hsin</creatorcontrib><creatorcontrib>Ma, Luyan Z.</creatorcontrib><creatorcontrib>Masuda, Yoshimitsu</creatorcontrib><creatorcontrib>Honjoh, Ken-ichi</creatorcontrib><creatorcontrib>Miyamoto, Takahisa</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><jtitle>Food microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhang, Yu</au><au>Huang, Hung-Hsin</au><au>Ma, Luyan Z.</au><au>Masuda, Yoshimitsu</au><au>Honjoh, Ken-ichi</au><au>Miyamoto, Takahisa</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Inactivation of mixed Escherichia coli O157:H7 biofilms on lettuce by bacteriophage in combination with slightly acidic hypochlorous water (SAHW) and mild heat treatment</atitle><jtitle>Food microbiology</jtitle><addtitle>Food Microbiol</addtitle><date>2022-06</date><risdate>2022</risdate><volume>104</volume><spage>104010</spage><pages>104010-</pages><artnum>104010</artnum><issn>0740-0020</issn><eissn>1095-9998</eissn><abstract>Escherichia coli O157:H7 is one of the most important foodborne pathogens that can persist in leafy green vegetables and subsequently produce biofilms. Biofilm formation is an ongoing concern in the food industry as biofilms are relatively resistant to a variety of antimicrobial treatments. In the present study, we evaluated the combined effects of phage FP43 and mild-heated slightly acidic hypochlorous water (SAHW) in reducing established biofilms on lettuce. Prior to the sequential treatments involving phage-SAHW and SAHW-phage for long-term storage, equal inoculum densities of E. coli O157:H7 and E. coli O91:H- were added on iceberg lettuce surfaces and the lettuce samples were stored at 10 °C for 48 h to allow biofilm formation. The sequential treatment with phage FP43 and SAHW significantly decreased the number of adhered cells, especially the combination of phage FP43 at 25 °C for 2 h and mild-heated SAHW, which considerably eliminated E. coli viable biofilm cells to undetectable levels (>3 log CFU/piece). However, the biofilms were not completely removed, as evidenced via SEM observation. Additionally, sequential treatment with SAHW and phage caused continuous reductions in viable counts, decreasing the viability of E. coli O157:H7 and total E. coli to the lower limit of detection after incubation for 5 d. Meanwhile, bacterial regrowth was observed after treatment with SAHW alone. These results indicated that the combination of phage and SAHW could be considered as a promising strategy to control the formation of E. coli O157:H7 biofilms on lettuce.
[Display omitted]
•Phage FP43 and SAHW strongly decontaminated mixed E. coli biofilms on lettuce.•Sequential treatment by FP43 and 50 °C-SAHW showed higher antibiofilm activity.•Phage FP43 at 10 °C continuously reduced viability of SAHW-treated biofilm cells.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>35287798</pmid><doi>10.1016/j.fm.2022.104010</doi><oa>free_for_read</oa></addata></record> |
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subjects | Bacteriophage Bacteriophages Biofilms Colony Count, Microbial Escherichia coli O157 Escherichia coli O157:H7 Food Microbiology Hot Temperature Lactuca - microbiology Lettuce Mild heat Mixed biofilm Slightly acidic hypochlorous water Water - pharmacology |
title | Inactivation of mixed Escherichia coli O157:H7 biofilms on lettuce by bacteriophage in combination with slightly acidic hypochlorous water (SAHW) and mild heat treatment |
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