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Photodynamic and antibiotic therapy impair the pathogenesis of Enterococcus faecium in a whole animal insect model
Enterococcus faecium has emerged as one of the most important pathogens in healthcare-associated infections worldwide due to its intrinsic and acquired resistance to many antibiotics, including vancomycin. Antimicrobial photodynamic therapy (aPDT) is an alternative therapeutic platform that is curre...
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| Published in: | PloS one 2013-02, Vol.8 (2), p.e55926-e55926 |
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| creator | Chibebe Junior, José Fuchs, Beth B Sabino, Caetano P Junqueira, Juliana C Jorge, Antonio O C Ribeiro, Martha S Gilmore, Michael S Rice, Louis B Tegos, George P Hamblin, Michael R Mylonakis, Eleftherios |
| description | Enterococcus faecium has emerged as one of the most important pathogens in healthcare-associated infections worldwide due to its intrinsic and acquired resistance to many antibiotics, including vancomycin. Antimicrobial photodynamic therapy (aPDT) is an alternative therapeutic platform that is currently under investigation for the control and treatment of infections. PDT is based on the use of photoactive dye molecules, widely known as photosensitizer (PS). PS, upon irradiation with visible light, produces reactive oxygen species that can destroy lipids and proteins causing cell death. We employed Galleria mellonella (the greater wax moth) caterpillar fatally infected with E. faecium to develop an invertebrate host model system that can be used to study the antimicrobial PDT (alone or combined with antibiotics). In the establishment of infection by E. faecium in G. mellonella, we found that the G. mellonella death rate was dependent on the number of bacterial cells injected into the insect hemocoel and all E. faecium strains tested were capable of infecting and killing G. mellonella. Antibiotic treatment with ampicillin, gentamicin or the combination of ampicillin and gentamicin prolonged caterpillar survival infected by E. faecium (P = 0.0003, P = 0.0001 and P = 0.0001, respectively). In the study of antimicrobial PDT, we verified that methylene blue (MB) injected into the insect followed by whole body illumination prolonged the caterpillar survival (P = 0.0192). Interestingly, combination therapy of larvae infected with vancomycin-resistant E. faecium, with antimicrobial PDT followed by vancomycin, significantly prolonged the survival of the caterpillars when compared to either antimicrobial PDT (P = 0.0095) or vancomycin treatment alone (P = 0.0025), suggesting that the aPDT made the vancomycin resistant E. faecium strain more susceptible to vancomycin action. In summary, G. mellonella provides an invertebrate model host to study the antimicrobial PDT and to explore combinatorial aPDT-based treatments. |
| doi_str_mv | 10.1371/journal.pone.0055926 |
| format | article |
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Antimicrobial photodynamic therapy (aPDT) is an alternative therapeutic platform that is currently under investigation for the control and treatment of infections. PDT is based on the use of photoactive dye molecules, widely known as photosensitizer (PS). PS, upon irradiation with visible light, produces reactive oxygen species that can destroy lipids and proteins causing cell death. We employed Galleria mellonella (the greater wax moth) caterpillar fatally infected with E. faecium to develop an invertebrate host model system that can be used to study the antimicrobial PDT (alone or combined with antibiotics). In the establishment of infection by E. faecium in G. mellonella, we found that the G. mellonella death rate was dependent on the number of bacterial cells injected into the insect hemocoel and all E. faecium strains tested were capable of infecting and killing G. mellonella. Antibiotic treatment with ampicillin, gentamicin or the combination of ampicillin and gentamicin prolonged caterpillar survival infected by E. faecium (P = 0.0003, P = 0.0001 and P = 0.0001, respectively). In the study of antimicrobial PDT, we verified that methylene blue (MB) injected into the insect followed by whole body illumination prolonged the caterpillar survival (P = 0.0192). Interestingly, combination therapy of larvae infected with vancomycin-resistant E. faecium, with antimicrobial PDT followed by vancomycin, significantly prolonged the survival of the caterpillars when compared to either antimicrobial PDT (P = 0.0095) or vancomycin treatment alone (P = 0.0025), suggesting that the aPDT made the vancomycin resistant E. faecium strain more susceptible to vancomycin action. In summary, G. mellonella provides an invertebrate model host to study the antimicrobial PDT and to explore combinatorial aPDT-based treatments.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0055926</identifier><identifier>PMID: 23457486</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Aminoglycosides ; Ampicillin ; Analysis ; Animals ; Anti-Bacterial Agents - therapeutic use ; Antibiotic resistance ; Antibiotics ; Antiinfectives and antibacterials ; Bacteria ; Biology ; Butterflies & moths ; Candida albicans ; Caterpillars ; Cell death ; Combinatorial analysis ; Cross infection ; Dentistry ; Dermatology ; Disease Models, Animal ; Drug therapy ; Enterococcus faecalis ; Enterococcus faecium ; Enterococcus faecium - drug effects ; Enterococcus faecium - radiation effects ; Galleria mellonella ; Gentamicin ; Gram-Positive Bacterial Infections - drug therapy ; Health aspects ; Health care ; Hemocoel ; Hospitals ; Infection control ; Infections ; Infectious diseases ; Insects ; Irradiation ; Killing ; Larvae ; Light ; Lipids ; Medical schools ; Medicine ; Methylene blue ; Methylene Blue - therapeutic use ; Microbial drug resistance ; Moths ; Moths - microbiology ; Moths - radiation effects ; Nosocomial infections ; Oxygen ; Pathogenesis ; Photochemotherapy ; Photodynamic therapy ; Photosensitizing Agents - therapeutic use ; Proteins ; Radiation ; Reactive oxygen species ; Regulatory approval ; Staphylococcus aureus ; Survival ; Vancomycin</subject><ispartof>PloS one, 2013-02, Vol.8 (2), p.e55926-e55926</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013. This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c758t-257e886c3b9580029c88d17670afe872f1ac776eba4aa91831c31011855a7fa23</citedby><cites>FETCH-LOGICAL-c758t-257e886c3b9580029c88d17670afe872f1ac776eba4aa91831c31011855a7fa23</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/1331690776/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/1331690776?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,315,733,786,790,891,25783,27957,27958,37047,37048,44625,53827,53829,75483</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23457486$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Msadek, Tarek</contributor><creatorcontrib>Chibebe Junior, José</creatorcontrib><creatorcontrib>Fuchs, Beth B</creatorcontrib><creatorcontrib>Sabino, Caetano P</creatorcontrib><creatorcontrib>Junqueira, Juliana C</creatorcontrib><creatorcontrib>Jorge, Antonio O C</creatorcontrib><creatorcontrib>Ribeiro, Martha S</creatorcontrib><creatorcontrib>Gilmore, Michael S</creatorcontrib><creatorcontrib>Rice, Louis B</creatorcontrib><creatorcontrib>Tegos, George P</creatorcontrib><creatorcontrib>Hamblin, Michael R</creatorcontrib><creatorcontrib>Mylonakis, Eleftherios</creatorcontrib><title>Photodynamic and antibiotic therapy impair the pathogenesis of Enterococcus faecium in a whole animal insect model</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Enterococcus faecium has emerged as one of the most important pathogens in healthcare-associated infections worldwide due to its intrinsic and acquired resistance to many antibiotics, including vancomycin. Antimicrobial photodynamic therapy (aPDT) is an alternative therapeutic platform that is currently under investigation for the control and treatment of infections. PDT is based on the use of photoactive dye molecules, widely known as photosensitizer (PS). PS, upon irradiation with visible light, produces reactive oxygen species that can destroy lipids and proteins causing cell death. We employed Galleria mellonella (the greater wax moth) caterpillar fatally infected with E. faecium to develop an invertebrate host model system that can be used to study the antimicrobial PDT (alone or combined with antibiotics). In the establishment of infection by E. faecium in G. mellonella, we found that the G. mellonella death rate was dependent on the number of bacterial cells injected into the insect hemocoel and all E. faecium strains tested were capable of infecting and killing G. mellonella. Antibiotic treatment with ampicillin, gentamicin or the combination of ampicillin and gentamicin prolonged caterpillar survival infected by E. faecium (P = 0.0003, P = 0.0001 and P = 0.0001, respectively). In the study of antimicrobial PDT, we verified that methylene blue (MB) injected into the insect followed by whole body illumination prolonged the caterpillar survival (P = 0.0192). Interestingly, combination therapy of larvae infected with vancomycin-resistant E. faecium, with antimicrobial PDT followed by vancomycin, significantly prolonged the survival of the caterpillars when compared to either antimicrobial PDT (P = 0.0095) or vancomycin treatment alone (P = 0.0025), suggesting that the aPDT made the vancomycin resistant E. faecium strain more susceptible to vancomycin action. In summary, G. mellonella provides an invertebrate model host to study the antimicrobial PDT and to explore combinatorial aPDT-based treatments.</description><subject>Aminoglycosides</subject><subject>Ampicillin</subject><subject>Analysis</subject><subject>Animals</subject><subject>Anti-Bacterial Agents - therapeutic use</subject><subject>Antibiotic resistance</subject><subject>Antibiotics</subject><subject>Antiinfectives and antibacterials</subject><subject>Bacteria</subject><subject>Biology</subject><subject>Butterflies & moths</subject><subject>Candida albicans</subject><subject>Caterpillars</subject><subject>Cell death</subject><subject>Combinatorial analysis</subject><subject>Cross infection</subject><subject>Dentistry</subject><subject>Dermatology</subject><subject>Disease Models, Animal</subject><subject>Drug therapy</subject><subject>Enterococcus faecalis</subject><subject>Enterococcus faecium</subject><subject>Enterococcus faecium - drug effects</subject><subject>Enterococcus faecium - radiation effects</subject><subject>Galleria mellonella</subject><subject>Gentamicin</subject><subject>Gram-Positive Bacterial Infections - drug therapy</subject><subject>Health aspects</subject><subject>Health care</subject><subject>Hemocoel</subject><subject>Hospitals</subject><subject>Infection control</subject><subject>Infections</subject><subject>Infectious diseases</subject><subject>Insects</subject><subject>Irradiation</subject><subject>Killing</subject><subject>Larvae</subject><subject>Light</subject><subject>Lipids</subject><subject>Medical schools</subject><subject>Medicine</subject><subject>Methylene blue</subject><subject>Methylene Blue - therapeutic use</subject><subject>Microbial drug resistance</subject><subject>Moths</subject><subject>Moths - microbiology</subject><subject>Moths - radiation effects</subject><subject>Nosocomial infections</subject><subject>Oxygen</subject><subject>Pathogenesis</subject><subject>Photochemotherapy</subject><subject>Photodynamic therapy</subject><subject>Photosensitizing Agents - therapeutic use</subject><subject>Proteins</subject><subject>Radiation</subject><subject>Reactive oxygen species</subject><subject>Regulatory approval</subject><subject>Staphylococcus aureus</subject><subject>Survival</subject><subject>Vancomycin</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNqNk12L1DAUhoso7rr6D0QLgujFjPlok_RGWJZVBxZW_LoNp2kyzdA23SRV59-bcbrLjOyFlNLm5HnfJCfnZNlzjJaYcvxu4yY_QLcc3aCXCJVlRdiD7BRXlCwYQfThwf9J9iSETYKoYOxxdkJoUfJCsNPMf25ddM12gN6qHIYmvdHW1sU0jK32MG5z249g_W6YjxBbt9aDDjbkzuSXQ9TeKafUFHIDWtmpz-2QQ_6rdZ1ObraHLkWCVjHvXaO7p9kjA13Qz-bvWfb9w-W3i0-Lq-uPq4vzq4XipYgLUnItBFO0rkqBEKmUEA3mjCMwWnBiMCjOma6hAKiwoFhRjDAWZQncAKFn2cu979i5IOd0BYkpxaxCSZqI1Z5oHGzk6NNW_VY6sPJvwPm1BJ8S0WnJKsw0MTXDBBVlqQA3BmpGSlHVBpsieb2fV5vqXjdKD9FDd2R6PDPYVq7dT0lLThEVyeDNbODdzaRDlL0NSncdDNpNu33jgiNekR366h_0_tPN1BrSAexgXFpX7UzlecEFESyVR6KW91DpaXSqiFRbxqb4keDtkSAxUf-Oa5hCkKuvX_6fvf5xzL4-YFsNXWyD66Zo3RCOwWIPKu9C8NrcJRkjuWuN22zIXWvIuTWS7MXhBd2JbnuB_gESIwmV</recordid><startdate>20130214</startdate><enddate>20130214</enddate><creator>Chibebe Junior, José</creator><creator>Fuchs, Beth B</creator><creator>Sabino, Caetano P</creator><creator>Junqueira, Juliana C</creator><creator>Jorge, Antonio O C</creator><creator>Ribeiro, Martha S</creator><creator>Gilmore, Michael S</creator><creator>Rice, Louis B</creator><creator>Tegos, George P</creator><creator>Hamblin, Michael R</creator><creator>Mylonakis, Eleftherios</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20130214</creationdate><title>Photodynamic and antibiotic therapy impair the pathogenesis of Enterococcus faecium in a whole animal insect model</title><author>Chibebe Junior, José ; Fuchs, Beth B ; Sabino, Caetano P ; Junqueira, Juliana C ; Jorge, Antonio O C ; Ribeiro, Martha S ; Gilmore, Michael S ; Rice, Louis B ; Tegos, George P ; Hamblin, Michael R ; Mylonakis, Eleftherios</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c758t-257e886c3b9580029c88d17670afe872f1ac776eba4aa91831c31011855a7fa23</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Aminoglycosides</topic><topic>Ampicillin</topic><topic>Analysis</topic><topic>Animals</topic><topic>Anti-Bacterial Agents - 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Academic</collection><collection>ProQuest Engineering Collection</collection><collection>Biological Sciences</collection><collection>Agricultural Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Engineering Database</collection><collection>Nursing & Allied Health Premium</collection><collection>Advanced Technologies & Aerospace Database</collection><collection>ProQuest Advanced Technologies & Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials Science Collection</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>Directory of Open Access Journals (DOAJ)</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Chibebe Junior, José</au><au>Fuchs, Beth B</au><au>Sabino, Caetano P</au><au>Junqueira, Juliana C</au><au>Jorge, Antonio O C</au><au>Ribeiro, Martha S</au><au>Gilmore, Michael S</au><au>Rice, Louis B</au><au>Tegos, George P</au><au>Hamblin, Michael R</au><au>Mylonakis, Eleftherios</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Photodynamic and antibiotic therapy impair the pathogenesis of Enterococcus faecium in a whole animal insect model</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2013-02-14</date><risdate>2013</risdate><volume>8</volume><issue>2</issue><spage>e55926</spage><epage>e55926</epage><pages>e55926-e55926</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><notes>Competing Interests: The authors have declared that no competing interests exist.</notes><notes>Conceived and designed the experiments: J. Chibebe Junior BBF CPS J.C. Junqueira MRH EM. Performed the experiments: J. Chibebe Junior BBF CPS. Analyzed the data: J. Chibebe Junior J.C. Junqueira AOCJ MSR. Contributed reagents/materials/analysis tools: MSG LBR MRH. Wrote the paper: J. Chibebe Junior CPS J.C. Junqueira MRH GT EM.</notes><abstract>Enterococcus faecium has emerged as one of the most important pathogens in healthcare-associated infections worldwide due to its intrinsic and acquired resistance to many antibiotics, including vancomycin. Antimicrobial photodynamic therapy (aPDT) is an alternative therapeutic platform that is currently under investigation for the control and treatment of infections. PDT is based on the use of photoactive dye molecules, widely known as photosensitizer (PS). PS, upon irradiation with visible light, produces reactive oxygen species that can destroy lipids and proteins causing cell death. We employed Galleria mellonella (the greater wax moth) caterpillar fatally infected with E. faecium to develop an invertebrate host model system that can be used to study the antimicrobial PDT (alone or combined with antibiotics). In the establishment of infection by E. faecium in G. mellonella, we found that the G. mellonella death rate was dependent on the number of bacterial cells injected into the insect hemocoel and all E. faecium strains tested were capable of infecting and killing G. mellonella. Antibiotic treatment with ampicillin, gentamicin or the combination of ampicillin and gentamicin prolonged caterpillar survival infected by E. faecium (P = 0.0003, P = 0.0001 and P = 0.0001, respectively). In the study of antimicrobial PDT, we verified that methylene blue (MB) injected into the insect followed by whole body illumination prolonged the caterpillar survival (P = 0.0192). Interestingly, combination therapy of larvae infected with vancomycin-resistant E. faecium, with antimicrobial PDT followed by vancomycin, significantly prolonged the survival of the caterpillars when compared to either antimicrobial PDT (P = 0.0095) or vancomycin treatment alone (P = 0.0025), suggesting that the aPDT made the vancomycin resistant E. faecium strain more susceptible to vancomycin action. In summary, G. mellonella provides an invertebrate model host to study the antimicrobial PDT and to explore combinatorial aPDT-based treatments.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23457486</pmid><doi>10.1371/journal.pone.0055926</doi><tpages>e55926</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2013-02, Vol.8 (2), p.e55926-e55926 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1331690776 |
| source | Open Access: PubMed Central; Publicly Available Content Database |
| subjects | Aminoglycosides Ampicillin Analysis Animals Anti-Bacterial Agents - therapeutic use Antibiotic resistance Antibiotics Antiinfectives and antibacterials Bacteria Biology Butterflies & moths Candida albicans Caterpillars Cell death Combinatorial analysis Cross infection Dentistry Dermatology Disease Models, Animal Drug therapy Enterococcus faecalis Enterococcus faecium Enterococcus faecium - drug effects Enterococcus faecium - radiation effects Galleria mellonella Gentamicin Gram-Positive Bacterial Infections - drug therapy Health aspects Health care Hemocoel Hospitals Infection control Infections Infectious diseases Insects Irradiation Killing Larvae Light Lipids Medical schools Medicine Methylene blue Methylene Blue - therapeutic use Microbial drug resistance Moths Moths - microbiology Moths - radiation effects Nosocomial infections Oxygen Pathogenesis Photochemotherapy Photodynamic therapy Photosensitizing Agents - therapeutic use Proteins Radiation Reactive oxygen species Regulatory approval Staphylococcus aureus Survival Vancomycin |
| title | Photodynamic and antibiotic therapy impair the pathogenesis of Enterococcus faecium in a whole animal insect model |
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