Breaking down antibiotic resistance in methicillin-resistant Staphylococcus aureus : Combining antimicrobial photodynamic and antibiotic treatments

The widespread use of antibiotics drives the evolution of antimicrobial-resistant bacteria (ARB), threatening patients and healthcare professionals. Therefore, the development of novel strategies to combat resistance is recognized as a global healthcare priority. The two methods to combat ARB are de...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Proceedings of the National Academy of Sciences - PNAS 2022-09, Vol.119 (36), p.e2208378119-e2208378119
Hauptverfasser: Willis, Jace A, Cheburkanov, Vsevolod, Chen, Shaorong, Soares, Jennifer M, Kassab, Giulia, Blanco, Kate C, Bagnato, Vanderlei S, de Figueiredo, Paul, Yakovlev, Vladislav V
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page e2208378119
container_issue 36
container_start_page e2208378119
container_title Proceedings of the National Academy of Sciences - PNAS
container_volume 119
creator Willis, Jace A
Cheburkanov, Vsevolod
Chen, Shaorong
Soares, Jennifer M
Kassab, Giulia
Blanco, Kate C
Bagnato, Vanderlei S
de Figueiredo, Paul
Yakovlev, Vladislav V
description The widespread use of antibiotics drives the evolution of antimicrobial-resistant bacteria (ARB), threatening patients and healthcare professionals. Therefore, the development of novel strategies to combat resistance is recognized as a global healthcare priority. The two methods to combat ARB are development of new antibiotics or reduction in existing resistances. Development of novel antibiotics is a laborious and slow-progressing task that is no longer a safe reserve against looming risks. In this research, we suggest a method for reducing resistance to extend the efficacious lifetime of current antibiotics. Antimicrobial photodynamic therapy (aPDT) is used to generate reactive oxygen species (ROS) via the photoactivation of a photosensitizer. ROS then nonspecifically damage cellular components, leading to general impairment and cell death. Here, we test the hypothesis that concurrent treatment of bacteria with antibiotics and aPDT achieves an additive effect in the elimination of ARB. Performing aPDT with the photosensitizer methylene blue in combination with antibiotics chloramphenicol and tetracycline results in significant reductions in resistance for two methicillin-resistant (MRSA) strains, USA300 and RN4220. Additional resistant strain and antibiotic combinations reveal similar results. Taken together, these results suggest that concurrent aPDT consistently decreases resistance by improving susceptibility to antibiotic treatment. In turn, this development exhibits an alternative to overcome some of the growing MRSA challenge.
doi_str_mv 10.1073/pnas.2208378119
format Article
fullrecord <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9457041</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2708259288</sourcerecordid><originalsourceid>FETCH-LOGICAL-c421t-b8a3aea229784f4c70e91f698d6c66905252e7569dc46416e3888f1ce58101303</originalsourceid><addsrcrecordid>eNpdkUlv1TAUhS0Eoo_Cmh2KxIZN2ushHlgglScmqRILYG05jtPnktjBdkDvd_QP108dKKyu5PP53OEg9BLDCQZBT5dg8gkhIKmQGKtHaINB4ZYzBY_RBoCIVjLCjtCznC8BQHUSnqIjyoEKyvgGXb1Pzvz04aIZ4p_QmFB872Pxtkku-1xMsK7xoZld2Xnrp8mH9k4pzbdilt1-ijZau-bGrMnV8rbZxrn34eB6MJy9TbH3ZmqWXSxx2AdTn6o0POxX6iBldqHk5-jJaKbsXtzWY_Tj44fv28_t-ddPX7Zn561lBJe2l4YaZwhRQrKRWQFO4ZErOXDLuYKOdMSJjqvBMs4wd1RKOWLrOokBU6DH6N2N77L2sxts7Z3MpJfkZ5P2Ohqv_1WC3-mL-Fsr1glguBq8uTVI8dfqctGzz9ZNkwkurlkTAZJ0ikhZ0df_oZdxTaGuVylMiOgkF5U6vaHqwXJObrwfBoM-BK4Pgeu_gdcfrx7ucM_fJUyvAdzeq2g</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2712275867</pqid></control><display><type>article</type><title>Breaking down antibiotic resistance in methicillin-resistant Staphylococcus aureus : Combining antimicrobial photodynamic and antibiotic treatments</title><source>MEDLINE</source><source>PubMed Central</source><source>Alma/SFX Local Collection</source><source>Free Full-Text Journals in Chemistry</source><creator>Willis, Jace A ; Cheburkanov, Vsevolod ; Chen, Shaorong ; Soares, Jennifer M ; Kassab, Giulia ; Blanco, Kate C ; Bagnato, Vanderlei S ; de Figueiredo, Paul ; Yakovlev, Vladislav V</creator><creatorcontrib>Willis, Jace A ; Cheburkanov, Vsevolod ; Chen, Shaorong ; Soares, Jennifer M ; Kassab, Giulia ; Blanco, Kate C ; Bagnato, Vanderlei S ; de Figueiredo, Paul ; Yakovlev, Vladislav V</creatorcontrib><description>The widespread use of antibiotics drives the evolution of antimicrobial-resistant bacteria (ARB), threatening patients and healthcare professionals. Therefore, the development of novel strategies to combat resistance is recognized as a global healthcare priority. The two methods to combat ARB are development of new antibiotics or reduction in existing resistances. Development of novel antibiotics is a laborious and slow-progressing task that is no longer a safe reserve against looming risks. In this research, we suggest a method for reducing resistance to extend the efficacious lifetime of current antibiotics. Antimicrobial photodynamic therapy (aPDT) is used to generate reactive oxygen species (ROS) via the photoactivation of a photosensitizer. ROS then nonspecifically damage cellular components, leading to general impairment and cell death. Here, we test the hypothesis that concurrent treatment of bacteria with antibiotics and aPDT achieves an additive effect in the elimination of ARB. Performing aPDT with the photosensitizer methylene blue in combination with antibiotics chloramphenicol and tetracycline results in significant reductions in resistance for two methicillin-resistant (MRSA) strains, USA300 and RN4220. Additional resistant strain and antibiotic combinations reveal similar results. Taken together, these results suggest that concurrent aPDT consistently decreases resistance by improving susceptibility to antibiotic treatment. In turn, this development exhibits an alternative to overcome some of the growing MRSA challenge.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.2208378119</identifier><identifier>PMID: 36037346</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Anti-Bacterial Agents - pharmacology ; Antibiotic resistance ; Antibiotics ; Antiinfectives and antibacterials ; Bacteria ; Biological Sciences ; Breaking down ; Cell death ; Chloramphenicol ; Chloromycetin ; Drug resistance ; Drug Resistance, Microbial - drug effects ; Drug Resistance, Microbial - radiation effects ; Global health ; Health care ; Humans ; Methicillin ; Methicillin-Resistant Staphylococcus aureus - drug effects ; Methicillin-Resistant Staphylococcus aureus - radiation effects ; Methylene blue ; Penicillin ; Photoactivation ; Photochemotherapy ; Photodynamic therapy ; Photosensitizing Agents - pharmacology ; Public health ; Reactive oxygen species ; Reactive Oxygen Species - pharmacology ; Staphylococcus aureus ; Staphylococcus infections</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2022-09, Vol.119 (36), p.e2208378119-e2208378119</ispartof><rights>Copyright National Academy of Sciences Sep 6, 2022</rights><rights>Copyright © 2022 the Author(s). Published by PNAS. 2022</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c421t-b8a3aea229784f4c70e91f698d6c66905252e7569dc46416e3888f1ce58101303</citedby><cites>FETCH-LOGICAL-c421t-b8a3aea229784f4c70e91f698d6c66905252e7569dc46416e3888f1ce58101303</cites><orcidid>0000-0003-4833-239X ; 0000-0002-9055-7763 ; 0000-0002-4557-1013 ; 0000-0003-0361-9725</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/PMC9457041/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9457041/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36037346$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Willis, Jace A</creatorcontrib><creatorcontrib>Cheburkanov, Vsevolod</creatorcontrib><creatorcontrib>Chen, Shaorong</creatorcontrib><creatorcontrib>Soares, Jennifer M</creatorcontrib><creatorcontrib>Kassab, Giulia</creatorcontrib><creatorcontrib>Blanco, Kate C</creatorcontrib><creatorcontrib>Bagnato, Vanderlei S</creatorcontrib><creatorcontrib>de Figueiredo, Paul</creatorcontrib><creatorcontrib>Yakovlev, Vladislav V</creatorcontrib><title>Breaking down antibiotic resistance in methicillin-resistant Staphylococcus aureus : Combining antimicrobial photodynamic and antibiotic treatments</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>The widespread use of antibiotics drives the evolution of antimicrobial-resistant bacteria (ARB), threatening patients and healthcare professionals. Therefore, the development of novel strategies to combat resistance is recognized as a global healthcare priority. The two methods to combat ARB are development of new antibiotics or reduction in existing resistances. Development of novel antibiotics is a laborious and slow-progressing task that is no longer a safe reserve against looming risks. In this research, we suggest a method for reducing resistance to extend the efficacious lifetime of current antibiotics. Antimicrobial photodynamic therapy (aPDT) is used to generate reactive oxygen species (ROS) via the photoactivation of a photosensitizer. ROS then nonspecifically damage cellular components, leading to general impairment and cell death. Here, we test the hypothesis that concurrent treatment of bacteria with antibiotics and aPDT achieves an additive effect in the elimination of ARB. Performing aPDT with the photosensitizer methylene blue in combination with antibiotics chloramphenicol and tetracycline results in significant reductions in resistance for two methicillin-resistant (MRSA) strains, USA300 and RN4220. Additional resistant strain and antibiotic combinations reveal similar results. Taken together, these results suggest that concurrent aPDT consistently decreases resistance by improving susceptibility to antibiotic treatment. In turn, this development exhibits an alternative to overcome some of the growing MRSA challenge.</description><subject>Anti-Bacterial Agents - pharmacology</subject><subject>Antibiotic resistance</subject><subject>Antibiotics</subject><subject>Antiinfectives and antibacterials</subject><subject>Bacteria</subject><subject>Biological Sciences</subject><subject>Breaking down</subject><subject>Cell death</subject><subject>Chloramphenicol</subject><subject>Chloromycetin</subject><subject>Drug resistance</subject><subject>Drug Resistance, Microbial - drug effects</subject><subject>Drug Resistance, Microbial - radiation effects</subject><subject>Global health</subject><subject>Health care</subject><subject>Humans</subject><subject>Methicillin</subject><subject>Methicillin-Resistant Staphylococcus aureus - drug effects</subject><subject>Methicillin-Resistant Staphylococcus aureus - radiation effects</subject><subject>Methylene blue</subject><subject>Penicillin</subject><subject>Photoactivation</subject><subject>Photochemotherapy</subject><subject>Photodynamic therapy</subject><subject>Photosensitizing Agents - pharmacology</subject><subject>Public health</subject><subject>Reactive oxygen species</subject><subject>Reactive Oxygen Species - pharmacology</subject><subject>Staphylococcus aureus</subject><subject>Staphylococcus infections</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkUlv1TAUhS0Eoo_Cmh2KxIZN2ushHlgglScmqRILYG05jtPnktjBdkDvd_QP108dKKyu5PP53OEg9BLDCQZBT5dg8gkhIKmQGKtHaINB4ZYzBY_RBoCIVjLCjtCznC8BQHUSnqIjyoEKyvgGXb1Pzvz04aIZ4p_QmFB872Pxtkku-1xMsK7xoZld2Xnrp8mH9k4pzbdilt1-ijZau-bGrMnV8rbZxrn34eB6MJy9TbH3ZmqWXSxx2AdTn6o0POxX6iBldqHk5-jJaKbsXtzWY_Tj44fv28_t-ddPX7Zn561lBJe2l4YaZwhRQrKRWQFO4ZErOXDLuYKOdMSJjqvBMs4wd1RKOWLrOokBU6DH6N2N77L2sxts7Z3MpJfkZ5P2Ohqv_1WC3-mL-Fsr1glguBq8uTVI8dfqctGzz9ZNkwkurlkTAZJ0ikhZ0df_oZdxTaGuVylMiOgkF5U6vaHqwXJObrwfBoM-BK4Pgeu_gdcfrx7ucM_fJUyvAdzeq2g</recordid><startdate>20220906</startdate><enddate>20220906</enddate><creator>Willis, Jace A</creator><creator>Cheburkanov, Vsevolod</creator><creator>Chen, Shaorong</creator><creator>Soares, Jennifer M</creator><creator>Kassab, Giulia</creator><creator>Blanco, Kate C</creator><creator>Bagnato, Vanderlei S</creator><creator>de Figueiredo, Paul</creator><creator>Yakovlev, Vladislav V</creator><general>National Academy of Sciences</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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-4833-239X</orcidid><orcidid>https://orcid.org/0000-0002-9055-7763</orcidid><orcidid>https://orcid.org/0000-0002-4557-1013</orcidid><orcidid>https://orcid.org/0000-0003-0361-9725</orcidid></search><sort><creationdate>20220906</creationdate><title>Breaking down antibiotic resistance in methicillin-resistant Staphylococcus aureus : Combining antimicrobial photodynamic and antibiotic treatments</title><author>Willis, Jace A ; Cheburkanov, Vsevolod ; Chen, Shaorong ; Soares, Jennifer M ; Kassab, Giulia ; Blanco, Kate C ; Bagnato, Vanderlei S ; de Figueiredo, Paul ; Yakovlev, Vladislav V</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c421t-b8a3aea229784f4c70e91f698d6c66905252e7569dc46416e3888f1ce58101303</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Anti-Bacterial Agents - pharmacology</topic><topic>Antibiotic resistance</topic><topic>Antibiotics</topic><topic>Antiinfectives and antibacterials</topic><topic>Bacteria</topic><topic>Biological Sciences</topic><topic>Breaking down</topic><topic>Cell death</topic><topic>Chloramphenicol</topic><topic>Chloromycetin</topic><topic>Drug resistance</topic><topic>Drug Resistance, Microbial - drug effects</topic><topic>Drug Resistance, Microbial - radiation effects</topic><topic>Global health</topic><topic>Health care</topic><topic>Humans</topic><topic>Methicillin</topic><topic>Methicillin-Resistant Staphylococcus aureus - drug effects</topic><topic>Methicillin-Resistant Staphylococcus aureus - radiation effects</topic><topic>Methylene blue</topic><topic>Penicillin</topic><topic>Photoactivation</topic><topic>Photochemotherapy</topic><topic>Photodynamic therapy</topic><topic>Photosensitizing Agents - pharmacology</topic><topic>Public health</topic><topic>Reactive oxygen species</topic><topic>Reactive Oxygen Species - pharmacology</topic><topic>Staphylococcus aureus</topic><topic>Staphylococcus infections</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Willis, Jace A</creatorcontrib><creatorcontrib>Cheburkanov, Vsevolod</creatorcontrib><creatorcontrib>Chen, Shaorong</creatorcontrib><creatorcontrib>Soares, Jennifer M</creatorcontrib><creatorcontrib>Kassab, Giulia</creatorcontrib><creatorcontrib>Blanco, Kate C</creatorcontrib><creatorcontrib>Bagnato, Vanderlei S</creatorcontrib><creatorcontrib>de Figueiredo, Paul</creatorcontrib><creatorcontrib>Yakovlev, Vladislav V</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium &amp; Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors 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>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Willis, Jace A</au><au>Cheburkanov, Vsevolod</au><au>Chen, Shaorong</au><au>Soares, Jennifer M</au><au>Kassab, Giulia</au><au>Blanco, Kate C</au><au>Bagnato, Vanderlei S</au><au>de Figueiredo, Paul</au><au>Yakovlev, Vladislav V</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Breaking down antibiotic resistance in methicillin-resistant Staphylococcus aureus : Combining antimicrobial photodynamic and antibiotic treatments</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2022-09-06</date><risdate>2022</risdate><volume>119</volume><issue>36</issue><spage>e2208378119</spage><epage>e2208378119</epage><pages>e2208378119-e2208378119</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>The widespread use of antibiotics drives the evolution of antimicrobial-resistant bacteria (ARB), threatening patients and healthcare professionals. Therefore, the development of novel strategies to combat resistance is recognized as a global healthcare priority. The two methods to combat ARB are development of new antibiotics or reduction in existing resistances. Development of novel antibiotics is a laborious and slow-progressing task that is no longer a safe reserve against looming risks. In this research, we suggest a method for reducing resistance to extend the efficacious lifetime of current antibiotics. Antimicrobial photodynamic therapy (aPDT) is used to generate reactive oxygen species (ROS) via the photoactivation of a photosensitizer. ROS then nonspecifically damage cellular components, leading to general impairment and cell death. Here, we test the hypothesis that concurrent treatment of bacteria with antibiotics and aPDT achieves an additive effect in the elimination of ARB. Performing aPDT with the photosensitizer methylene blue in combination with antibiotics chloramphenicol and tetracycline results in significant reductions in resistance for two methicillin-resistant (MRSA) strains, USA300 and RN4220. Additional resistant strain and antibiotic combinations reveal similar results. Taken together, these results suggest that concurrent aPDT consistently decreases resistance by improving susceptibility to antibiotic treatment. In turn, this development exhibits an alternative to overcome some of the growing MRSA challenge.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>36037346</pmid><doi>10.1073/pnas.2208378119</doi><orcidid>https://orcid.org/0000-0003-4833-239X</orcidid><orcidid>https://orcid.org/0000-0002-9055-7763</orcidid><orcidid>https://orcid.org/0000-0002-4557-1013</orcidid><orcidid>https://orcid.org/0000-0003-0361-9725</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 0027-8424
ispartof Proceedings of the National Academy of Sciences - PNAS, 2022-09, Vol.119 (36), p.e2208378119-e2208378119
issn 0027-8424
1091-6490
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9457041
source MEDLINE; PubMed Central; Alma/SFX Local Collection; Free Full-Text Journals in Chemistry
subjects Anti-Bacterial Agents - pharmacology
Antibiotic resistance
Antibiotics
Antiinfectives and antibacterials
Bacteria
Biological Sciences
Breaking down
Cell death
Chloramphenicol
Chloromycetin
Drug resistance
Drug Resistance, Microbial - drug effects
Drug Resistance, Microbial - radiation effects
Global health
Health care
Humans
Methicillin
Methicillin-Resistant Staphylococcus aureus - drug effects
Methicillin-Resistant Staphylococcus aureus - radiation effects
Methylene blue
Penicillin
Photoactivation
Photochemotherapy
Photodynamic therapy
Photosensitizing Agents - pharmacology
Public health
Reactive oxygen species
Reactive Oxygen Species - pharmacology
Staphylococcus aureus
Staphylococcus infections
title Breaking down antibiotic resistance in methicillin-resistant Staphylococcus aureus : Combining antimicrobial photodynamic and antibiotic treatments
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-04T16%3A07%3A33IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Breaking%20down%20antibiotic%20resistance%20in%20methicillin-resistant%20Staphylococcus%20aureus%20:%20Combining%20antimicrobial%20photodynamic%20and%20antibiotic%20treatments&rft.jtitle=Proceedings%20of%20the%20National%20Academy%20of%20Sciences%20-%20PNAS&rft.au=Willis,%20Jace%20A&rft.date=2022-09-06&rft.volume=119&rft.issue=36&rft.spage=e2208378119&rft.epage=e2208378119&rft.pages=e2208378119-e2208378119&rft.issn=0027-8424&rft.eissn=1091-6490&rft_id=info:doi/10.1073/pnas.2208378119&rft_dat=%3Cproquest_pubme%3E2708259288%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2712275867&rft_id=info:pmid/36037346&rfr_iscdi=true