{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,21]],"date-time":"2026-09-21T10:37:50Z","timestamp":1789987070470,"version":"4.0.1"},"reference-count":25,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2024,4,16]],"date-time":"2024-04-16T00:00:00Z","timestamp":1713225600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000968","name":"American Heart Association","doi-asserted-by":"publisher","award":["18IPA34170108"],"award-info":[{"award-number":["18IPA34170108"]}],"id":[{"id":"10.13039\/100000968","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000968","name":"American Heart Association","doi-asserted-by":"publisher","award":["CBET-1133297"],"award-info":[{"award-number":["CBET-1133297"]}],"id":[{"id":"10.13039\/100000968","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["18IPA34170108"],"award-info":[{"award-number":["18IPA34170108"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["CBET-1133297"],"award-info":[{"award-number":["CBET-1133297"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>Staphylococcus epidermidis is a major contributor to bacterial infections on medical implants, currently treated by surgical removal of the device and the surrounding infected tissue at considerable morbidity and expense. In situ hyperthermia is being investigated as a non-invasive means of mitigating these bacterial biofilm infections, but minimizing damage to the surrounding tissue requires augmenting the thermal shock with other approaches such as antibiotics and discerning the minimum shock required to eliminate the biofilm. S. epidermidis biofilms were systematically shocked at a variety of temperatures (50\u201380 \u00b0C) and durations (1\u201310 min) to characterize their thermal susceptibility and compare it to other common nosocomial pathogens such as Staphylococcus aureus and Pseudomonas aeruginosa. Biofilms were also exposed to three classes of antibiotics (ciprofloxacin, tobramycin and erythromycin) separately at concentrations ranging from 0 to 128 \u03bcg mL\u22121 to evaluate their impact on the efficacy of thermal shock and the subsequent potential regrowth of the biofilm. S. epidermidis biofilms were shown to be more thermally susceptible to hyperthermia than other common bacterial pathogens. All three antibiotics substantially decreased the duration and\/or temperature needed to eliminate the biofilms, though this augmentation did not meet the criteria of synergism immediately following thermal shock. Subsequent reincubation, however, revealed strong synergism on a longer timescale.<\/jats:p>","DOI":"10.3390\/pathogens13040327","type":"journal-article","created":{"date-parts":[[2024,4,17]],"date-time":"2024-04-17T08:22:44Z","timestamp":1713342164000},"page":"327","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Antibiotic Augmentation of Thermal Eradication of Staphylococcus epidermidis Biofilm Infections"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-5051-4048","authenticated-orcid":false,"given":"Haydar A. S.","family":"Aljaafari","sequence":"first","affiliation":[{"name":"Department of Chemical and Biochemical Engineering, University of Iowa, Iowa City, IA 52242, USA"},{"name":"Department of Chemical Engineering, University of Technology, Baghdad 10066, Iraq"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nadia I.","family":"Abdulwahhab","sequence":"additional","affiliation":[{"name":"Department of Chemical and Biochemical Engineering, University of Iowa, Iowa City, IA 52242, USA"},{"name":"Department of Applied Sciences, University of Technology, Baghdad 10066, Iraq"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eric","family":"Nuxoll","sequence":"additional","affiliation":[{"name":"Department of Chemical and Biochemical Engineering, University of Iowa, Iowa City, IA 52242, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,4,16]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1099\/jmm.0.000032","article-title":"Healthcare-associated infections, medical devices and biofilms: Risk, tolerance and control","volume":"64","author":"Percival","year":"2015","journal-title":"J. Med. Microbiol."},{"key":"ref_2","unstructured":"McDermott, K.W., Freeman, W.J., and Elixhauser, A. (2017). Healthcare Cost and Utilization Project (HCUP) Statistical Briefs, Agency for Healthcare Reesarch and Quality."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1016\/j.arth.2015.07.034","article-title":"Projected Increase in Periprosthetic Joint Infections Secondary to Rise in Diabetes and Obesity","volume":"31","author":"Maltenfort","year":"2016","journal-title":"J. Arthroplast."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1318","DOI":"10.1126\/science.284.5418.1318","article-title":"Bacterial biofilms: A common cause of persistent infections","volume":"284","author":"Costerton","year":"1999","journal-title":"Science"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"302","DOI":"10.1128\/CMR.00111-13","article-title":"Prosthetic Joint Infection","volume":"27","author":"Tande","year":"2014","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1711","DOI":"10.1016\/j.biomaterials.2006.11.046","article-title":"Polysaccharide intercellular adhesin or protein factors in biofilm accumulation of Staphylococcus epidermidis and Staphylococcus aureus isolated from prosthetic hip and knee joint infections","volume":"28","author":"Rohde","year":"2007","journal-title":"Biomaterials"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1016\/S1286-4579(02)01563-0","article-title":"Staphylococcus epidermidis infections","volume":"4","author":"Vuong","year":"2002","journal-title":"Microbes Infect."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1175","DOI":"10.1038\/s41564-018-0230-7","article-title":"Global spread of three multidrug-resistant lineages of Staphylococcus epidermidis","volume":"3","author":"Lee","year":"2018","journal-title":"Nat. Microbiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1128\/am.30.3.381-395.1975","article-title":"Distribution and Persistence of Staphylococcus and Micrococcus Species and Other Aerobic Bacteria on Human Skin","volume":"30","author":"Kloos","year":"1975","journal-title":"Appl. Microbiol."},{"key":"ref_10","first-page":"207","article-title":"Staphylococcal biofilms","volume":"322","author":"Otto","year":"2008","journal-title":"Curr. Top. Microbiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"665","DOI":"10.1080\/08927014.2015.1083985","article-title":"Thermal mitigation of Pseudomonas aeruginosa biofilms","volume":"31","author":"Ricker","year":"2015","journal-title":"Biofouling"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"7520","DOI":"10.1038\/s41598-017-07321-6","article-title":"Employing high-frequency alternating magnetic fields for the non-invasive treatment of prosthetic joint infections","volume":"7","author":"Chopra","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1302\/2046-3758.65.BJR-2016-0308.R1","article-title":"Non-contact electromagnetic induction heating for eradicating bacteria and yeasts on biomaterials and possible relevance to orthopaedic implant infections","volume":"6","author":"Pijls","year":"2017","journal-title":"Bone Jt. Res."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1080\/02656736.2017.1347964","article-title":"Thermal shock susceptibility and regrowth of Pseudomonas aeruginosa biofilms","volume":"34","author":"Ricker","year":"2018","journal-title":"Int. J. Hyperther"},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Fang, C.H., Tsai, P.I., Huang, S.W., Sun, J.S., Chang, J.Z.C., Shen, H.H., Chen, S.Y., Lin, F.H., Hsu, L.T., and Chen, Y.C. (2017). Magnetic hyperthermia enhance the treatment efficacy of peri-implant osteomyelitis. Bmc Infect. Dis., 17.","DOI":"10.1186\/s12879-017-2621-4"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"4078","DOI":"10.1128\/AAC.00275-10","article-title":"Increased Temperature Enhances the Antimicrobial Effects of Daptomycin, Vancomycin, Tigecycline, Fosfomycin, and Cefamandole on Staphylococcal Biofilms","volume":"54","author":"Hajdu","year":"2010","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"192","DOI":"10.1302\/2046-3758.94.BJR-2019-0274.R1","article-title":"Induction heating for eradicating Staphylococcus epidermidis from biofilm","volume":"9","author":"Pijls","year":"2020","journal-title":"Bone Joint Res."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1302\/2046-3758.119.BJR-2022-0010.R1","article-title":"Effectiveness of mechanical cleaning, antibiotics, and induction heating on eradication of Staphylococcus aureus in mature biofilms","volume":"11","author":"Pijls","year":"2022","journal-title":"Bone Joint Res."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Wang, Q., Vachon, J., Prasad, B., Pybus, C.A., Lapin, N., Chopra, R., and Greenberg, D.E. (2021). Alternating magnetic fields and antibiotics eradicate biofilm on metal in a synergistic fashion. NPJ Biofilms Microbiomes, 7.","DOI":"10.1038\/s41522-021-00239-y"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"7538","DOI":"10.1039\/C5TB01540E","article-title":"Magnetic nanoparticle\/polymer composites for medical implant infection control","volume":"3","author":"Coffel","year":"2015","journal-title":"J. Mater. Chem. B"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1080\/02656736.2019.1710269","article-title":"Synergy between induction heating, antibiotics, and N-acetylcysteine eradicates Staphylococcus aureus from biofilm","volume":"37","author":"Pijls","year":"2020","journal-title":"Int. J. Hyperther"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Aljaafari, H., Gu, Y., Chicchelly, H., and Nuxoll, E. (2021). Thermal Shock and Ciprofloxacin Act Orthogonally on Pseudomonas aeruginosa Biofilms. Antibiotics, 10.","DOI":"10.3390\/antibiotics10081017"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"516","DOI":"10.1080\/08927014.2023.2234290","article-title":"Thermal susceptibility and antibiotic synergism of methicillin-resistant Staphylococcus aureus biofilms","volume":"39","author":"Aljaafari","year":"2023","journal-title":"Biofouling"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"855","DOI":"10.1080\/08927014.2017.1381688","article-title":"Synergistic effects of heat and antibiotics on Pseudomonas aeruginosa biofilms","volume":"33","author":"Ricker","year":"2017","journal-title":"Biofouling"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"320","DOI":"10.3109\/02656736.2010.534527","article-title":"Thresholds for thermal damage to normal tissues: An update","volume":"27","author":"Yarmolenko","year":"2011","journal-title":"Int. J. Hyperth."}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/13\/4\/327\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T14:28:46Z","timestamp":1760106526000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/13\/4\/327"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,4,16]]},"references-count":25,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2024,4]]}},"alternative-id":["pathogens13040327"],"URL":"https:\/\/doi.org\/10.3390\/pathogens13040327","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,4,16]]}}}