Synergy between induction heating, antibiotics, and N-acetylcysteine eradicates Staphylococcus aureus from biofilm

References

• Del Pozo JL, Patel R. Clinical practice. Infection associated with prosthetic joints. N Engl J Med. 2009;361:787–794.
   PubMed Web of Science ®Google Scholar
• Tande AJ, Patel R. Prosthetic joint infection. Clin Microbiol Rev. 2014;27:302–345.
   PubMed Web of Science ®Google Scholar
• Anguita-Alonso P, Hanssen AD, Osmon DR, et al. High rate of aminoglycoside resistance among staphylococci causing prosthetic joint infection. Clin Orthop Relat Res. 2005;439:43–47.
   PubMed Web of Science ®Google Scholar
• Gomes DM, Ward KE, LaPlante KL. Clinical implications of vancomycin heteroresistant and intermediately susceptible Staphylococcus aureus. Pharmacotherapy. 2015;35:424–432.
   PubMed Web of Science ®Google Scholar
• Lee JYH, Monk IR, Gonçalves da Silva A, et al. Global spread of three multidrug-resistant lineages of Staphylococcus epidermidis. Nat Microbiol. 2018;3:1175–1185.
   PubMed Web of Science ®Google Scholar
• Ravi S, Zhu M, Luey C, et al. Antibiotic resistance in early periprosthetic joint infection. ANZ J Surg. 2016;86:1014–1018.
   PubMed Web of Science ®Google Scholar
• Cheng B, Chatzinoff Y, Szczepanski D, et al. Remote acoustic sensing as a safety mechanism during exposure of metal implants to alternating magnetic fields. PLoS One. 2018;13:e0197380.
   PubMed Web of Science ®Google Scholar
• Chopra R, Shaikh S, Chatzinoff Y, et al. Employing high-frequency alternating magnetic fields for the non-invasive treatment of prosthetic joint infections. Sci Rep. 2017;7:7520.
   PubMed Web of Science ®Google Scholar
• Pijls BG, Sanders IMJG, Kuijper EJ, et al. Non-contact electromagnetic induction heating for eradicating bacteria and yeasts on biomaterials and possible relevance to orthopaedic implant infections: in vitro findings. Bone Joint Res. 2017;6:323–330.
   PubMed Web of Science ®Google Scholar
• Pijls BG, Sanders IMJG, Kuijper EJ, et al. Segmental induction heating of orthopaedic metal implants. Bone Joint Res. 2018;7:609–619.
   PubMed Web of Science ®Google Scholar
• Deramond H, Wright NT, Belkoff SM. Temperature elevation caused by bone cement polymerization during vertebroplasty. Bone. 1999;25:17S–21S.
   PubMed Web of Science ®Google Scholar
• Eriksson AR, Albrektsson T, Albrektsson B. Heat caused by drilling cortical bone. Temperature measured in vivo in patients and animals. Acta Orthop Scand. 1984;55:629–631.
   PubMed Web of Science ®Google Scholar
• Sutton PA, Awad S, Perkins AC, et al. Comparison of lateral thermal spread using monopolar and bipolar diathermy, the Harmonic Scalpel and the Ligasure. Br J Surg. 2010;97:428–433.
   PubMed Web of Science ®Google Scholar
• Samara E, Moriarty TF, Decosterd LA, et al. Antibiotic stability over six weeks in aqueous solution at body temperature with and without heat treatment that mimics the curing of bone cement. Bone Joint Res. 2017;6:296–306.
   PubMed Web of Science ®Google Scholar
• Hajdu S, Holinka J, Reichmann S, et al. Increased temperature enhances the antimicrobial effects of daptomycin, vancomycin, tigecycline, fosfomycin, and cefamandole on staphylococcal biofilms. Antimicrob Agents Chemother. 2010;54:4078–4084.
   PubMed Web of Science ®Google Scholar
• Eroshenko D, Polyudova T, Korobov V. N-acetylcysteine inhibits growth, adhesion and biofilm formation of Gram-positive skin pathogens. Microb Pathog. 2017;105:145–152.
   PubMed Web of Science ®Google Scholar
• Leite B, Gomes F, Teixeira P, et al. Staphylococcus epidermidis biofilms control by N-acetylcysteine and rifampicin. Am J Ther. 2013;20:322–328.
   PubMed Web of Science ®Google Scholar
• Koseki H, Yonekura A, Shida T, et al. Early staphylococcal biofilm formation on solid orthopaedic implant materials: in vitro study. PLoS One. 2014;9:e107588.
   PubMed Web of Science ®Google Scholar
• Vollmer M, Mollmann KP. Infrared thermal imaging. Fundamentals, research and applications. 2nd ed. Weinheim: Wiley; 2010.
   Google Scholar
• Pettit RK, Weber CA, Pettit GR. Application of a high throughput Alamar blue biofilm susceptibility assay to Staphylococcus aureus biofilms. Ann Clin Microbiol Antimicrob. 2009;8:28.
   PubMed Web of Science ®Google Scholar
• Soni I, Chakrapani H, Chopra S. Draft genome sequence of methicillin-sensitive Staphylococcus aureus ATCC 29213. Genome Announc. 2015;3:e01095–15.
   PubMedGoogle Scholar
• Aarnoutse RE, Kibiki GS, Reither K, et al. Pharmacokinetics, tolerability, and bacteriological response of Rifampin administered at 600, 900, and 1,200 milligrams daily in patients with pulmonary Tuberculosis. Antimicrob Agents Chemother. 2017;61:e01054–17.
   PubMed Web of Science ®Google Scholar
• Holdiness MR. Clinical pharmacokinetics of N-acetylcysteine. Clin Pharmacokinet. 1991;20:123–134.
   PubMed Web of Science ®Google Scholar
• Thabit AK, Fatani DF, Bamakhrama MS, et al. Antibiotic penetration into bone and joints: an updated review. Int J Infect Dis. 2019;81:128–136.
   PubMed Web of Science ®Google Scholar
• Osmon DR, Berbari EF, Berendt AR, et al. Diagnosis and management of prosthetic joint infection: clinical practice guidelines by the Infectious Diseases Society of America. Clin Infect Dis. 2013;56:e1–e25.
   PubMed Web of Science ®Google Scholar
• Scheper H, van Hooven D, van de Sande M, et al. Outcome of acute staphylococcal prosthetic joint infection treated with debridement, implant retention and antimicrobial treatment with short duration of rifampicin. J Infect. 2018;76:498–500.
   PubMed Web of Science ®Google Scholar
• Amrhein V, Greenland S, McShane B. Scientists rise up against statistical significance. Nature. 2019;567:305–307.
   PubMed Web of Science ®Google Scholar
• Ricker EB, Nuxoll E. Synergistic effects of heat and antibiotics on Pseudomonas aeruginosa biofilms. Biofouling. 2017;33:855–866.
   PubMed Web of Science ®Google Scholar
• Muller CW, ElKashef T, Pfeifer R, et al. Transcutaneous electromagnetic induction heating of an intramedullary nickel-titanium shape memory implant. Int Orthop. 2014;38:2551–2557.
   PubMed Web of Science ®Google Scholar
• Muller CW, Pfeifer R, Meier K, et al. A novel shape memory plate osteosynthesis for noninvasive modulation of fixation stiffness in a rabbit Tibia Osteotomy model. Biomed Res Int. 2015;2015:652940.
   PubMed Web of Science ®Google Scholar
• Fang C-H, Tsai P-I, Huang S-W, et al. Magnetic hyperthermia enhance the treatment efficacy of peri-implant osteomyelitis. BMC Infect Dis. 2017;17:516.
   PubMed Web of Science ®Google Scholar
• ICNIRP. ICNIRP Guidelines for limiting exposure to time-varying electric, magnetic and electromagnetic fields (100kHz to 300GHz). 2018 [cited 2019 Oct 7]. Available from: https://www.icnirp.org/cms/upload/consultation_upload/ICNIRP_RF_Guidelines_PCD_2018_07_11.pd
   Google Scholar
• van den Tempel N, Horsman MR, Kanaar R. Improving efficacy of hyperthermia in oncology by exploiting biological mechanisms. Int J Hyperthermia. 2016;32:446–454.
   PubMed Web of Science ®Google Scholar
• Gazel D, Yilmaz M. Are infectious diseases and microbiology new fields for thermal therapy research? Int J Hyperthermia. 2018;34:918–924.
   PubMed Web of Science ®Google Scholar