1887

Abstract

Healthcare-associated infections (HCAIs) are a major challenge and the near patient surface is important in harbouring causes such as methicillin-resistant (MRSA) and . Current approaches to decontamination are sub-optimal and many studies have demonstrated that microbial causes of HCAIs may persist with onward transmission. This may be due to the capacity of these microbes to survive in biofilms on surfaces. New technologies to enhance hospital decontamination may have a role in addressing this challenge. We have reviewed current technologies such as UV light and hydrogen peroxide and also assessed the potential use of cold atmospheric pressure plasma (CAPP) in surface decontamination. The antimicrobial mechanisms of CAPP are not fully understood but the production of reactive oxygen and other species is believed to be important. CAPP systems have been shown to partially or completely remove a variety of biofilms including those caused by , and multi-drug-resistant bacteria such as MRSA. There are some studies that suggest promise for CAPP in the challenge of surface decontamination in the healthcare setting. However, further work is required to define better the mechanism of action. We need to know what surfaces are most amenable to treatment, how microbial components and the maturity of biofilms may affect successful treatment, and how would CAPP be used in the clinical setting.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001582
2022-10-06
2024-05-02
Loading full text...

Full text loading...

/deliver/fulltext/jmm/71/10/jmm001582.html?itemId=/content/journal/jmm/10.1099/jmm.0.001582&mimeType=html&fmt=ahah

References

  1. Percival SL, Suleman L, Vuotto C, Donelli G. Healthcare-associated infections, medical devices and biofilms: risk, tolerance and control. J Med Microbiol 2015; 64:323–334 [View Article] [PubMed]
    [Google Scholar]
  2. The European Centre for Disease Prevention and Control Point prevalence survey of healthcare associated infections and antimicrobial use in european acute care hospitals ECDC; 2013
  3. de Kraker MEA, Wolkewitz M, Davey PG, Koller W, Berger J et al. Burden of antimicrobial resistance in European hospitals: excess mortality and length of hospital stay associated with bloodstream infections due to Escherichia coli resistant to third-generation cephalosporins. J Antimicrob Chemother 2011; 66:398–407 [View Article]
    [Google Scholar]
  4. The European Centre for Disease Prevention and Control Point prevalence survey of healthcare-associated infections and antimicrobial use in European acute care hospitals - ECDC PPS validation protocol version 3.1.2. [Internet]; 2020Mar23 https://www.ecdc.europa.eu/en/publications-data/point-prevalence-survey-healthcare-associated-infections-and-antimicrobial-use-4#copy-to-clipboard
  5. Costa DM, Johani K, Melo DS, Lopes LKO, Lopes Lima LKO et al. Biofilm contamination of high-touched surfaces in intensive care units: epidemiology and potential impacts. Lett Appl Microbiol 2019; 68:269–276 [View Article] [PubMed]
    [Google Scholar]
  6. Creamer E, Humphreys H. The contribution of beds to healthcare-associated infection: the importance of adequate decontamination. J Hosp Infect 2008; 69:8–23 [View Article] [PubMed]
    [Google Scholar]
  7. FitzGerald G, Moore G, Wilson APR. Hand hygiene after touching a patient’s surroundings: the opportunities most commonly missed. J Hosp Infect 2013; 84:27–31 [View Article] [PubMed]
    [Google Scholar]
  8. Dancer SJ, White LF, Lamb J, Girvan EK, Robertson C. Measuring the effect of enhanced cleaning in a UK hospital: a prospective cross-over study. BMC Med 2009; 7:28 [View Article]
    [Google Scholar]
  9. Dancer SJ, Cormack K, Loh M, Coulombe C, Thomas L et al. Healthcare-acquired clusters of COVID-19 across multiple wards in a Scottish health board. J Hosp Infect 2022; 120:23–30 [View Article]
    [Google Scholar]
  10. Hu H, Johani K, Gosbell IB, Jacombs ASW, Almatroudi A et al. Intensive care unit environmental surfaces are contaminated by multidrug-resistant bacteria in biofilms: combined results of conventional culture, pyrosequencing, scanning electron microscopy, and confocal laser microscopy. J Hosp Infect 2015; 91:35–44 [View Article] [PubMed]
    [Google Scholar]
  11. Vickery K, Deva A, Jacombs A, Allan J, Valente P et al. Presence of biofilm containing viable multiresistant organisms despite terminal cleaning on clinical surfaces in an intensive care unit. J Hosp Infect 2012; 80:52–55 [View Article] [PubMed]
    [Google Scholar]
  12. Lindsay D, von Holy A. Bacterial biofilms within the clinical setting: what healthcare professionals should know. J Hosp Infect 2006; 64:313–325 [View Article] [PubMed]
    [Google Scholar]
  13. Carling PC. Wastewater drains: epidemiology and interventions in 23 carbapenem-resistant organism outbreaks. Infect Control Hosp Epidemiol 2018; 39:972–979 [View Article]
    [Google Scholar]
  14. Roberts CG. The role of biofilms in reprocessing medical devices. Am J Infect Control 2013; 41:S77–80 [View Article]
    [Google Scholar]
  15. Vickery K. Special Issue: microbial biofilms in healthcare: formation, revention and Treatment. Materials 2019; 12:E2001 [View Article]
    [Google Scholar]
  16. Ledwoch K, Dancer SJ, Otter JA, Kerr K, Roposte D et al. Beware biofilm! Dry biofilms containing bacterial pathogens on multiple healthcare surfaces; a multi-centre study. J Hosp Infect 2018; 100:e47–e56 [View Article] [PubMed]
    [Google Scholar]
  17. Ledwoch K, Maillard JY. Candida auris Dry Surface Biofilm (DSB) for Disinfectant Efficacy Testing. Materials 2018; 12:E18 [View Article]
    [Google Scholar]
  18. Johani K, Abualsaud D, Costa DM, Hu H, Whiteley G et al. Characterization of microbial community composition, antimicrobial resistance and biofilm on intensive care surfaces. J Infect Public Health 2018; 11:418–424 [View Article] [PubMed]
    [Google Scholar]
  19. Chowdhury D, Tahir S, Legge M, Hu H, Prvan T et al. Transfer of dry surface biofilm in the healthcare environment: the role of healthcare workers’ hands as vehicles. J Hosp Infect 2018; 100:e85–e90 [View Article] [PubMed]
    [Google Scholar]
  20. Hong SH, Wang X, O’Connor HF, Benedik MJ, Wood TK. Bacterial persistence increases as environmental fitness decreases. Microb Biotechnol 2012; 5:509–522 [View Article] [PubMed]
    [Google Scholar]
  21. Parvin F, Hu H, Whiteley GS, Glasbey T, Vickery K. Difficulty in removing biofilm from dry surfaces. J Hosp Infect 2019; 103:465–467 [View Article] [PubMed]
    [Google Scholar]
  22. Almatroudi A, Gosbell IB, Hu H, Jensen SO, Espedido BA et al. Staphylococcus aureus dry-surface biofilms are not killed by sodium hypochlorite: implications for infection control. J Hosp Infect 2016; 93:263–270 [View Article] [PubMed]
    [Google Scholar]
  23. Dancer SJ. Hospital cleaning in the 21st century. Eur J Clin Microbiol Infect Dis 2011; 30:1473–1481 [View Article] [PubMed]
    [Google Scholar]
  24. Carling PC, Parry MF, Bruno-Murtha LA, Dick B. Improving environmental hygiene in 27 intensive care units to decrease multidrug-resistant bacterial transmission. Crit Care Med 2010; 38:1054–1059 [View Article] [PubMed]
    [Google Scholar]
  25. Doll M, Stevens M, Bearman G. Environmental cleaning and disinfection of patient areas. Int J Infect Dis 2018; 67:52–57 [View Article] [PubMed]
    [Google Scholar]
  26. Anderson DJ, Chen LF, Weber DJ, Moehring RW, Lewis SS et al. Enhanced terminal room disinfection and acquisition and infection caused by multidrug-resistant organisms and Clostridium difficile (the benefits of enhanced terminal room disinfection study): a cluster-randomised, multicentre, crossover study. Lancet 2017; 389:805–814 [View Article]
    [Google Scholar]
  27. Tingpej P, Tiengtip R, Kondo S. Decontamination efficacy of ultraviolet radiation against biofilms of common Nosocomial bacteria. J Med Assoc Thai 2015; 98:582–588 [PubMed]
    [Google Scholar]
  28. Weber DJ, Rutala WA, Anderson DJ, Chen LF, Sickbert-Bennett EE et al. Effectiveness of ultraviolet devices and hydrogen peroxide systems for terminal room decontamination: focus on clinical trials. Am J Infect Control 2016; 44:e77–84 [View Article] [PubMed]
    [Google Scholar]
  29. Doll M, Morgan DJ, Anderson D, Bearman G. Touchless technologies for decontamination in the hospital: a review of Hydrogen Peroxide and UV devices. Curr Infect Dis Rep 2015; 17:498 [View Article] [PubMed]
    [Google Scholar]
  30. Dancer SJ. Controlling hospital-acquired infection: focus on the role of the environment and new technologies for decontamination. Clin Microbiol Rev 2014; 27:665–690 [View Article] [PubMed]
    [Google Scholar]
  31. Gora SL, Rauch KD, Ontiveros CC, Stoddart AK, Gagnon GA. Inactivation of biofilm-bound Pseudomonas aeruginosa bacteria using UVC light emitting diodes (UVC LEDs). Water Res 2019; 151:193–202 [View Article] [PubMed]
    [Google Scholar]
  32. Memarzadeh F, Olmsted RN, Bartley JM. Applications of ultraviolet germicidal irradiation disinfection in health care facilities: effective adjunct, but not stand-alone technology. Am J Infect Control 2010; 38:S13–24 [View Article] [PubMed]
    [Google Scholar]
  33. Sinha RP, Häder DP. UV-induced DNA damage and repair: a review. Photochem Photobiol Sci 2002; 1:225–236 [View Article] [PubMed]
    [Google Scholar]
  34. Sholtes K, Linden KG. Pulsed and continuous light UV LED: microbial inactivation, electrical, and time efficiency. Water Res 2019; 165:114965 [View Article] [PubMed]
    [Google Scholar]
  35. Nerandzic MM, Cadnum JL, Pultz MJ, Donskey CJ. Evaluation of an automated ultraviolet radiation device for decontamination of Clostridium difficile and other healthcare-associated pathogens in hospital rooms. BMC Infect Dis 2010; 10:197 [View Article] [PubMed]
    [Google Scholar]
  36. Smolle C, Huss F, Lindblad M, Reischies F, Tano E. Effectiveness of automated ultraviolet-C light for decontamination of textiles inoculated with Enterococcus faecium. J Hosp Infect 2018; 98:102–104 [View Article] [PubMed]
    [Google Scholar]
  37. Haas JP, Menz J, Dusza S, Montecalvo MA. Implementation and impact of ultraviolet environmental disinfection in an acute care setting. Am J Infect Control 2014; 42:586–590 [View Article] [PubMed]
    [Google Scholar]
  38. Jinadatha C, Villamaria FC, Restrepo MI, Ganachari-Mallappa N, Liao I-C et al. Is the pulsed xenon ultraviolet light no-touch disinfection system effective on methicillin-resistant Staphylococcus aureus in the absence of manual cleaning?. Am J Infect Control 2015; 43:878–881 [View Article] [PubMed]
    [Google Scholar]
  39. Gidari A, Sabbatini S, Bastianelli S, Pierucci S, Busti C et al. SARS-CoV-2 survival on surfaces and the effect of UV-C light. Viruses 2021; 13:408 [View Article] [PubMed]
    [Google Scholar]
  40. Mustapha A, Alhmidi H, Cadnum JL, Jencson AL, Donskey CJ. Efficacy of manual cleaning and an ultraviolet C room decontamination device in reducing health care-associated pathogens on hospital floors. Am J Infect Control 2018; 46:584–586 [View Article] [PubMed]
    [Google Scholar]
  41. Wong T, Woznow T, Petrie M, Murzello E, Muniak A et al. Postdischarge decontamination of MRSA, VRE, and Clostridium difficile isolation rooms using 2 commercially available automated ultraviolet-C-emitting devices. Am J Infect Control 2016; 44:416–420 [View Article] [PubMed]
    [Google Scholar]
  42. Bae YM, Lee SY. Inhibitory effects of UV treatment and a combination of UV and dry heat against pathogens on stainless steel and polypropylene surfaces. J Food Sci 2012; 77:M61–4 [View Article] [PubMed]
    [Google Scholar]
  43. Boyce JM, Farrel PA, Towle D, Fekieta R, Aniskiewicz M. Impact of room location on UV-C irradiance and UV-C dosage and antimicrobial effect delivered by a mobile UV-C light device. Infect Control Hosp Epidemiol 2016; 37:667–672 [View Article] [PubMed]
    [Google Scholar]
  44. Falagas ME, Thomaidis PC, Kotsantis IK, Sgouros K, Samonis G et al. Airborne hydrogen peroxide for disinfection of the hospital environment and infection control: a systematic review. J Hosp Infect 2011; 78:171–177 [View Article] [PubMed]
    [Google Scholar]
  45. Mitchell BG, Digney W, Locket P, Dancer SJ. Controlling methicillin-resistant Staphylococcus aureus (MRSA) in a hospital and the role of hydrogen peroxide decontamination: an interrupted time series analysis. BMJ Open 2014; 4:e004522 [View Article] [PubMed]
    [Google Scholar]
  46. Boyce JM, Guercia KA, Sullivan L, Havill NL, Fekieta R, Kozakiewicz J et al. Prospective cluster controlled crossover trial to compare the impact of an improved hydrogen peroxide disinfectant and a quaternary ammonium-based disinfectant on surface contamination and health care outcomes. Am J Infect Control 2017; 45:91006–10
    [Google Scholar]
  47. Cadnum JL, Pearlmutter BS, Haq MF, Jencson AL, Donskey CJ. Effectiveness and real-world materials compatibility of a novel hydrogen peroxide disinfectant cleaner. Am J Infect Control 2021; 49:1572–1574 [View Article]
    [Google Scholar]
  48. Janik E, Bartos M, Niemcewicz M, Gorniak L, Bijak M. SARS-CoV-2: outline, prevention, and decontamination. Pathogens 2021; 10:114 [View Article]
    [Google Scholar]
  49. Linley E, Denyer SP, McDonnell G, Simons C, Maillard JY. Use of hydrogen peroxide as a biocide: new consideration of its mechanisms of biocidal action. J Antimicrob Chemother 2012; 67:1589–1596 [View Article]
    [Google Scholar]
  50. Rutala WA, Gergen MF, Weber DJ. Efficacy of improved hydrogen peroxide against important healthcare-associated pathogens. Infect Control Hosp Epidemiol 2012; 33:1159–1161 [View Article] [PubMed]
    [Google Scholar]
  51. Emmert S, Brehmer F, Hänßle H, Helmke A, Mertens N et al. Atmospheric pressure plasma in dermatology: ulcus treatment and much more. Clin Plasma Med 2013; 1:24–29 [View Article]
    [Google Scholar]
  52. Metelmann H-R, Seebauer C, Miller V, Fridman A, Bauer G et al. Clinical experience with cold plasma in the treatment of locally advanced head and neck cancer. Clin Plasma Med 2018; 9:6–13 [View Article]
    [Google Scholar]
  53. Moreau M, Orange N, Feuilloley MGJ. Non-thermal plasma technologies: new tools for bio-decontamination. Biotechnol Adv 2008; 26:610–617 [View Article] [PubMed]
    [Google Scholar]
  54. Conrads H, Schmidt M. Plasma generation and plasma sources. Plasma Sources Sci Technol 2000; 9:441–454 [View Article]
    [Google Scholar]
  55. Joaquin JC, Kwan C, Abramzon N, Vandervoort K, Brelles-Mariño G. Is gas-discharge plasma a new solution to the old problem of biofilm inactivation?. Microbiology 2009; 155:724–732 [View Article]
    [Google Scholar]
  56. Mai-Prochnow A, Clauson M, Hong J, Murphy AB. Gram positive and gram negative bacteria differ in their sensitivity to cold plasma. Sci Rep 2016; 6:38610 [View Article] [PubMed]
    [Google Scholar]
  57. Laroussi M. Plasma medicine: A brief introduction. Plasma 2018; 1:47–60 [View Article]
    [Google Scholar]
  58. O’Connor N, Cahill O, Daniels S, Galvin S, Humphreys H. Cold atmospheric pressure plasma and decontamination. Can it contribute to preventing hospital-acquired infections?. J Hosp Infect 2014; 88:59–65 [View Article]
    [Google Scholar]
  59. Bioproces Biotechniq J. Challenges in biofilm inactivation: the use of cold plasma as a new approach; 2012
  60. Lu X, Naidis GV, Laroussi M, Reuter S, Graves DB et al. Reactive species in non-equilibrium atmospheric-pressure plasmas: generation, transport, and biological effects. Phys Rep 2016; 630:1–84 [View Article]
    [Google Scholar]
  61. Asghar AH, Ahmed OB, Galaly AR. Inactivation of E. coli using atmospheric pressure plasma jet with dry and wet argon discharges. Membranes (Basel) 2021; 11:46 [View Article] [PubMed]
    [Google Scholar]
  62. Scholtz V, Pazlarova J, Souskova H, Khun J, Julak J. Nonthermal plasma--a tool for decontamination and disinfection. Biotechnol Adv 2015; 33:1108–1119 [View Article] [PubMed]
    [Google Scholar]
  63. Slauch JM. How does the oxidative burst of macrophages kill bacteria? Still an open question. Mol Microbiol 2011; 80:580–583 [View Article] [PubMed]
    [Google Scholar]
  64. Imlay JA. The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat Rev Microbiol 2013; 11:443–454 [View Article] [PubMed]
    [Google Scholar]
  65. Dedon PC, Tannenbaum SR. Reactive nitrogen species in the chemical biology of inflammation. Arch Biochem Biophys 2004; 423:12–22 [View Article] [PubMed]
    [Google Scholar]
  66. Jha N, Ryu JJ, Choi EH, Kaushik NK. Generation and role of reactive oxygen and nitrogen species induced by plasma, lasers, chemical agents, and other systems in dentistry. Oxid Med Cell Longev 2017; 2017:7542540 [View Article] [PubMed]
    [Google Scholar]
  67. Vaze ND, Park S, Brooks AD, Fridman A, Joshi SG. Involvement of multiple stressors induced by non-thermal plasma-charged aerosols during inactivation of airborne bacteria. PLoS One 2017; 12:e0171434 [View Article]
    [Google Scholar]
  68. Dezest M, Bulteau A-L, Quinton D, Chavatte L, Le Bechec M et al. Oxidative modification and electrochemical inactivation of Escherichia coli upon cold atmospheric pressure plasma exposure. PLoS One 2017; 12:e0173618 [View Article] [PubMed]
    [Google Scholar]
  69. Han L, Patil S, Boehm D, Milosavljević V, Cullen PJ et al. Mechanisms of inactivation by high-voltage atmospheric cold plasma differ for Escherichia coli and Staphylococcus aureus. Appl Environ Microbiol 2016; 82:450–458 [View Article] [PubMed]
    [Google Scholar]
  70. Schnabel U, Andrasch M, Weltmann K-D, Ehlbeck J. Inactivation of vegetative microorganisms and Bacillus atrophaeus Endospores by Reactive Nitrogen Species (RNS). Plasma Process Polym 2014; 11:110–116 [View Article]
    [Google Scholar]
  71. Ulu M, Pekbagriyanik T, Ibis F, Enhos S, Ercan UK. Antibiofilm efficacies of cold plasma and er: YAG laser on Staphylococcus aureus biofilm on titanium for nonsurgical treatment of peri-implantitis. Niger J Clin Pract 2018; 21:758–765 [View Article] [PubMed]
    [Google Scholar]
  72. Liu T, Wu L, Babu JP, Hottel TL, Garcia-Godoy F et al. Effects of atmospheric non-thermal argon/oxygen plasma on biofilm viability and hydrophobicity of oral bacteria. Am J Dent 2017; 30:52–56 [PubMed]
    [Google Scholar]
  73. Liu X, Wang Z, Li J, Wang Y, Sun Y et al. Inactivation of E. coli, S. aureus, and bacteriophages in biofilms by humidified air plasma. IJMS 2022; 23:4856 [View Article]
    [Google Scholar]
  74. Flynn PB, Graham WG, Gilmore BF. Acinetobacter baumannii biofilm biomass mediates tolerance to cold plasma. Lett Appl Microbiol 2019; 68:344–349 [View Article] [PubMed]
    [Google Scholar]
  75. Toté K, Horemans T, Vanden Berghe D, Maes L, Cos P. Inhibitory effect of biocides on the viable masses and matrices of Staphylococcus aureus and Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 2010; 76:3135–3142 [View Article] [PubMed]
    [Google Scholar]
  76. Leung CY, Chan YC, Samaranayake LP, Seneviratne CJ. Biocide resistance of Candida and Escherichia coli biofilms is associated with higher antioxidative capacities. J Hosp Infect 2012; 81:79–86 [View Article] [PubMed]
    [Google Scholar]
  77. Otter JA, Vickery K, Walker JT, deLancey Pulcini E, Stoodley P et al. Surface-attached cells, biofilms and biocide susceptibility: implications for hospital cleaning and disinfection. J Hosp Infect 2015; 89:16–27 [View Article] [PubMed]
    [Google Scholar]
  78. Machala Z, Chládeková L, Pelach M. Plasma agents in bio-decontamination by dc discharges in atmospheric air. J Phys D: Appl Phys 2010; 43:222001 [View Article]
    [Google Scholar]
  79. Klämpfl TG, Isbary G, Shimizu T, Li Y-F, Zimmermann JL et al. Cold atmospheric air plasma sterilization against spores and other microorganisms of clinical interest. Appl Environ Microbiol 2012; 78:5077–5082 [View Article]
    [Google Scholar]
  80. Schneider S, Lackmann J-W, Ellerweg D, Denis B, Narberhaus F et al. The role of VUV radiation in the inactivation of bacteria with an Atmospheric Pressure Plasma Jet. Plasma Process Polym [Internet] 2012; 9:561–568
    [Google Scholar]
  81. Qian K, Pan H, Li Y, Wang G, Zhang J et al. Time-related surface modification of denture base acrylic resin treated by atmospheric pressure cold plasma. Dent Mater J 2016; 35:97–103 [View Article]
    [Google Scholar]
  82. Boyce JM. Modern technologies for improving cleaning and disinfection of environmental surfaces in hospitals. Antimicrob Resist Infect Control 2016; 5:10 [View Article]
    [Google Scholar]
  83. Cahill OJ, Claro T, O’Connor N, Cafolla AA, Stevens NT et al. Cold air plasma to decontaminate inanimate surfaces of the hospital environment. Appl Environ Microbiol 2014; 80:2004–2010 [View Article]
    [Google Scholar]
  84. Lawley TD, Croucher NJ, Yu L, Clare S, Sebaihia M et al. Proteomic and genomic characterization of highly infectious Clostridium difficile 630 spores. J Bacteriol 2009; 191:5377–5386 [View Article] [PubMed]
    [Google Scholar]
  85. Claro T, Cahill OJ, O’Connor N, Daniels S, Humphreys H. Cold-air atmospheric pressure plasma against Clostridium difficile spores: a potential alternative for the decontamination of hospital inanimate surfaces. Infect Control Hosp Epidemiol 2015; 36:742–744 [View Article] [PubMed]
    [Google Scholar]
  86. Connor M, Flynn PB, Fairley DJ, Marks N, Manesiotis P et al. Evolutionary clade affects resistance of Clostridium difficile spores to cold atmospheric plasma. Sci Rep 2017; 7:41814 [View Article] [PubMed]
    [Google Scholar]
  87. Abramzon N, Joaquin JC, Bray J, Brelles-Marino G. Biofilm Destruction by RF High-Pressure Cold Plasma Jet. IEEE Trans Plasma Sci 2006; 34:1304–1309 [View Article]
    [Google Scholar]
  88. Sun Y, Yu S, Sun P, Wu H, Zhu W et al. Inactivation of Candida biofilms by non-thermal plasma and its enhancement for fungistatic effect of antifungal drugs. PLoS ONE 2012; 7:e40629 [View Article]
    [Google Scholar]
  89. Alkawareek MY, Algwari QT, Laverty G, Gorman SP, Graham WG et al. Eradication of Pseudomonas aeruginosa biofilms by atmospheric pressure non-thermal plasma. PLoS One 2012; 7:e44289 [View Article] [PubMed]
    [Google Scholar]
  90. Zimmermann JL, Shimizu T, Schmidt HU, Li YF, Morfill GE et al. Test for bacterial resistance build-up against plasma treatment. New J Phys 2012; 14:073037 [View Article]
    [Google Scholar]
  91. Matthes R, Assadian O, Kramer A. Repeated applications of cold atmospheric pressure plasma does not induce resistance in Staphylococcus aureus embedded in biofilms. GMS Hyg Infect Control 2014; 9:Doc17 [View Article] [PubMed]
    [Google Scholar]
  92. Flynn PB, Higginbotham S, Alshraiedeh NH, Gorman SP, Graham WG et al. Bactericidal efficacy of atmospheric pressure non-thermal plasma (APNTP) against the ESKAPE pathogens. Int J Antimicrob Agents 2015; 46:101–107 [View Article] [PubMed]
    [Google Scholar]
  93. Patange A, Boehm D, Ziuzina D, Cullen PJ, Gilmore B et al. High voltage atmospheric cold air plasma control of bacterial biofilms on fresh produce. Int J Food Microbiol 2019; 293:137–145 [View Article] [PubMed]
    [Google Scholar]
  94. Ziuzina D, Han L, Cullen PJ, Bourke P. Cold plasma inactivation of internalised bacteria and biofilms for Salmonella enterica serovar Typhimurium, Listeria monocytogenes and Escherichia coli. Int J Food Microbiol 2015; 210:53–61 [View Article] [PubMed]
    [Google Scholar]
  95. Guo L, Yang L, Qi Y, Niyazi G, Huang L et al. Cold atmospheric-pressure plasma caused protein damage in methicillin-resistant Staphylococcus aureus cells in biofilms. Microorganisms 2021; 9:1072 [View Article] [PubMed]
    [Google Scholar]
  96. Liao X, Hu W, Liu D, Ding T. Stress resistance and pathogenicity of nonthermal-plasma-induced viable-but-nonculturable Staphylococcus aureus through energy suppression, oxidative stress defense, and immune-escape mechanisms. Appl Environ Microbiol 2021; 87:1–17 [View Article] [PubMed]
    [Google Scholar]
  97. Liao X, Liu D, Ding T. Nonthermal plasma induces the viable-but-nonculturable state in Staphylococcus aureus via metabolic suppression and the oxidative stress response. Appl Environ Microbiol 2020; 86:e02216-19 [View Article] [PubMed]
    [Google Scholar]
  98. Zhao X, Zhong J, Wei C, Lin CW, Ding T. Current perspectives on viable but non-culturable state in foodborne pathogens. Front Microbiol 2017; 8:APR [View Article] [PubMed]
    [Google Scholar]
  99. Puligundla P, Mok C. Potential applications of nonthermal plasmas against biofilm-associated micro-organisms in vitro. J Appl Microbiol 2017; 122:1134–1148
    [Google Scholar]
  100. Jahid IK, Han N, Zhang C-Y, Ha S-D. Mixed culture biofilms of Salmonella Typhimurium and cultivable indigenous microorganisms on lettuce show enhanced resistance of their sessile cells to cold oxygen plasma. Food Microbiol 2015; 46:383–394 [View Article] [PubMed]
    [Google Scholar]
  101. Rao Y, Shang W, Yang Y, Zhou R, Rao X. Fighting mixed-species microbial biofilms with cold atmospheric plasma. Front Microbiol 2020; 11:1000 [View Article]
    [Google Scholar]
  102. Modic M, McLeod NP, Sutton JM, Walsh JL. Cold atmospheric pressure plasma elimination of clinically important single- and mixed-species biofilms. Int J Antimicrob Agents 2017; 49:375–378 [View Article]
    [Google Scholar]
  103. Kadri HE, Costello KM, Thomas P, Wantock T, Sandison G et al. The antimicrobial efficacy of remote cold atmospheric plasma effluent against single and mixed bacterial biofilms of varying age. Food Res Int 2021; 141:110126
    [Google Scholar]
  104. Labadie M, Marchal F, Merbahi N, Girbal-Neuhauser E, Fontagné-Faucher C et al. Response of controlled cell load biofilms to cold atmospheric plasma jet: evidence of extracellular matrix contribution. Life 2021; 11:694 [View Article]
    [Google Scholar]
  105. Fallon M, Boyle M, Kennedy S, Daniels S, Humphreys H. Cold atmospheric plasma, the removal of blood from steel and its effect on staphylococcal biofilm formation. A pilot study. Clin Plasma Med 2020; 19–20:100104 [View Article]
    [Google Scholar]
  106. Fernández A, Shearer N, Wilson DR, Thompson A. Effect of microbial loading on the efficiency of cold atmospheric gas plasma inactivation of Salmonella enterica serovar Typhimurium. Int J Food Microbiol 2012; 152:175–180 [View Article]
    [Google Scholar]
  107. Fallon M, Kennedy S, Kumar S, Daniels S, Humphreys H. The potential use of a cold atmospheric plasma jet for decontamination of hospital surfaces. A pilot study. Plasma Med 2021; 11:15–30 [View Article]
    [Google Scholar]
  108. Lu X, Naidis GV, Laroussi M, Reuter S, Graves DB et al. Reactive species in non-equilibrium atmospheric-pressure plasmas: generation, transport, and biological effects. React species non-equilibrium atmos plasmas. Gener Transp Biol Eff [Internet] 2016; 630:1–84
    [Google Scholar]
  109. Yang B, Chen J, Yu Q, Li H, Lin M et al. Oral bacterial deactivation using a low-temperature atmospheric argon plasma brush. J Dent 2011; 39:48–56 [View Article] [PubMed]
    [Google Scholar]
  110. Perni S, Liu DW, Shama G, Kong MG. Cold atmospheric plasma decontamination of the pericarps of fruit. J Food Prot 2008; 71:302–308 [View Article] [PubMed]
    [Google Scholar]
  111. Lai ACK, Cheung ACT, Wong MML, Li WS. Evaluation of cold plasma inactivation efficacy against different airborne bacteria in ventilation duct flow. Build Environ 2016; 98:39–46 [View Article]
    [Google Scholar]
  112. Calvo T, Álvarez-Ordóñez A, Prieto M, González-Raurich M, López M. Influence of processing parameters and stress adaptation on the inactivation of Listeria monocytogenes by Non-Thermal Atmospheric Plasma (NTAP). Food Res Int 2016; 89:631–637 [View Article] [PubMed]
    [Google Scholar]
  113. Nishime TMC, Borges AC, Koga-Ito CY, Machida M, Hein LRO et al. Non-thermal atmospheric pressure plasma jet applied to inactivation of different microorganisms. Surf Coat Technol 2017; 312:19–24 [View Article]
    [Google Scholar]
  114. Reuter S, von Woedtke T, Weltmann K-D. The kINPen—a review on physics and chemistry of the atmospheric pressure plasma jet and its applications. J Phys D: Appl Phys 2018; 51:233001 [View Article]
    [Google Scholar]
  115. Bekeschus S, Schmidt A, Weltmann K-D, von Woedtke T. The plasma jet kINPen – a powerful tool for wound healing. Clin Plasma Med 2016; 4:19–28 [View Article]
    [Google Scholar]
  116. Gorbanev Y, Golda J, Schulz von der Gathen V, Bogaerts A. Applications of the COST Plasma Jet: More than a reference standard. Plasma 2019; 2:316–327 [View Article]
    [Google Scholar]
  117. Quinn MM, Henneberger PK, Braun B, Delclos GL, Fagan K et al. Cleaning and disinfecting environmental surfaces in health care: toward an integrated framework for infection and occupational illness prevention. Am J Infect Control 2015; 43: [View Article]
    [Google Scholar]
  118. ASTM International Standard Test Method for Determining Disinfectant Efficacy Against Biofilm Grown in the CDC Biofilm Reactor Using the Single Tube Method. Internet 2022May24 https://www.astm.org/e2871-21.html
    [Google Scholar]
  119. Almatroudi A, Hu H, Deva A, Gosbell IB, Jacombs A et al. A new dry-surface biofilm model: an essential tool for efficacy testing of hospital surface decontamination procedures. J Microbiol Methods 2015; 117:171–176 [View Article]
    [Google Scholar]
  120. Ledwoch K, Said J, Norville P, Maillard J ‐Y. Artificial dry surface biofilm models for testing the efficacy of cleaning and disinfection. Lett Appl Microbiol 2019; 68:329–336 [View Article]
    [Google Scholar]
  121. Kearney AD, Boyle MA, Babu SK, Fallon M, Segurado R et al. Challenges in assessing contamination levels and novel decontamination technologies in the critical care setting. Infect Control Hosp Epidemiol 2020; 41:622–623 [View Article] [PubMed]
    [Google Scholar]
  122. Perumal PK, Wand ME, Sutton JM, Bock LJ. Evaluation of the effectiveness of hydrogen-peroxide-based disinfectants on biofilms formed by Gram-negative pathogens. J Hosp Infect 2014; 87:227–233 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.001582
Loading
/content/journal/jmm/10.1099/jmm.0.001582
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error