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Peracetic Acid

  • Günter Kampf
Chapter

Abstract

Peracetic acid has bactericidal activity at 1.6% in 3–5 min, yeasticidal activity at 0.25% in 1 min, and mycobactericidal activity at 0.35% in 5 min. Some food-associated fungi or ascospores, however, are resistant. High MIC values indicating resistance to peracetic acid have so far not been reported but tolerant isolates of E. coli, L. monocytogenes and Salmonella spp. have been described after exposure to nalidixic acid or terpenes. An epidemiological cut-off value to determine acquired resistance has not been proposed yet. No specific resistance mechanisms are currently known for peracetic acid in medically relevant micro-organisms. No cross-tolerance to antibiotics has been reported but peracetic acid can transform different beta-lactam antibiotics in wastewater and help to reduce selection pressure. Low-level exposure does not change the susceptibility of S. enterica and L. monocytogenes but of E. coli. Virulence genes may be induced (S. aureus) or reduced (L. monocytogenes). S. Typhimurium survivors of low-level exposure may be viable but not culturable. Peracetic acid inhibits or even prevents biofilm formation. Biofilm fixation by peracetic acid is between 0 and 54% and depends on the formulation. Biofilm removal is mostly poor (0–63%) and also depends on the formulation.

References

  1. 1.
    Aarnisalo K, Lundén J, Korkeala H, Wirtanen G (2007) Susceptibility of Listeria monocytogenes strains to disinfectants and chlorinated alkaline cleaners at cold temperatures. LWT Food Sci Technol 40(6):1041–1048CrossRefGoogle Scholar
  2. 2.
    Akinbobola AB, Sherry L, McKay WG, Ramage G, Williams C (2017) Tolerance of Pseudomonas aeruginosa in in-vitro biofilms to high-level peracetic acid disinfection. J Hosp Infect 97(2):162–168.  https://doi.org/10.1016/j.jhin.2017.06.024CrossRefPubMedGoogle Scholar
  3. 3.
    Alfa MJ, DeGagne P, Olson N, Hizon R (1998) Comparison of liquid chemical sterilization with peracetic acid and ethylene oxide sterilization for long narrow lumens. Am J Infect Control 26(5):469–477.  https://doi.org/10.1016/S0196-6553(98)70018-5CrossRefPubMedGoogle Scholar
  4. 4.
    Alonso-Hernando A, Alonso-Calleja C, Capita R (2010) Effects of exposure to poultry chemical decontaminants on the membrane fluidity of Listeria monocytogenes and Salmonella enterica strains. Int J Food Microbiol 137(2–3):130–136.  https://doi.org/10.1016/j.ijfoodmicro.2009.11.022CrossRefPubMedGoogle Scholar
  5. 5.
    Anonymous (2010) Peracetic acid. In: Committee on Acute Exposure Guideline Levels (ed) Acute exposure guideline levels for selected airborne chemicals (vol 8). The National Academic Press, Washington, pp 327–367Google Scholar
  6. 6.
    Arias-Moliz MT, Ordinola-Zapata R, Baca P, Ruiz-Linares M, Garcia Garcia E, Hungaro Duarte MA, Monteiro Bramante C, Ferrer-Luque CM (2015) Antimicrobial activity of Chlorhexidine, Peracetic acid and Sodium hypochlorite/etidronate irrigant solutions against Enterococcus faecalis biofilms. Int Endod J 48(12):1188–1193.  https://doi.org/10.1111/iej.12424CrossRefPubMedGoogle Scholar
  7. 7.
    Bang HJ, Park SY, Kim SE, Rahaman MDF, Ha SD (2017) Synergistic effects of combined ultrasound and peroxyacetic acid treatments against Cronobacter sakazakii biofilms on fresh cucumber. LWT Food Sci Technol 84(Supplement C):91–98.  https://doi.org/10.1016/j.lwt.2017.05.037
  8. 8.
    Barton E, Borman A, Johnson E, Sherlock J, Giles A (2016) Pseudo-outbreak of Fusarium oxysporum associated with bronchoscopy. J Hosp Infect 94(2):197–198.  https://doi.org/10.1016/j.jhin.2016.06.016CrossRefPubMedGoogle Scholar
  9. 9.
    Belessi CE, Gounadaki AS, Psomas AN, Skandamis PN (2011) Efficiency of different sanitation methods on Listeria monocytogenes biofilms formed under various environmental conditions. Int J Food Microbiol 145(Suppl 1):S46–52.  https://doi.org/10.1016/j.ijfoodmicro.2010.10.020CrossRefPubMedGoogle Scholar
  10. 10.
    Biswal BK, Khairallah R, Bibi K, Mazza A, Gehr R, Masson L, Frigon D (2014) Impact of UV and peracetic acid disinfection on the prevalence of virulence and antimicrobial resistance genes in uropathogenic Escherichia coli in wastewater effluents. Appl Environ Microbiol 80(12):3656–3666.  https://doi.org/10.1128/aem.00418-14CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Bore E, Langsrud S (2005) Characterization of micro-organisms isolated from dairy industry after cleaning and fogging disinfection with alkyl amine and peracetic acid. J Appl Microbiol 98(1):96–105.  https://doi.org/10.1111/j.1365-2672.2004.02436.xCrossRefPubMedGoogle Scholar
  12. 12.
    Bradley CR, Babb JR, Ayliffe GA (1995) Evaluation of the steris system 1 peracetic acid endoscope processor. J Hosp Infect 29(2):143–151CrossRefPubMedGoogle Scholar
  13. 13.
    Bridier A, Briandet R, Thomas V, Dubois-Brissonnet F (2011) Comparative biocidal activity of peracetic acid, benzalkonium chloride and ortho-phthalaldehyde on 77 bacterial strains. J Hosp Infect 78(3):208–213.  https://doi.org/10.1016/j.jhin.2011.03.014CrossRefPubMedGoogle Scholar
  14. 14.
    Bridier A, Dubois-Brissonnet F, Greub G, Thomas V, Briandet R (2011) Dynamics of the action of biocides in Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 55(6):2648–2654.  https://doi.org/10.1128/aac.01760-10CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Bridier A, Sanchez-Vizuete Mdel P, Le Coq D, Aymerich S, Meylheuc T, Maillard JY, Thomas V, Dubois-Brissonnet F, Briandet R (2012) Biofilms of a Bacillus subtilis hospital isolate protect Staphylococcus aureus from biocide action. PLoS ONE 7(9):e44506.  https://doi.org/10.1371/journal.pone.0044506CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Bundgaard-Nielsen K, Nielsen PV (1996) Fungicidal effect of 15 disinfectants against 25 fungal contaminants commonly found in bread and cheese manufacturing. J Food Prot 59(3):268–275CrossRefPubMedGoogle Scholar
  17. 17.
    Burgess W, Margolis A, Gibbs S, Duarte RS, Jackson M (2017) Disinfectant susceptibility profiling of glutaraldehyde-resistant nontuberculous mycobacteria. Infect Control Hosp Epidemiol 38(7):784–791.  https://doi.org/10.1017/ice.2017.75CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Cadnum JL, Jencson AL, O’Donnell MC, Flannery ER, Nerandzic MM, Donskey CJ (2017) An increase in healthcare-associated clostridium difficile infection associated with use of a defective peracetic acid-based surface disinfectant. Infect Control Hosp Epidemiol 38(3):300–305.  https://doi.org/10.1017/ice.2016.275CrossRefPubMedGoogle Scholar
  19. 19.
    Candeliere A, Campese E, Donatiello A, Pagano S, Iatarola M, Tolve F, Antonino L, Fasanella A (2016) Biocidal and sporicidal efficacy of pathoster ((R)) 0.35% and pathoster ((R)) 0.50% against bacterial agents in potential bioterrorism use. Health Security 14(4):250–257.  https://doi.org/10.1089/hs.2016.0003
  20. 20.
    Chang W, Small DA, Toghrol F, Bentley WE (2005) Microarray analysis of toxicogenomic effects of peracetic acid on Pseudomonas aeruginosa. Environ Sci Technol 39(15):5893–5899CrossRefPubMedGoogle Scholar
  21. 21.
    Chang W, Toghrol F, Bentley WE (2006) Toxicogenomic response of Staphylococcus aureus to peracetic acid. Environ Sci Technol 40(16):5124–5131CrossRefPubMedGoogle Scholar
  22. 22.
    Chenjiao W, Hongyan Z, Qing G, Xiaoqi Z, Liying G, Ying F (2016) In-use evaluation of peracetic acid for high-level disinfection of endoscopes. Gastroenterol Nursing: Off J Soc Gastroenterol Nurses Assoc 39(2):116–120.  https://doi.org/10.1097/sga.0000000000000192CrossRefGoogle Scholar
  23. 23.
    Clapp PA, Davies MJ, French MS, Gilbert BC (1994) The bactericidal action of peroxides; an E.P.R. spin-trapping study. Free Radical Res 21(3):147–167CrossRefGoogle Scholar
  24. 24.
    Costa SA, Paula OF, Silva CR, Leao MV, Santos SS (2015) Stability of antimicrobial activity of peracetic acid solutions used in the final disinfection process. Brazilian Oral Res 29.  https://doi.org/10.1590/1807-3107bor-2015.vol29.0038
  25. 25.
    Cronmiller JR, Nelson DK, Jackson DK, Kim CH (1999) Efficacy of conventional endoscopic disinfection and sterilization methods against Helicobacter pylori contamination. Helicobacter 4(3):198–203CrossRefPubMedGoogle Scholar
  26. 26.
    Cronmiller JR, Nelson DK, Salman G, Jackson DK, Dean RS, Hsu JJ, Kim CH (1999) Antimicrobial efficacy of endoscopic disinfection procedures: a controlled, multifactorial investigation. Gastrointest Endosc 50(2):152–158CrossRefPubMedGoogle Scholar
  27. 27.
    Cruz CD, Fletcher GC (2012) Assessing manufacturers’ recommended concentrations of commercial sanitizers on inactivation of Listeria monocytogenes. Food Control 26(1):194–199.  https://doi.org/10.1016/j.foodcont.2012.01.041CrossRefGoogle Scholar
  28. 28.
    Das JR, Bhakoo M, Jones MV, Gilbert P (1998) Changes in the biocide susceptibility of Staphylococcus epidermidis and Escherichia coli cells associated with rapid attachment to plastic surfaces. J Appl Microbiol 84(5):852–858CrossRefPubMedGoogle Scholar
  29. 29.
    de Souza EL, Meira QG, de Medeiros Barbosa I, Athayde AJ, da Conceicao ML, de Siqueira Junior JP (2014) Biofilm formation by Staphylococcus aureus from food contact surfaces in a meat-based broth and sensitivity to sanitizers. Brazilian J Microbiol: [Publication of the Brazilian Society for Microbiology] 45(1):67–75CrossRefGoogle Scholar
  30. 30.
    Deshpande A, Mana TS, Cadnum JL, Jencson AC, Sitzlar B, Fertelli D, Hurless K, Kundrapu S, Sunkesula VC, Donskey CJ (2014) Evaluation of a sporicidal peracetic acid/hydrogen peroxide-based daily disinfectant cleaner. Infect Control Hosp Epidemiol 35(11):1414–1416.  https://doi.org/10.1086/678416CrossRefPubMedGoogle Scholar
  31. 31.
    Deva AK, Vickery K, Zou J, West RH, Selby W, Benn RA, Harris JP, Cossart YE (1998) Detection of persistent vegetative bacteria and amplified viral nucleic acid from in-use testing of gastrointestinal endoscopes. J Hosp Infect 39(2):149–157CrossRefPubMedGoogle Scholar
  32. 32.
    Di Cesare A, Fontaneto D, Doppelbauer J, Corno G (2016) Fitness and recovery of bacterial communities and antibiotic resistance genes in urban wastewaters exposed to classical disinfection treatments. Environ Sci Technol 50(18):10153–10161.  https://doi.org/10.1021/acs.est.6b02268CrossRefPubMedGoogle Scholar
  33. 33.
    Dominciano LCC, Oliveira CAF, Lee SH, Corassin CH (2016) Individual and combined antimicrobial activity of oleuropein and chemical sanitizers. J Food Chem Nanotechnol 2(3):124–127Google Scholar
  34. 34.
    dos Anjos MM, Ruiz SP, Nakamura CV, de Abreu Filho BA (2013) Resistance of Alicyclobacillus acidoterrestris spores and biofilm to industrial sanitizers. J Food Prot 76(8):1408–1413.  https://doi.org/10.4315/0362-028x.jfp-13-020CrossRefPubMedGoogle Scholar
  35. 35.
    Dubois-Brissonnet F, Naitali M, Mafu AA, Briandet R (2011) Induction of fatty acid composition modifications and tolerance to biocides in Salmonella enterica serovar Typhimurium by plant-derived terpenes. Appl Environ Microbiol 77(3):906–910.  https://doi.org/10.1128/aem.01480-10CrossRefPubMedGoogle Scholar
  36. 36.
    Duc DL, Ribiollet A, Dode X, Ducel G, Marchetti B, Calop J (2001) Evaluation of the microbicidal efficacy of Steris System I for digestive endoscopes using GERMANDE and ASTM validation protocols. J Hosp Infect 48(2):135–141.  https://doi.org/10.1053/jhin.2001.0900CrossRefPubMedGoogle Scholar
  37. 37.
    El-Azizi M, Farag N, Khardori N (2016) Efficacy of selected biocides in the decontamination of common nosocomial bacterial pathogens in biofilm and planktonic forms. Comp Immunol Microbiol Infect Dis 47:60–71.  https://doi.org/10.1016/j.cimid.2016.06.002CrossRefPubMedGoogle Scholar
  38. 38.
    Espigares E, Bueno A, Espigares M, Galvez R (2006) Isolation of Salmonella serotypes in wastewater and effluent: effect of treatment and potential risk. Int J Hyg Environ Health 209(1):103–107.  https://doi.org/10.1016/j.ijheh.2005.08.006CrossRefPubMedGoogle Scholar
  39. 39.
    Espigares E, Bueno A, Fernandez-Crehuet M, Espigares M (2003) Efficacy of some neutralizers in suspension tests determining the activity of disinfectants. J Hosp Infect 55(2):137–140CrossRefPubMedGoogle Scholar
  40. 40.
    Espigares E, Moreno Roldan E, Espigares M, Abreu R, Castro B, Dib AL, Arias A (2017) Phenotypic resistance to disinfectants and antibiotics in methicillin-resistant Staphylococcus aureus strains isolated from pigs. Zoonoses Public Health 64(4):272–280.  https://doi.org/10.1111/zph.12308CrossRefPubMedGoogle Scholar
  41. 41.
    European Chemicals Agency (ECHA) Peracetic acid. Substance information. https://echa.europa.eu/substance-information/-/substanceinfo/100.001.079. Accessed 25 Oct 2017
  42. 42.
    European Chemicals Agency (ECHA) (2015) Opinion on the application for approval of the active substance: peracetic acid. Product-type: 2. ECHA/BPC/068/2015. https://echa.europa.eu/documents/10162/e10165ca10148f10165-10168c10158-10164baf-10168ced-10162ece65470ffa
  43. 43.
    Exner M, Tuschewitzki GJ, Scharnagel J (1987) Influence of biofilms by chemical disinfectants and mechanical cleaning. Zentralbl Bakteriol Mikrobiol Hyg B 183(5–6):549–563PubMedGoogle Scholar
  44. 44.
    Fagerlund A, Moretro T, Heir E, Briandet R, Langsrud S (2017) Cleaning and disinfection of biofilms composed of Listeria monocytogenes and background microbiota from meat processing surfaces. Appl Environ Microbiol.  https://doi.org/10.1128/aem.01046-17CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Fatemi P, Frank JF (1999) Inactivation of Listeria monocytogenes/Pseudomonas biofilms by peracid sanitizers. J Food Prot 62(7):761–765CrossRefPubMedGoogle Scholar
  46. 46.
    Finland (2015) Assessment report. Peracetic acid. Product-types 1–6Google Scholar
  47. 47.
    Foliente RL, Kovacs BJ, Aprecio RM, Bains HJ, Kettering JD, Chen YK (2001) Efficacy of high-level disinfectants for reprocessing GI endoscopes in simulated-use testing. Gastrointest Endosc 53(4):456–462.  https://doi.org/10.1067/mge.2001.113380CrossRefPubMedGoogle Scholar
  48. 48.
    Gilbert P, Das JR, Jones MV, Allison DG (2001) Assessment of resistance towards biocides following the attachment of micro-organisms to, and growth on, surfaces. J Appl Microbiol 91(2):248–254CrossRefPubMedGoogle Scholar
  49. 49.
    Gkana EN, Giaouris ED, Doulgeraki AI, Kathariou S, Nychas GJE (2017) Biofilm formation by Salmonella Typhimurium and Staphylococcus aureus on stainless steel under either mono- or dual-species multi-strain conditions and resistance of sessile communities to sub-lethal chemical disinfection. Food Control 73 (Part B):838–846.  https://doi.org/10.1016/j.foodcont.2016.09.038
  50. 50.
    Gomes IB, Malheiro J, Mergulhao F, Maillard JY, Simoes M (2016) Comparison of the efficacy of natural-based and synthetic biocides to disinfect silicone and stainless steel surfaces. Pathog Dis 74(4):ftw014.  https://doi.org/10.1093/femspd/ftw014
  51. 51.
    Grasteau A, Guiraud T, Daniel P, Calvez S, Chesneau V, Le Hénaff M (2015) Evaluation of glutaraldehyde, chloramine-t, bronopol, incimaxx aquatic® and hydrogen peroxide as biocides against flavobacterium psychrophilum for sanitization of rainbow trout eyed eggs. J Aquac Res Develop 6(12):382CrossRefGoogle Scholar
  52. 52.
    Griffiths PA, Babb JR, Bradley CR, Fraise AP (1997) Glutaraldehyde-resistant Mycobacterium chelonae from endoscope washer disinfectors. J Appl Microbiol 82(4):519–526CrossRefPubMedGoogle Scholar
  53. 53.
    Griffiths PA, Babb JR, Fraise AP (1999) Mycobactericidal activity of selected disinfectants using a quantitative suspension test. J Hosp Infect 41(2):111–121CrossRefPubMedGoogle Scholar
  54. 54.
    Henoun Loukili N, Becker H, Harno J, Bientz M, Meunier O (2004) Effect of peracetic acid and aldehyde disinfectants on biofilm. J Hosp Infect 58(2):151–154CrossRefPubMedGoogle Scholar
  55. 55.
    Hernández A, Martró E, Matas L, Ausina V (2003) In-vitro evaluation of Perasafe compared with 2% alkaline glutaraldehyde against Mycobacterium spp. J Hosp Infect 54(1):52–56CrossRefPubMedGoogle Scholar
  56. 56.
    Hernández A, Martró E, Puzo C, Matas L, Burgués C, Vázquez N, Castella J, Ausina V (2003) In-use evaluation of Perasafe compared with Cidex in fibreoptic bronchoscope disinfection. J Hosp Infect 54(1):46–51Google Scholar
  57. 57.
    Herruzo R, Vizcaino MJ, Herruzo I (2010) Efficacy of a new peracetic acid-based disinfectant agent (‘Adaspor ready to use’). J Hosp Infect 74(2):192–193.  https://doi.org/10.1016/j.jhin.2009.10.019CrossRefPubMedGoogle Scholar
  58. 58.
    Holton J, Nye P, McDonald V (1994) Efficacy of selected disinfectants against mycobacteria and cryptosporidia. J Hosp Infect 27(2):105–115CrossRefPubMedGoogle Scholar
  59. 59.
    Holton J, Shetty N, McDonald V (1995) Efficacy of ‘Nu-Cidex’ (0.35% peracetic acid) against mycobacteria and cryptosporidia. J Hosp Infect 31(3):235–237CrossRefPubMedGoogle Scholar
  60. 60.
    Humphreys PN, Finan P, Rout S, Hewitt J, Thistlethwaite P, Barnes S, Pilling S (2013) A systematic evaluation of a peracetic-acid-based high performance disinfectant. J Infect Prevent 14(4):126–131.  https://doi.org/10.1177/1757177413476125CrossRefGoogle Scholar
  61. 61.
    Jackson J, Leggett JE, Wilson DA, Gilbert DN (1996) Mycobacterium gordonae in fiberoptic bronchoscopes. Am J Infect Control 24(1):19–23CrossRefPubMedGoogle Scholar
  62. 62.
    Jaglic Z, Červinková D, Vlková H, Michu E, Kunová G, Babák V (2012) Bacterial biofilms resist oxidising agents due to the presence of organic matter. Czech J Food Sci 30(2):178–187CrossRefGoogle Scholar
  63. 63.
    Jolivet-Gougeon A, Sauvager F, Arturo-Schaan M, Bonnaure-Mallet M, Cormier M (2003) Influence of peracetic acid on adhesion/invasion of Salmonella enterica serotype typhimurium LT2. Cell Biol Toxicol 19(2):83–93CrossRefPubMedGoogle Scholar
  64. 64.
    Jolivet-Gougeon A, Sauvager F, Bonnaure-Mallet M, Colwell RR, Cormier M (2006) Virulence of viable but nonculturable S. Typhimurium LT2 after peracetic acid treatment. Int J Food Microbiol 112(2):147–152.  https://doi.org/10.1016/j.ijfoodmicro.2006.06.019CrossRefPubMedGoogle Scholar
  65. 65.
    Juncker JC (2016) COMMISSION IMPLEMENTING REGULATION (EU) 2016/672 of 29 April 2016 approving peracetic acid as an existing active substance for use in biocidal products for product-types 1, 2, 3, 4, 5 and 6. Off J Eur Union 59(L 116):3–7Google Scholar
  66. 66.
    Juncker JC (2016) COMMISSION IMPLEMENTING REGULATION (EU) 2016/2290 of 16 December 2016 approving peracetic acid as an existing active substance for use in biocidal products of product-types 11 and 12. Off J Eur Union 59(L 344):71–73Google Scholar
  67. 67.
    Kampf G (2017) Black box oxidizers. Infect Control Hosp Epidemiol 38(11):1387–1388.  https://doi.org/10.1017/ice.2017.199CrossRefPubMedGoogle Scholar
  68. 68.
    Kassaify ZG, El Hakim RG, Rayya EG, Shaib HA, Barbour EK (2007) Preliminary study on the efficacy and safety of eight individual and blended disinfectants against poultry and dairy indicator organisms. Veterinaria Italiana 43(4):821–830PubMedGoogle Scholar
  69. 69.
    Kastbjerg VG, Gram L (2012) Industrial disinfectants do not select for resistance in Listeria monocytogenes following long term exposure. Int J Food Microbiol 160(1):11–15.  https://doi.org/10.1016/j.ijfoodmicro.2012.09.009CrossRefPubMedGoogle Scholar
  70. 70.
    Kastbjerg VG, Larsen MH, Gram L, Ingmer H (2010) Influence of sublethal concentrations of common disinfectants on expression of virulence genes in Listeria monocytogenes. Appl Environ Microbiol 76(1):303–309.  https://doi.org/10.1128/aem.00925-09CrossRefPubMedGoogle Scholar
  71. 71.
    Katara G, Hemvani N, Chitnis S, Chitnis V, Chitnis D (2016) Efficacy studies on peracetic acid against pathogenic microorganisms. J Patient Saf Infect Control 4(1):17–21.  https://doi.org/10.4103/2214-207x.203545CrossRefGoogle Scholar
  72. 72.
    Kean R, Sherry L, Townsend E, McKloud E, Short B, Akinbobola A, Mackay WG, Williams C, Jones BL, Ramage G (2018) Surface disinfection challenges for Candida auris: an in-vitro study. J Hosp Infect 98(4):433–436.  https://doi.org/10.1016/j.jhin.2017.11.015CrossRefPubMedGoogle Scholar
  73. 73.
    Konrat K, Schwebke I, Laue M, Dittmann C, Levin K, Andrich R, Arvand M, Schaudinn C (2016) The bead assay for biofilms: a quick, easy and robust method for testing disinfectants. PLoS ONE 11(6):e0157663.  https://doi.org/10.1371/journal.pone.0157663CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Korukluoglu M, Sahan Y, Yigit A (2006) The fungicidal efficacy of various commercial disinfectants used in the food industry. Ann Microbiol 56(4):325–330CrossRefGoogle Scholar
  75. 75.
    Köse H, Yapar N (2017) The comparison of various disinfectants’ efficacy on Staphylococcus aureus and Pseudomonas aeruginosa biofilm layers. Turkish J Med Sci 47(4):1287–1294CrossRefGoogle Scholar
  76. 76.
    Kostaki M, Chorianopoulos N, Braxou E, Nychas GJ, Giaouris E (2012) Differential biofilm formation and chemical disinfection resistance of sessile cells of Listeria monocytogenes strains under monospecies and dual-species (with Salmonella enterica) conditions. Appl Environ Microbiol 78(8):2586–2595.  https://doi.org/10.1128/aem.07099-11CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    La Scola B, Rolain J-M, Maurin M, Raoult D (2003) Can Whipple’s disease be transmitted by gastroscopes? Infect Control Hosp Epidemiol 24(3):191–194CrossRefPubMedGoogle Scholar
  78. 78.
    Lagace L, Jacques M, Mafu AA, Roy D (2006) Biofilm formation and biocides sensitivity of Pseudomonas marginalis isolated from a maple sap collection system. J Food Prot 69(10):2411–2416CrossRefPubMedGoogle Scholar
  79. 79.
    Lalueza P, Carmona D, Monzón M, Arruebo M, Santamaría J (2012) Strong bactericidal synergy between peracetic acid and silver-exchanged zeolites. Microporous Mesoporous Mater 156(Supplement C):171–175.  https://doi.org/10.1016/j.micromeso.2012.02.035
  80. 80.
    Langsrud S, Moretro T, Sundheim G (2003) Characterization of Serratia marcescens surviving in disinfecting footbaths. J Appl Microbiol 95(1):186–195CrossRefPubMedGoogle Scholar
  81. 81.
    Lee SH, Cappato LP, Corassin CH, Cruz AG, Oliveira CA (2016) Effect of peracetic acid on biofilms formed by Staphylococcus aureus and Listeria monocytogenes isolated from dairy plants. J Dairy Sci 99(3):2384–2390.  https://doi.org/10.3168/jds.2015-10007CrossRefPubMedGoogle Scholar
  82. 82.
    Lorena NS, Pitombo MB, Cortes PB, Maya MC, Silva MG, Carvalho AC, Coelho FS, Miyazaki NH, Marques EA, Chebabo A, Freitas AD, Lupi O, Duarte RS (2010) Mycobacterium massiliense BRA100 strain recovered from postsurgical infections: resistance to high concentrations of glutaraldehyde and alternative solutions for high level disinfection. Acta cirurgica brasileira 25(5):455–459CrossRefPubMedGoogle Scholar
  83. 83.
    Loukili NH, Granbastien B, Faure K, Guery B, Beaucaire G (2006) Effect of different stabilized preparations of peracetic acid on biofilm. J Hosp Infect 63(1):70–72.  https://doi.org/10.1016/j.jhin.2005.11.015CrossRefPubMedGoogle Scholar
  84. 84.
    Luprano ML, De Sanctis M, Del Moro G, Di Iaconi C, Lopez A, Levantesi C (2016) Antibiotic resistance genes fate and removal by a technological treatment solution for water reuse in agriculture. Sci Total Environ 571:809–818.  https://doi.org/10.1016/j.scitotenv.2016.07.055CrossRefPubMedGoogle Scholar
  85. 85.
    Lynam PA, Babb JR, Fraise AP (1995) Comparison of the mycobactericidal activity of 2% alkaline glutaraldehyde and ‘Nu-Cidex’ (0.35% peracetic acid). J Hosp Infect 30(3):237–240CrossRefPubMedGoogle Scholar
  86. 86.
    Mariscal A, Lopez-Gigosos RM, Carnero-Varo M, Fernandez-Crehuet J (2009) Fluorescent assay based on resazurin for detection of activity of disinfectants against bacterial biofilm. Appl Microbiol Biotechnol 82(4):773–783.  https://doi.org/10.1007/s00253-009-1879-xCrossRefPubMedGoogle Scholar
  87. 87.
    Martín-Espada MC, D’ors A, Bartolomé MC, Pereira M, Sánchez-Fortún S (2014) Peracetic acid disinfectant efficacy against Pseudomonas aeruginosa biofilms on polystyrene surfaces and comparison between methods to measure it. LWT Food Sci Technol 56(1):58–61Google Scholar
  88. 88.
    Martin DJ, Denyer SP, McDonnell G, Maillard JY (2008) Resistance and cross-resistance to oxidising agents of bacterial isolates from endoscope washer disinfectors. J Hosp Infect 69(4):377–383.  https://doi.org/10.1016/j.jhin.2008.04.010CrossRefPubMedGoogle Scholar
  89. 89.
    Meade E, Garvey M (2018) Efficacy testing of novel chemical disinfectants on clinically relevant microbial pathogens. Am J Infect Control 46(1):44–49.  https://doi.org/10.1016/j.ajic.2017.07.001CrossRefPubMedGoogle Scholar
  90. 90.
    Melo RT, Mendonca EP, Monteiro GP, Siqueira MC, Pereira CB, Peres P, Fernandez H, Rossi DA (2017) Intrinsic and extrinsic aspects on Campylobacter jejuni biofilms. Front Microbiol 8:1332.  https://doi.org/10.3389/fmicb.2017.01332CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Meylheuc T, Renault M, Bellon-Fontaine MN (2006) Adsorption of a biosurfactant on surfaces to enhance the disinfection of surfaces contaminated with Listeria monocytogenes. Int J Food Microbiol 109(1–2):71–78.  https://doi.org/10.1016/j.ijfoodmicro.2006.01.013CrossRefPubMedGoogle Scholar
  92. 92.
    Middleton AM, Chadwick MV, Gaya H (1997) Disinfection of bronchoscopes, contaminated in vitro with Mycobacterium tuberculosis, Mycobacterium avium-intracellulare and Mycobacterium chelonae in sputum, using stabilized, buffered peracetic acid solution (‘Nu-Cidex’). J Hosp Infect 37(2):137–143CrossRefPubMedGoogle Scholar
  93. 93.
    Montebugnoli L, Chersoni S, Prati C, Dolci G (2004) A between-patient disinfection method to control water line contamination and biofilm inside dental units. J Hosp Infect 56(4):297–304.  https://doi.org/10.1016/j.jhin.2004.01.015CrossRefPubMedGoogle Scholar
  94. 94.
    Nakayama M, Hosoya K, Tomiyama D, Tsugukuni T, Matsuzawa T, Imanishi Y, Yaguchi T (2013) Method for rapid detection and identification of chaetomium and evaluation of resistance to peracetic acid. J Food Prot 76(6):999–1005.  https://doi.org/10.4315/0362-028x.jfp-12-543CrossRefPubMedGoogle Scholar
  95. 95.
    Neo SY, Lim PY, Phua LK, Khoo GH, Kim SJ, Lee SC, Yuk HG (2013) Efficacy of chlorine and peroxyacetic acid on reduction of natural microflora, Escherichia coli O157:H7, Listeria monocyotgenes and Salmonella spp. on mung bean sprouts. Food Microbiol 36(2):475–480.  https://doi.org/10.1016/j.fm.2013.05.001CrossRefPubMedGoogle Scholar
  96. 96.
    Neves MS, da Silva MG, Ventura GM, Cortes PB, Duarte RS, de Souza HS (2016) Effectiveness of current disinfection procedures against biofilm on contaminated GI endoscopes. Gastrointest Endosc 83(5):944–953.  https://doi.org/10.1016/j.gie.2015.09.016CrossRefPubMedGoogle Scholar
  97. 97.
    Ntsama-Essomba C, Bouttier S, Ramaldes M, Dubois-Brissonnet F, Fourniat J (1997) Resistance of Escherichia coli growing as biofilms to disinfectants. Vet Res 28(4):353–363PubMedGoogle Scholar
  98. 98.
    Penna TC, Mazzola PG, Silva Martins AM (2001) The efficacy of chemical agents in cleaning and disinfection programs. BMC Infect Dis 1:16CrossRefPubMedPubMedCentralGoogle Scholar
  99. 99.
    Pineau L, Desbuquois C, Marchetti B, Luu Duc D (2008) Comparison of the fixative properties of five disinfectant solutions. J Hosp Infect 68(2):171–177.  https://doi.org/10.1016/j.jhin.2007.10.021CrossRefPubMedGoogle Scholar
  100. 100.
    Pires RH, da Silva Jde F, Gomes Martins CH, Fusco Almeida AM, Pienna Soares C, Soares Mendes-Giannini MJ (2013) Effectiveness of disinfectants used in hemodialysis against both Candida orthopsilosis and C. parapsilosis sensu stricto biofilms. Antimicrob Agents Chemother 57(5):2417–2421.  https://doi.org/10.1128/aac.01308-12CrossRefPubMedPubMedCentralGoogle Scholar
  101. 101.
    Poimenidou SV, Chrysadakou M, Tzakoniati A, Bikouli VC, Nychas GJ, Skandamis PN (2016) Variability of Listeria monocytogenes strains in biofilm formation on stainless steel and polystyrene materials and resistance to peracetic acid and quaternary ammonium compounds. Int J Food Microbiol 237:164–171.  https://doi.org/10.1016/j.ijfoodmicro.2016.08.029CrossRefPubMedGoogle Scholar
  102. 102.
    Reis L, Zanetti AL, Castro Junior OV, Martinez EF (2012) Use of 0.25% and 0.025% peracetic acid as disinfectant agent for chemically activated acrylic resin: an in vitro study. Rev Gaúcha Odontol 60(3):315–320Google Scholar
  103. 103.
    Ruckerl I, Muhterem-Uyar M, Muri-Klinger S, Wagner KH, Wagner M, Stessl B (2014) L. monocytogenes in a cheese processing facility: Learning from contamination scenarios over three years of sampling. Int J Food Microbiol 189:98–105.  https://doi.org/10.1016/j.ijfoodmicro.2014.08.001CrossRefPubMedGoogle Scholar
  104. 104.
    Saa Ibusquiza P, Herrera JJ, Cabo ML (2011) Resistance to benzalkonium chloride, peracetic acid and nisin during formation of mature biofilms by Listeria monocytogenes. Food Microbiol 28(3):418–425.  https://doi.org/10.1016/j.fm.2010.09.014CrossRefPubMedGoogle Scholar
  105. 105.
    Sagripanti J-L, Eklund CA, Trost PA, Jinneman KC, Abeyta C, Kaysner CA, Hill WE (1997) Comparative sensitivity of 13 species of pathogenic bacteria to seven chemical germicides. Am J Infect Control 25(4):335–339CrossRefPubMedGoogle Scholar
  106. 106.
    Sattar SA, Kibbee RJ, Tetro JA, Rook TA (2006) Experimental evaluation of an automated endoscope reprocessor with in situ generation of peracetic acid for disinfection of semicritical devices. Infect Control Hosp Epidemiol 27(11):1193–1199.  https://doi.org/10.1086/508830CrossRefPubMedGoogle Scholar
  107. 107.
    Shetty N, Srinivasan S, Holton J, Ridgway GL (1999) Evaluation of microbicidal activity of a new disinfectant: Sterilox 2500 against Clostridium difficile spores, Helicobacter pylori, vancomycin resistant Enterococcus species, Candida albicans and several Mycobacterium species. J Hosp Infect 41:101–105CrossRefPubMedGoogle Scholar
  108. 108.
    Sisti M, Brandi G, De Santi M, Rinaldi L, Schiavano GF (2012) Disinfection efficacy of chlorine and peracetic acid alone or in combination against Aspergillus spp. and Candida albicans in drinking water. J Water Health 10(1):11–19.  https://doi.org/10.2166/wh.2011.150CrossRefPubMedGoogle Scholar
  109. 109.
    Sofokleous P, Ali S, Wilson P, Buanz A, Gaisford S, Mistry D, Fellows A, Day RM (2017) Sustained antimicrobial activity and reduced toxicity of oxidative biocides through biodegradable microparticles. Acta Biomater 64:301–312.  https://doi.org/10.1016/j.actbio.2017.10.001CrossRefPubMedPubMedCentralGoogle Scholar
  110. 110.
    Sorin M, Segal-Maurer S, Mariano N, Urban C, Combest A, Rahal JJ (2001) Nosocomial transmission of imipenem-resistant Pseudomonas aeruginosa following bronchoscopy associated with improper connection to the Steris System 1 processor. Infect Control Hosp Epidemiol 22(7):409–413.  https://doi.org/10.1086/501925CrossRefPubMedGoogle Scholar
  111. 111.
    Stanley PM (1999) Efficacy of peroxygen compounds against glutaraldehyde-resistant mycobacteria. Am J Infect Control 27(4):339–343CrossRefPubMedGoogle Scholar
  112. 112.
    Stigt JA, Wolfhagen MJ, Smulders P, Lammers V (2015) The Identification of Stenotrophomonas maltophilia contamination in ultrasound endoscopes and reproduction of decontamination failure by deliberate soiling tests. Respiration; Int Rev Thoracic Dis 89(6):565–571.  https://doi.org/10.1159/000381725CrossRefGoogle Scholar
  113. 113.
    Stopforth JD, Samelis J, Sofos JN, Kendall PA, Smith GC (2003) Influence of extended acid stressing in fresh beef decontamination runoff fluids on sanitizer resistance of acid-adapted Escherichia coli O157:H7 in biofilms. J Food Prot 66(12):2258–2266CrossRefPubMedGoogle Scholar
  114. 114.
    Surdeau N, Laurent-Maquin D, Bouthors S, Gelle MP (2006) Sensitivity of bacterial biofilms and planktonic cells to a new antimicrobial agent, Oxsil 320N. J Hosp Infect 62(4):487–493.  https://doi.org/10.1016/j.jhin.2005.09.003CrossRefPubMedGoogle Scholar
  115. 115.
    Tote K, Horemans T, Vanden Berghe D, Maes L, Cos P (2010) Inhibitory effect of biocides on the viable masses and matrices of Staphylococcus aureus and Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 76(10):3135–3142.  https://doi.org/10.1128/aem.02095-09CrossRefPubMedPubMedCentralGoogle Scholar
  116. 116.
    Trachoo N, Frank JF (2002) Effectiveness of chemical sanitizers against Campylobacter jejuni-containing biofilms. J Food Prot 65(7):1117–1121CrossRefPubMedGoogle Scholar
  117. 117.
    Turolla A, Sabatino R, Fontaneto D, Eckert EM, Colinas N, Corno G, Citterio B, Biavasco F, Antonelli M, Mauro A, Mangiaterra G, Di Cesare A (2017) Defence strategies and antibiotic resistance gene abundance in enterococci under stress by exposure to low doses of peracetic acid. Chemosphere 185:480–488.  https://doi.org/10.1016/j.chemosphere.2017.07.032CrossRefPubMedGoogle Scholar
  118. 118.
    United States Environmental Protection Agency (1993) EPA R.E.D. Facts. Peroxy Compounds. https://www3.epa.gov/pesticides/chem_search/reg_actions/reregistration/red_G-67_1-Dec-93.pdf
  119. 119.
    van der Veen S, Abee T (2010) HrcA and DnaK are important for static and continuous-flow biofilm formation and disinfectant resistance in Listeria monocytogenes. Microbiology (Reading, England) 156(Pt 12):3782–3790.  https://doi.org/10.1099/mic.0.043000-0
  120. 120.
    van der Veen S, Abee T (2011) Mixed species biofilms of Listeria monocytogenes and Lactobacillus plantarum show enhanced resistance to benzalkonium chloride and peracetic acid. Int J Food Microbiol 144(3):421–431.  https://doi.org/10.1016/j.ijfoodmicro.2010.10.029CrossRefPubMedGoogle Scholar
  121. 121.
    van Klingeren B, Pullen W (1993) Glutaraldehyde resistant mycobacteria from endoscope washers. J Hosp Infect 25(2):147–149CrossRefPubMedGoogle Scholar
  122. 122.
    Vázquez-Sánchez D, Cabo ML, Ibusquiza PS, Rodríguez-Herrera JJ (2014) Biofilm-forming ability and resistance to industrial disinfectants of Staphylococcus aureus isolated from fishery products. Food Control 39(Supplement C):8–16.  https://doi.org/10.1016/j.foodcont.2013.09.029
  123. 123.
    Verner–Jeffreys DW, Joiner CL, Bagwell NJ, Reese RA, Husby A, Dixon PF (2009) Development of bactericidal and virucidal testing standards for aquaculture disinfectants. Aquaculture 286(3):190–197.  https://doi.org/10.1016/j.aquaculture.2008.10.001
  124. 124.
    Vesley D, Melson J, Stanley P (1999) Microbial bioburden in endoscope reprocessing and an in-use evaluation of the high-level disinfection capabilities of Cidex PA. Gastroenterol Nursing: Off J Soc Gastroenterol Nurses Assoc 22(2):63–68CrossRefGoogle Scholar
  125. 125.
    Vieira CD, Farias Lde M, Diniz CG, Alvarez-Leite ME, Camargo ER, Carvalho MA (2005) New methods in the evaluation of chemical disinfectants used in health care services. Am J Infect Control 33(3):162–169.  https://doi.org/10.1016/j.ajic.2004.10.007CrossRefPubMedGoogle Scholar
  126. 126.
    Vizcaino-Alcaide MJ, Herruzo-Cabrera R, Fernandez-Acenero MJ (2003) Comparison of the disinfectant efficacy of Perasafe and 2% glutaraldehyde in in vitro tests. J Hosp Infect 53:124–128CrossRefPubMedGoogle Scholar
  127. 127.
    Walsh SE, Maillard JY, Russell AD (1999) Ortho-phthalaldehyde: a possible alternative to glutaraldehyde for high level disinfection. J Appl Microbiol 86(6):1039–1046CrossRefPubMedGoogle Scholar
  128. 128.
    Wang GQ, Zhang CW, Liu HC, Chen ZB (2005) Comparison of susceptibilities of M. tuberculosis H37Ra and M. chelonei subsp. abscessus to disinfectants. Biomed Environ Sci: BES 18(2):124–127Google Scholar
  129. 129.
    Wessels S, Ingmer H (2013) Modes of action of three disinfectant active substances: a review. Regul Toxicol Pharmacol: RTP 67(3):456–467.  https://doi.org/10.1016/j.yrtph.2013.09.006CrossRefPubMedGoogle Scholar
  130. 130.
    Witney AA, Gould KA, Pope CF, Bolt F, Stoker NG, Cubbon MD, Bradley CR, Fraise A, Breathnach AS, Butcher PD, Planche TD, Hinds J (2014) Genome sequencing and characterization of an extensively drug-resistant sequence type 111 serotype O12 hospital outbreak strain of Pseudomonas aeruginosa. Clin Microbiol Infect 20(10):O609–618.  https://doi.org/10.1111/1469-0691.12528CrossRefPubMedGoogle Scholar
  131. 131.
    Wuthiekanun V, Wongsuwan G, Pangmee S, Teerawattanasook N, Day NP, Peacock SJ (2011) Perasafe, Virkon and bleach are bactericidal for Burkholderia pseudomallei, a select agent and the cause of melioidosis. J Hosp Infect 77(2):183–184.  https://doi.org/10.1016/j.jhin.2010.06.026CrossRefPubMedPubMedCentralGoogle Scholar
  132. 132.
    Zanotto C, Bissa M, Illiano E, Mezzanotte V, Marazzi F, Turolla A, Antonelli M, De Giuli Morghen C, Radaelli A (2016) Identification of antibiotic-resistant Escherichia coli isolated from a municipal wastewater treatment plant. Chemosphere 164:627–633.  https://doi.org/10.1016/j.chemosphere.2016.08.040CrossRefPubMedGoogle Scholar
  133. 133.
    Zhang K, Zhou X, Du P, Zhang T, Cai M, Sun P, Huang CH (2017) Oxidation of beta-lactam antibiotics by peracetic acid: reaction kinetics, product and pathway evaluation. Water Res 123:153–161.  https://doi.org/10.1016/j.watres.2017.06.057CrossRefPubMedGoogle Scholar
  134. 134.
    Zook CD, Busta FF, Brady LJ (2001) Sublethal sanitizer stress and adaptive response of Escherichia coli O157:H7. J Food Prot 64(6):767–769CrossRefPubMedGoogle Scholar

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© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Institute of Hygiene and Environmental MedicineUniversity of GreifswaldGreifswaldGermany

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