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Hydrogen Peroxide

  • Günter Kampf
Chapter

Abstract

Hydrogen peroxide is mostly bactericidal at 0.5% in 30 min and yeasticidal at 3% in 30 min. A comprehensive fungicidal activity was not seen with 3% hydrogen peroxide in 6 h, similar to a lack of a comprehensive mycobactericidal activity with 3% hydrogen peroxide in 1 h. High MIC values indicating resistance to hydrogen peroxide have so far not been reported. An epidemiological cut-off value to determine acquired resistance has not been proposed yet. Peroxidases and catalases encoded by various genes have been described as specific resistance mechanisms. No cross-tolerance to antibiotics has been reported. Low-level exposure can increase catalyse activity in S. Typhimurium and S. cerevisiae and can induce cross-resistance, e.g. to ethanol in S. cerevisiae. In most bacterial species, there is no or only a small MIC increase after low-level exposure. Hydrogen peroxide increases biofilm formation in A. oleivorans, P. aeruginosa and S. parasanguinis, whereas it is inhibited in Candida spp. In S. epidermidis. the effect depends on the hydrogen peroxide concentration (increase at 1%, inhibition at 0.02–0.25%). Biofilm removal is mostly moderate, e.g. between 55% and 63% for 3% hydrogen peroxide. The potential to cause biofilm fixation is unknown.

References

  1. 1.
    Aarestrup FM, Hasman H (2004) Susceptibility of different bacterial species isolated from food animals to copper sulphate, zinc chloride and antimicrobial substances used for disinfection. Vet Microbiol 100(1–2):83–89.  https://doi.org/10.1016/j.vetmic.2004.01.013CrossRefPubMedGoogle Scholar
  2. 2.
    Ali S, Muzslay M, Bruce M, Jeanes A, Moore G, Wilson AP (2016) Efficacy of two hydrogen peroxide vapour aerial decontamination systems for enhanced disinfection of meticillin-resistant Staphylococcus aureus, Klebsiella pneumoniae and Clostridium difficile in single isolation rooms. J Hosp Infect 93(1):70–77.  https://doi.org/10.1016/j.jhin.2016.01.016CrossRefPubMedGoogle Scholar
  3. 3.
    Angelillo IF, Bianco A, Nobile CG, Pavia M (1998) Evaluation of the efficacy of glutaraldehyde and peroxygen for disinfection of dental instruments. Lett Appl Microbiol 27(5):292–296CrossRefPubMedGoogle Scholar
  4. 4.
    Aparecida Guimaraes M, Rocchetto Coelho L, Rodrigues Souza R, Ferreira-Carvalho BT, Marie Sa Figueiredo A (2012) Impact of biocides on biofilm formation by methicillin-resistant Staphylococcus aureus (ST239-SCCmecIII) isolates. Microbiol Immunol 56(3):203–207.  https://doi.org/10.1111/j.1348-0421.2011.00423.xCrossRefPubMedGoogle Scholar
  5. 5.
    Assis ML, De Mattos JC, Caceres MR, Dantas FJ, Asad LM, Asad NR, Bezerra RJ, Caldeira-de-Araujo A, Bernardo-Filho M (2002) Adaptive response to H(2)O(2) protects against SnCl(2) damage: the OxyR system involvement. Biochimie 84(4):291–294CrossRefPubMedGoogle Scholar
  6. 6.
    Ban GH, Kang DH (2016) Effect of sanitizer combined with steam heating on the inactivation of foodborne pathogens in a biofilm on stainless steel. Food Microbiol 55:47–54.  https://doi.org/10.1016/j.fm.2015.11.003CrossRefPubMedGoogle Scholar
  7. 7.
    Bardouniotis E, Huddleston W, Ceri H, Olson ME (2001) Characterization of biofilm growth and biocide susceptibility testing of Mycobacterium phlei using the MBEC assay system. FEMS Microbiol Lett 203(2):263–267PubMedGoogle Scholar
  8. 8.
    Best M, Springthorpe VS, Sattar SA (1994) Feasibility of a combined carrier test for disinfectants: studies with a mixture of five types of microorganisms. Am J Infect Control 22(3):152–162CrossRefPubMedGoogle Scholar
  9. 9.
    Boles BR, Thoendel M, Singh PK (2004) Self-generated diversity produces “insurance effects” in biofilm communities. Proc Natl Acad Sci USA 101(47):16630–16635.  https://doi.org/10.1073/pnas.0407460101CrossRefPubMedGoogle Scholar
  10. 10.
    Borgmann-Strahsen R (2003) Comparative assessment of di#erent biocides in swimming pool water. Int Biodeter Biodegr 51(4):291–297CrossRefGoogle Scholar
  11. 11.
    Brinez WJ, Roig-Sagués AX, Hernández Herrero MM, López-Pedemonte T, Guamis B (2006) Bactericidal efficacy of peracetic acid in combination with hydrogen peroxide against pathogenic and non pathogenic strains of Staphylococcus spp., Listeria spp. and Escherichia coli. Food Control 17(7):516–521CrossRefGoogle Scholar
  12. 12.
    Buergers R, Rosentritt M, Schneider-Brachert W, Behr M, Handel G, Hahnel S (2008) Efficacy of denture disinfection methods in controlling Candida albicans colonization in vitro. Acta Odontol Scand 66(3):174–180.  https://doi.org/10.1080/00016350802165614CrossRefPubMedGoogle Scholar
  13. 13.
    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
  14. 14.
    Burgers R, Witecy C, Hahnel S, Gosau M (2012) The effect of various topical peri-implantitis antiseptics on Staphylococcus epidermidis, Candida albicans, and Streptococcus sanguinis. Arch Oral Biol 57(7):940–947.  https://doi.org/10.1016/j.archoralbio.2012.01.015CrossRefPubMedGoogle Scholar
  15. 15.
    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
  16. 16.
    Chaieb K, Zmantar T, Souiden Y, Mahdouani K, Bakhrouf A (2011) XTT assay for evaluating the effect of alcohols, hydrogen peroxide and benzalkonium chloride on biofilm formation of Staphylococcus epidermidis. Microb Pathog 50(1):1–5.  https://doi.org/10.1016/j.micpath.2010.11.004CrossRefPubMedGoogle Scholar
  17. 17.
    Choi NY, Baek SY, Yoon JH, Choi MR, Kang DH, Lee SY (2012) Efficacy of aerosolized hydrogen peroxide-based sanitizer on the reduction of pathogenic bacteria on a stainless steel surface. Food Control 27(1):57–63CrossRefGoogle Scholar
  18. 18.
    Christman MF, Morgan RW, Jacobson FS, Ames BN (1985) Positive control of a regulon for defenses against oxidative stress and some heat-shock proteins in Salmonella typhimurium. Cell 41(3):753–762CrossRefPubMedGoogle Scholar
  19. 19.
    da Costa Luciano C, Olson N, Tipple AF, Alfa M (2016) Evaluation of the ability of different detergents and disinfectants to remove and kill organisms in traditional biofilm. Am J Infect Control 44(11):e243–e249.  https://doi.org/10.1016/j.ajic.2016.03.040CrossRefGoogle Scholar
  20. 20.
    Derecho I, McCoy KB, Vaishampayan P, Venkateswaran K, Mogul R (2014) Characterization of hydrogen peroxide-resistant Acinetobacter species isolated during the Mars Phoenix spacecraft assembly. Astrobiology 14(10):837–847.  https://doi.org/10.1089/ast.2014.1193CrossRefPubMedGoogle Scholar
  21. 21.
    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
  22. 22.
    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
  23. 23.
    Duan D, Scoffield JA, Zhou X, Wu H (2016) Fine-tuned production of hydrogen peroxide promotes biofilm formation of Streptococcus parasanguinis by a pathogenic cohabitant Aggregatibacter actinomycetemcomitans. Environ Microbiol 18(11):4023–4036.  https://doi.org/10.1111/1462-2920.13425CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Dukan S, Touati D (1996) Hypochlorous acid stress in Escherichia coli: resistance, DNA damage, and comparison with hydrogen peroxide stress. J Bacteriol 178(21):6145–6150CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Eissa ME, Abd El Naby M, Beshir MM (2014) Bacterial versus fungal spore resistance to peroxygen biocide on inanimate surfaces. Bull Facult Pharm 52 (2):219–224. doi: https://doi.org/10.1016/j.bfopcu.2014.06.003
  26. 26.
    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
  27. 27.
    Engelmann S, Hecker M (1996) Impaired oxidative stress resistance of Bacillus subtilis sigB mutants and the role of katA and katE. FEMS Microbiol Lett 145(1):63–69CrossRefPubMedGoogle Scholar
  28. 28.
    European Chemicals Agency (ECHA) Hydrogen peroxide. Substance information. https://echa.europa.eu/substance-information/-/substanceinfo/100.028.878. Accessed 12 Oct 2017
  29. 29.
    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
  30. 30.
    Faguy DM, Doolittle WF (2000) Horizontal transfer of catalase-peroxidase genes between archaea and pathogenic bacteria. Trends Genet: TIG 16(5):196–197CrossRefPubMedGoogle Scholar
  31. 31.
    Ferguson JW, Hatton JF, Gillespie MJ (2002) Effectiveness of intracanal irrigants and medications against the yeast Candida albicans. J Endod 28(2):68–71.  https://doi.org/10.1097/00004770-200202000-00004CrossRefPubMedGoogle Scholar
  32. 32.
    Fernandes PN, Mannarino SC, Silva CG, Pereira MD, Panek AD, Eleutherio EC (2007) Oxidative stress response in eukaryotes: effect of glutathione, superoxide dismutase and catalase on adaptation to peroxide and menadione stresses in Saccharomyces cerevisiae. Redox Rep: Commun Free Radical Res 12(5):236–244.  https://doi.org/10.1179/135100007x200344CrossRefGoogle Scholar
  33. 33.
    Finland (2015) Assessment report. Hydrogen peroxide. Product-types 1–6Google Scholar
  34. 34.
    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
  35. 35.
    Glynn AA, O’Donnell ST, Molony DC, Sheehan E, McCormack DJ, O’Gara JP (2009) Hydrogen peroxide induced repression of icaADBC transcription and biofilm development in Staphylococcus epidermidis. J Orthop Res: Off Publ Orthop Res Soc 27(5):627–630.  https://doi.org/10.1002/jor.20758CrossRefGoogle Scholar
  36. 36.
    Gosau M, Hahnel S, Schwarz F, Gerlach T, Reichert TE, Burgers R (2010) Effect of six different peri-implantitis disinfection methods on in vivo human oral biofilm. Clin Oral Implant Res 21(8):866–872.  https://doi.org/10.1111/j.1600-0501.2009.01908.xCrossRefGoogle Scholar
  37. 37.
    Goulart CL, Barbosa LC, Bisch PM, von Kruger WM (2016) Catalases and PhoB/PhoR system independently contribute to oxidative stress resistance in Vibrio cholerae O1. Microbiology (Reading, England) 162(11):1955–1962.  https://doi.org/10.1099/mic.0.000364
  38. 38.
    Grant CM, MacIver FH, Dawes IW (1997) Mitochondrial function is required for resistance to oxidative stress in the yeast Saccharomyces cerevisiae. FEBS Lett 410(2–3):219–222CrossRefPubMedGoogle Scholar
  39. 39.
    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 Dev 6(12):382CrossRefGoogle Scholar
  40. 40.
    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
  41. 41.
    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
  42. 42.
    Gutierrez-Martin CB, Yubero S, Martinez S, Frandoloso R, Rodriguez-Ferri EF (2011) Evaluation of efficacy of several disinfectants against Campylobacter jejuni strains by a suspension test. Res Vet Sci 91(3):e44–e47.  https://doi.org/10.1016/j.rvsc.2011.01.020CrossRefPubMedGoogle Scholar
  43. 43.
    He J, Sakaguchi K, Suzuki T (2012) Acquired tolerance to oxidative stress in Bifidobacterium longum 105-A via expression of a catalase gene. Appl Environ Microbiol 78(8):2988–2990.  https://doi.org/10.1128/aem.07093-11CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Holmberg K, Hallander HO (1973) Production of bactericidal concentrations of hydrogen peroxide by Streptococcus sanguis. Arch Oral Biol 18(3):423–434CrossRefPubMedGoogle Scholar
  45. 45.
    Holton J, Nye P, McDonald V (1994) Efficacy of selected disinfectants against mycobacteria and cryptosporidia. J Hosp Infect 27(2):105–115CrossRefPubMedGoogle Scholar
  46. 46.
    Howie R, Alfa MJ, Coombs K (2008) Survival of enveloped and non-enveloped viruses on surfaces compared with other micro-organisms and impact of suboptimal disinfectant exposure. J Hosp Infect 69(4):368–376.  https://doi.org/10.1016/j.jhin.2008.04.024CrossRefPubMedGoogle Scholar
  47. 47.
    Huang Y, Chen H (2011) Effect of organic acids, hydrogen peroxide and mild heat on inactivation of Escherichia coli O157:H7 on baby spinach. Food Control 22(8):1178–1183CrossRefGoogle Scholar
  48. 48.
    Hyslop PA, Hinshaw DB, Scraufstatter IU, Cochrane CG, Kunz S, Vosbeck K (1995) Hydrogen peroxide as a potent bacteriostatic antibiotic: implications for host defense. Free Radic Biol Med 19(1):31–37CrossRefPubMedGoogle Scholar
  49. 49.
    Iniguez-Moreno M, Avila-Novoa MG, Iniguez-Moreno E, Guerrero-Medina PJ, Gutierrez-Lomeli M (2017) Antimicrobial activity of disinfectants commonly used in the food industry in Mexico. J Glob Antimicrob Res 10:143–147.  https://doi.org/10.1016/j.jgar.2017.05.013CrossRefGoogle Scholar
  50. 50.
    Ittatirut S, Matangkasombut O, Thanyasrisung P (2014) In-office bleaching gel with 35% hydrogen peroxide enhanced biofilm formation of early colonizing streptococci on human enamel. J Dent 42(11):1480–1486.  https://doi.org/10.1016/j.jdent.2014.08.003CrossRefPubMedGoogle Scholar
  51. 51.
    Jang IA, Kim J, Park W (2016) Endogenous hydrogen peroxide increases biofilm formation by inducing exopolysaccharide production in Acinetobacter oleivorans DR1. Sci Rep 6:21121.  https://doi.org/10.1038/srep21121CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Juncker JC (2015) COMMISSION IMPLEMENTING REGULATION (EU) 2015/1730 of 28 September 2015 approving hydrogen peroxide as an existing active substance for use in biocidal products for product-types 1, 2, 3, 4, 5 and 6. Off J Eur Union 58(L 252):27–32Google Scholar
  53. 53.
    Kampf G (2017) Black Box Oxidizers. Infect Control Hosp Epidemiol 38(11):1387–1388.  https://doi.org/10.1017/ice.2017.199CrossRefPubMedGoogle Scholar
  54. 54.
    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
  55. 55.
    Khakimova M, Ahlgren HG, Harrison JJ, English AM, Nguyen D (2013) The stringent response controls catalases in Pseudomonas aeruginosa and is required for hydrogen peroxide and antibiotic tolerance. J Bacteriol 195(9):2011–2020.  https://doi.org/10.1128/jb.02061-12CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Koban I, Geisel MH, Holtfreter B, Jablonowski L, Hubner NO, Matthes R, Masur K, Weltmann KD, Kramer A, Kocher T (2013) Synergistic effects of nonthermal plasma and disinfecting agents against dental biofilms in vitro. ISRN Dent 2013:573262.  https://doi.org/10.1155/2013/573262CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Köse H, Yapar N (2017) The comparison of various disinfectants’ efficacy on Staphylococcus aureus and Pseudomonas aeruginosa biofilm layers. Turk J Med Sci 47(4):1287–1294CrossRefPubMedGoogle Scholar
  58. 58.
    Krolasik J, Zakowska Z, Krepska M, Klimek L (2010) Resistance of bacterial biofilms formed on stainless steel surface to disinfecting agent. Pol J Microbiol 59(4):281–287PubMedGoogle Scholar
  59. 59.
    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
  60. 60.
    Leitch CS, Leitch AE, Tidman MJ (2015) Quantitative evaluation of dermatological antiseptics. Clin Exp Dermatol 40(8):912–915.  https://doi.org/10.1111/ced.12745CrossRefPubMedGoogle Scholar
  61. 61.
    Lemmen S, Scheithauer S, Hafner H, Yezli S, Mohr M, Otter JA (2015) Evaluation of hydrogen peroxide vapor for the inactivation of nosocomial pathogens on porous and nonporous surfaces. Am J Infect Control 43(1):82–85.  https://doi.org/10.1016/j.ajic.2014.10.007CrossRefPubMedGoogle Scholar
  62. 62.
    Leung CY, Chan YC, Samaranayake LP, Seneviratne CJ (2012) Biocide resistance of Candida and Escherichia coli biofilms is associated with higher antioxidative capacities. J Hosp Infect 81(2):79–86.  https://doi.org/10.1016/j.jhin.2011.09.014CrossRefPubMedGoogle Scholar
  63. 63.
    Li X, Wu J, Han J, Hu Y, Mi K (2015) Distinct Responses of Mycobacterium smegmatis to Exposure to Low and High Levels of Hydrogen Peroxide. PLoS ONE 10(7):e0134595.  https://doi.org/10.1371/journal.pone.0134595CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Liaqat I, Sabri AN (2008) Effect of biocides on biofilm bacteria from dental unit water lines. Curr Microbiol 56(6):619–624.  https://doi.org/10.1007/s00284-008-9136-6CrossRefPubMedGoogle Scholar
  65. 65.
    Lin F, Xu Y, Chang Y, Liu C, Jia X, Ling B (2017) Molecular characterization of reduced susceptibility to biocides in clinical isolates of Acinetobacter baumannii. Front Microbiol 8:1836.  https://doi.org/10.3389/fmicb.2017.01836
  66. 66.
    Lin SM, Svoboda KK, Giletto A, Seibert J, Puttaiah R (2011) Effects of hydrogen peroxide on dental unit biofilms and treatment water contamination. Eur J Dent 5(1):47–59PubMedPubMedCentralGoogle Scholar
  67. 67.
    Lou Y, Yousef AE (1997) Adaptation to sublethal environmental stresses protects Listeria monocytogenes against lethal preservation factors. Appl Environ Microbiol 63(4):1252–1255PubMedPubMedCentralGoogle Scholar
  68. 68.
    Luppens SB, Rombouts FM, Abee T (2002) The effect of the growth phase of Staphylococcus aureus on resistance to disinfectants in a suspension test. J Food Prot 65(1):124–129CrossRefPubMedGoogle Scholar
  69. 69.
    Marin C, Hernandiz A, Lainez M (2009) Biofilm development capacity of Salmonella strains isolated in poultry risk factors and their resistance against disinfectants. Poult Sci 88(2):424–431.  https://doi.org/10.3382/ps.2008-00241CrossRefPubMedGoogle Scholar
  70. 70.
    Mariscal A, Carnero-Varo M, Gutierrez-Bedmar M, Garcia-Rodriguez A, Fernandez-Crehuet J (2007) A fluorescent method for assessing the antimicrobial efficacy of disinfectant against Escherichia coli ATCC 35218 biofilm. Appl Microbiol Biotechnol 77(1):233–240.  https://doi.org/10.1007/s00253-007-1137-zCrossRefPubMedGoogle Scholar
  71. 71.
    Martienssen M (2000) Simultaneous catalytic detoxification and biodegradation of organic peroxides during the biofilm process. Water Res 34(16):3917–3926CrossRefGoogle Scholar
  72. 72.
    Martin H, Maris P (2012) Synergism between hydrogen peroxide and seventeen acids against six bacterial strains. J Appl Microbiol 113(3):578–590.  https://doi.org/10.1111/j.1365-2672.2012.05364.xCrossRefPubMedGoogle Scholar
  73. 73.
    Miyasaki KT, Wilson ME, Zambon JJ, Genco RJ (1985) Influence of endogenous catalase activity on the sensitivity of the oral bacterium Actinobacillus actinomycetemcomitans and the oral haemophili to the bactericidal properties of hydrogen peroxide. Arch Oral Biol 30(11–12):843–848CrossRefPubMedGoogle Scholar
  74. 74.
    Momba MNB, Cloete TE, Venter SN, Kfir R (1998) Evaluation of the impact of disinfection processes on the formation of biofilms in potable surface water distribution systems. Water Sci Technol 38(8):283–289.  https://doi.org/10.1016/S0273-1223(98)00703-3
  75. 75.
    Nakamura K, Shirato M, Kanno T, Ortengren U, Lingstrom P, Niwano Y (2016) Antimicrobial activity of hydroxyl radicals generated by hydrogen peroxide photolysis against Streptococcus mutans biofilm. Int J Antimicrob Agents 48(4):373–380.  https://doi.org/10.1016/j.ijantimicag.2016.06.007CrossRefPubMedGoogle Scholar
  76. 76.
    Nandy P, Lucas AD, Gonzalez EA, Hitchins VM (2016) Efficacy of commercially available wipes for disinfection of pulse oximeter sensors. Am J Infect Control 44(3):304–310.  https://doi.org/10.1016/j.ajic.2015.09.028CrossRefPubMedGoogle Scholar
  77. 77.
    National Center for Biotechnology Information Hydrogen peroxide. PubChem Compound Database; CID=784. https://pubchem.ncbi.nlm.nih.gov/compound/784. Accessed 7 Oct 2017
  78. 78.
    Nett JE, Guite KM, Ringeisen A, Holoyda KA, Andes DR (2008) Reduced biocide susceptibility in Candida albicans biofilms. Antimicrob Agents Chemother 52(9):3411–3413.  https://doi.org/10.1128/aac.01656-07CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Ntrouka V, Hoogenkamp M, Zaura E, van der Weijden F (2011) The effect of chemotherapeutic agents on titanium-adherent biofilms. Clin Oral Implant Res 22(11):1227–1234.  https://doi.org/10.1111/j.1600-0501.2010.02085.xCrossRefGoogle Scholar
  80. 80.
    Nunoshiba T, Hashimoto M, Nishioka H (1991) Cross-adaptive response in Escherichia coli caused by pretreatment with H2O2 against formaldehyde and other aldehyde compounds. Mutat Res 255(3):265–271CrossRefPubMedGoogle Scholar
  81. 81.
    Omidbakhsh N (2006) A new peroxide-based flexible endoscope-compatible high-level disinfectant. Am J Infect Control 34(9):571–577.  https://doi.org/10.1016/j.ajic.2006.02.003CrossRefPubMedGoogle Scholar
  82. 82.
    Omidbakhsh N, Sattar SA (2006) Broad-spectrum microbicidal activity, toxicologic assessment, and materials compatibility of a new generation of accelerated hydrogen peroxide-based environmental surface disinfectant. Am J Infect Control 34(5):251–257.  https://doi.org/10.1016/j.ajic.2005.06.002CrossRefPubMedGoogle Scholar
  83. 83.
    Oosterik LH, Tuntufye HN, Butaye P, Goddeeris BM (2014) Effect of serogroup, surface material and disinfectant on biofilm formation by avian pathogenic Escherichia coli. Vet J (London, England: 1997) 202(3):561–565.  https://doi.org/10.1016/j.tvjl.2014.10.001
  84. 84.
    Peeters E, Nelis HJ, Coenye T (2008) Evaluation of the efficacy of disinfection procedures against Burkholderia cenocepacia biofilms. J Hosp Infect 70(4):361–368.  https://doi.org/10.1016/j.jhin.2008.08.015CrossRefPubMedGoogle Scholar
  85. 85.
    Penna TC, Mazzola PG, Silva Martins AM (2001) The efficacy of chemical agents in cleaning and disinfection programs. BMC Infect Dis 1:16CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Perumal PK, Wand ME, Sutton JM, Bock LJ (2014) Evaluation of the effectiveness of hydrogen-peroxide-based disinfectants on biofilms formed by Gram-negative pathogens. J Hosp Infect 87(4):227–233.  https://doi.org/10.1016/j.jhin.2014.05.004CrossRefPubMedGoogle Scholar
  87. 87.
    Pezzoni M, Pizarro RA, Costa CS (2014) Protective role of extracellular catalase (KatA) against UVA radiation in Pseudomonas aeruginosa biofilms. J Photochem Photobiol, B 131:53–64.  https://doi.org/10.1016/j.jphotobiol.2014.01.005CrossRefGoogle Scholar
  88. 88.
    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
  89. 89.
    Piskin N, Celebi G, Kulah C, Mengeloglu Z, Yumusak M (2011) Activity of a dry mist-generated hydrogen peroxide disinfection system against methicillin-resistant Staphylococcus aureus and Acinetobacter baumannii. Am J Infect Control 39(9):757–762.  https://doi.org/10.1016/j.ajic.2010.12.003CrossRefPubMedGoogle Scholar
  90. 90.
    Pitten F-A, Werner H-P, Kramer A (2003) A standardized test to assess the impact of different organic challenges on the antimicrobial activity of antiseptics. J Hosp Infect 55(2):108–115CrossRefPubMedGoogle Scholar
  91. 91.
    Pliuta VA, Andreenko IuV, Kuznetsov AE, Khmel IA (2013) Formation of the Pseudomonas aeruginosa PAO1 biofilms in the presence of hydrogen peroxide; the effect of the AiiA gene. Molekuliarnaia genetika, mikrobiologiia i virusologiia 4:10–14Google Scholar
  92. 92.
    Presterl E, Suchomel M, Eder M, Reichmann S, Lassnigg A, Graninger W, Rotter M (2007) Effects of alcohols, povidone-iodine and hydrogen peroxide on biofilms of Staphylococcus epidermidis. J Antimicrob Chemother 60(2):417–420.  https://doi.org/10.1093/jac/dkm221CrossRefPubMedGoogle Scholar
  93. 93.
    Ravindra Kumar S, Imlay JA (2013) How Escherichia coli tolerates profuse hydrogen peroxide formation by a catabolic pathway. J Bacteriol 195(20):4569–4579.  https://doi.org/10.1128/jb.00737-13CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Redondo C, Sena-Véleza M, Gell I, Ferragud E, Sabuquillo P, Graham JH, Cubero J (2015) Influence of selected bactericides on biofilm formation and viability of Xanthomonas citri subsp. citri. Crop Protect 78:204–213CrossRefGoogle Scholar
  95. 95.
    Rizzotti L, Rossi F, Torriani S (2016) Biocide and antibiotic resistance of Enterococcus faecalis and Enterococcus faecium isolated from the swine meat chain. Food Microbiol 60:160–164.  https://doi.org/10.1016/j.fm.2016.07.009CrossRefPubMedGoogle Scholar
  96. 96.
    Rodriguez Ferri EF, Martinez S, Frandoloso R, Yubero S, Gutierrez Martin CB (2010) Comparative efficacy of several disinfectants in suspension and carrier tests against Haemophilus parasuis serovars 1 and 5. Res Vet Sci 88(3):385–389.  https://doi.org/10.1016/j.rvsc.2009.12.001CrossRefPubMedGoogle Scholar
  97. 97.
    Roeder RS, Lenz J, Tarne P, Gebel J, Exner M, Szewzyk U (2010) Long-term effects of disinfectants on the community composition of drinking water biofilms. Int J Hyg Environ Health 213(3):183–189.  https://doi.org/10.1016/j.ijheh.2010.04.007CrossRefPubMedGoogle Scholar
  98. 98.
    Rosenthal RA, Bell WM, Abshire R (1999) Disinfecting action of a new multi-purpose disinfection solution for contact lenses. Cont Lens Anterior Eye 22(4):104–109CrossRefPubMedGoogle Scholar
  99. 99.
    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
  100. 100.
    Rutala WA, Weber DJ (2013) Disinfectants used for environmental disinfection and new room decontamination technology. Am J Infect Control 41(5 Suppl):S36–S41.  https://doi.org/10.1016/j.ajic.2012.11.006CrossRefPubMedGoogle Scholar
  101. 101.
    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
  102. 102.
    Sattar SA, Adegbunrin O, Ramirez J (2002) Combined application of simulated reuse and quantitative carrier tests to assess high-level disinfection: experiments with an accelerated hydrogen peroxide-based formulation. Am J Infect Control 30(8):449–457CrossRefPubMedGoogle Scholar
  103. 103.
    Sattar SA, Bradley C, Kibbee R, Wesgate R, Wilkinson MA, Sharpe T, Maillard JY (2015) Disinfectant wipes are appropriate to control microbial bioburden from surfaces: use of a new ASTM standard test protocol to demonstrate efficacy. J Hosp Infect 91(4):319–325.  https://doi.org/10.1016/j.jhin.2015.08.026CrossRefPubMedGoogle Scholar
  104. 104.
    Seier-Petersen MA, Jasni A, Aarestrup FM, Vigre H, Mullany P, Roberts AP, Agerso Y (2014) Effect of subinhibitory concentrations of four commonly used biocides on the conjugative transfer of Tn916 in Bacillus subtilis. J Antimicrob Chemother 69(2):343–348.  https://doi.org/10.1093/jac/dkt370CrossRefPubMedGoogle Scholar
  105. 105.
    Semchyshyn HM (2014) Hormetic concentrations of hydrogen peroxide but not ethanol induce cross-adaptation to different stresses in budding yeast. Int J Microbiol 2014:485792.  https://doi.org/10.1155/2014/485792CrossRefPubMedPubMedCentralGoogle Scholar
  106. 106.
    Shirato M, Nakamura K, Kanno T, Lingstrom P, Niwano Y, Ortengren U (2017) Time-kill kinetic analysis of antimicrobial chemotherapy based on hydrogen peroxide photolysis against Streptococcus mutans biofilm. J Photochem Photobiol, B 173:434–440.  https://doi.org/10.1016/j.jphotobiol.2017.06.023CrossRefGoogle Scholar
  107. 107.
    Soto E, Halliday-Simmonds I, Francis S, Kearney MT, Hansen JD (2015) Biofilm formation of Francisella noatunensis subsp. orientalis. Vet Microbiol 181(3–4):313–317.  https://doi.org/10.1016/j.vetmic.2015.10.007CrossRefPubMedGoogle Scholar
  108. 108.
    Soumet C, Meheust D, Pissavin C, Le Grandois P, Fremaux B, Feurer C, Le Roux A, Denis M, Maris P (2016) Reduced susceptibilities to biocides and resistance to antibiotics in food-associated bacteria following exposure to quaternary ammonium compounds. J Appl Microbiol 121(5):1275–1281.  https://doi.org/10.1111/jam.13247CrossRefPubMedGoogle Scholar
  109. 109.
    Stanley PM (1999) Efficacy of peroxygen compounds against glutaraldehyde-resistant mycobacteria. Am J Infect Control 27(4):339–343CrossRefPubMedGoogle Scholar
  110. 110.
    Subbaiah TV, Mitchison DA, Selkon JD (1960) The Susceptibility to Hydrogen Peroxide of Indian and British Isoniazid-Sensitive and lsoniazid-Resistant Tubercle Bacilli. Tubercle 41(5):323–333CrossRefGoogle Scholar
  111. 111.
    Sun D, Crowell SA, Harding CM, De Silva PM, Harrison A, Fernando DM, Mason KM, Santana E, Loewen PC, Kumar A, Liu Y (2016) KatG and KatE confer Acinetobacter resistance to hydrogen peroxide but sensitize bacteria to killing by phagocytic respiratory burst. Life Sci 148:31–40.  https://doi.org/10.1016/j.lfs.2016.02.015CrossRefPubMedPubMedCentralGoogle Scholar
  112. 112.
    Suraju MO, Lalinde-Barnes S, Sanamvenkata S, Esmaeili M, Shishodia S, Rosenzweig JA (2015) The effects of indoor and outdoor dust exposure on the growth, sensitivity to oxidative-stress, and biofilm production of three opportunistic bacterial pathogens. Sci Total Environ 538:949–958.  https://doi.org/10.1016/j.scitotenv.2015.08.063CrossRefPubMedGoogle Scholar
  113. 113.
    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
  114. 114.
    Tachikawa M, Yamanaka K (2014) Synergistic disinfection and removal of biofilms by a sequential two-step treatment with ozone followed by hydrogen peroxide. Water Res 64:94–101.  https://doi.org/10.1016/j.watres.2014.06.047CrossRefPubMedGoogle Scholar
  115. 115.
    Theraud M, Bedouin Y, Guiguen C, Gangneux JP (2004) Efficacy of antiseptics and disinfectants on clinical and environmental yeast isolates in planktonic and biofilm conditions. J Med Microbiol 53(Pt 10):1013–1018.  https://doi.org/10.1099/jmm.0.05474-0CrossRefPubMedGoogle Scholar
  116. 116.
    Toki T, Nakamura K, Kurauchi M, Kanno T, Katsuda Y, Ikai H, Hayashi E, Egusa H, Sasaki K, Niwano Y (2015) Synergistic interaction between wavelength of light and concentration of H(2)O(2) in bactericidal activity of photolysis of H(2)O(2). J Biosci Bioeng 119(3):358–362.  https://doi.org/10.1016/j.jbiosc.2014.08.015CrossRefPubMedGoogle Scholar
  117. 117.
    Tondo ML, Delprato ML, Kraiselburd I, Fernandez Zenoff MV, Farias ME, Orellano EG (2016) KatG, the Bifunctional Catalase of Xanthomonas citri subsp. citri, Responds to Hydrogen Peroxide and Contributes to Epiphytic Survival on Citrus Leaves. PLoS ONE 11(3):e0151657.  https://doi.org/10.1371/journal.pone.0151657CrossRefPubMedPubMedCentralGoogle Scholar
  118. 118.
    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
  119. 119.
    Traore O, Springthorpe VS, Sattar SA (2002) Testing chemical germicides against Candida species using quantitative carrier and fingerpad methods. J Hosp Infect 50(1):66–75.  https://doi.org/10.1053/jhin.2001.1133CrossRefPubMedGoogle Scholar
  120. 120.
    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
  121. 121.
    Venturini ME, Blanco D, Oria R (2002) In vitro antifungal activity of several antimicrobial compounds against Penicillium expansum. J Food Prot 65(5):834–839CrossRefPubMedGoogle Scholar
  122. 122.
    Vicente CS, Nascimento FX, Ikuyo Y, Cock PJ, Mota M, Hasegawa K (2016) The genome and genetics of a high oxidative stress tolerant Serratia sp. LCN16 isolated from the plant parasitic nematode Bursaphelenchus xylophilus. BMC Genom 17:301.  https://doi.org/10.1186/s12864-016-2626-1CrossRefGoogle Scholar
  123. 123.
    Wesgate R, Grasha P, Maillard JY (2016) Use of a predictive protocol to measure the antimicrobial resistance risks associated with biocidal product usage. Am J Infect Control 44(4):458–464.  https://doi.org/10.1016/j.ajic.2015.11.009CrossRefPubMedGoogle Scholar
  124. 124.
    Wright MS, Mountain S, Beeri K, Adams MD (2017) Assessment of insertion sequence mobilization as an adaptive response to oxidative stress in Acinetobacter baumannii using IS-seq. J Bacteriol 199(9).  https://doi.org/10.1128/jb.00833-16
  125. 125.
    Xie K, Peng H, Hu H, Wang W, Zhang X (2013) OxyR, an important oxidative stress regulator to phenazines production and hydrogen peroxide resistance in Pseudomonas chlororaphis GP72. Microbiol Res 168(10):646–653.  https://doi.org/10.1016/j.micres.2013.05.001CrossRefPubMedGoogle Scholar
  126. 126.
    Yanai R, Yamada N, Ueda K, Tajiri M, Matsumoto T, Kido K, Nakamura S, Saito F, Nishida T (2006) Evaluation of povidone-iodine as a disinfectant solution for contact lenses: antimicrobial activity and cytotoxicity for corneal epithelial cells. Cont Lens Anterior Eye 29(2):85–91.  https://doi.org/10.1016/j.clae.2006.02.006CrossRefPubMedGoogle Scholar
  127. 127.
    Zamocky M, Furtmuller PG, Obinger C (2008) Evolution of catalases from bacteria to humans. Antioxid Redox Signal 10(9):1527–1548.  https://doi.org/10.1089/ars.2008.2046CrossRefPubMedPubMedCentralGoogle 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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