New Biocide Foam Containing Hydrogen Peroxide for the Decontamination of Vertical Surface Contaminated With Bacillus thuringiensis Spores

Frontiers in Microbiology

Volumn 9, Issue , 2018, Pages

  Le Toquin, Esther ^a,b   Faure, Sylvain ^c   Orange, Nicole ^b   Gas, Fabienne ^a  

^a Institut National de la Recherche Agronomique   (France)

^b UNIVERSITÉ DE ROUEN   (France)

^c UNIV MONTPELLIER   (France)

Author keywords

Bacillus thuringiensis; biocide; decontamination; foam; hydrogen peroxide; spores

Indexed keywords

EID: 85085680265     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2018.02295     Document Type: Article

References (53)

1. Andersen B. M. Rasch M. Hochlin K. Jensen F. H. Wismar P. Fredriksen J. E. (2006). Decontamination of rooms, medical equipment and ambulances using an aerosol of hydrogen peroxide disinfectant. J. Hosp. Infect. 62 149–155. 10.1016/j.jhin.2005.07.020 16337307
2. Benga L. Benten W. P. M. Engelhardt E. Gougoula C. Schulze-Robbecke R. Sager M. (2017). Survival of bacteria of laboratory animal origin on cage bedding and inactivation by hydrogen peroxide vapour. Lab. Anim. 51 412–421. 10.1177/0023677216675386 27932683
3. Dame U. Fritz C. Pitois O. Faure S. (2005). Relations between physicochemical properties and instability of decontamination foams. Colloids Surf. A Physicochem. Eng. Asp. 263 210–218. 10.1016/j.colsurfa.2004.12.053
4. Doona C. J. Feeherry F. E. Kustin K. Olinger G. G. Setlow P. Malkin A. J. et al. (2015). Fighting Ebola with novel spore decontamination technologies for the military. Front. Microbiol. 6:663. 10.3389/fmicb.2015.00663 26322021
5. Driks A. (1999). Bacillus subtilis spore coat. Microbiol. Mol. Biol. Rev. 63 1–20.
6. Driks A. (2002a). Maximum shields: the assembly and function of the bacterial spore coat. Trends Microbiol. 10 251–254. 10.1016/S0966-842x(02)02373-9 12088650
7. Driks A. (2002b). Overview: development in bacteria: spore formation in Bacillus subtilis. Cell. Mol. Life Sci. 59 389–391. 10.1007/s00018-002-8430-x 11964116
8. Edmonds J. M. Sabol J. P. Rastogi V. K. (2014). Decontamination efficacy of three commercial-off-the-shelf (COTS) sporicidal disinfectants on medium-sized panels contaminated with surrogate spores of Bacillus anthracis. PLoS One 9:e99827. 10.1371/journal.pone.0099827 24940605
9. Environmental Protection Agency (2006). Evaluation of Spray-Applied Sporicidal Decontamination Technologies. Washington, DC: Environmental Protection Agency.
10. Environmental Protection Agency (2010). Biological Agent Decontamination Technology Testing. Washington, DC: Environmental Protection Agency.
11. Eryilmaz M. Kaskatepe B. Kiymaci M. E. Erol H. B. Simsek D. Gumustas A. (2016). In vitro antimicrobial activity of three new generation disinfectants. Trop. J. Pharm. Res. 15 2191–2195. 10.4314/tjpr.v15i10.18
12. Faille C. Benezech T. Midelet-Bourdin G. Lequette Y. Clarisse M. Ronse G. et al. (2014). Sporulation of Bacillus spp. within biofilms: a potential source of contamination in food processing environments. Food Microbiol. 40 64–74. 10.1016/j.fm.2013.12.004 24549199
13. Faure S. Le Toquin E. Gas F. (2016). Disinfecting aqueous foam, process for preparing same and use thereof. Patent No WO2016202879. Saint Paul, MN: Ecolab Inc.
14. Fernandes M. D. Alvares A. C. C. Manoel J. G. M. Esper L. M. R. Kabuki D. Y. Kuaye A. Y. (2017). Formation of multi-species biofilms by Enterococcus faecium, Enterococcus faecalis, and Bacillus cereus isolated from ricotta processing and effectiveness of chemical sanitation procedures. Int. Dairy J. 72 23–28. 10.1016/j.idairyj.2017.03.016
15. Genest P. C. Setlow B. Melly E. Setlow P. (2002). Killing of spores of Bacillus subtilis by peroxynitrite appears to be caused by membrane damage. Microbiology 148 307–314. 10.1099/00221287-148-1-307 11782523
16. Gonzalez E. A. Nandy P. Lucas A. D. Hitchins V. M. (2015). Ability of cleaning-disinfecting wipes to remove bacteria from medical device surfaces. Am. J. Infect. Control 43 1331–1335. 10.1016/j.ajic.2015.07.024 26654235
17. Guan J. Chan M. Brooks B. W. Rohonczy L. (2013). Influence of temperature and organic load on chemical disinfection of Geobacillus stearothermophilus spores, a surrogate for Bacillus anthracis. Can. Vet. J. 77 100–104.
18. Higgins D. Dworkin J. (2012). Recent progress in Bacillus subtilis sporulation. FEMS Microbiol. Rev. 36 131–148. 10.1111/j.1574-6976.2011.00310.x 22091839
19. Hilgren J. Swanson K. M. J. Diez-Gonzalez F. Cords B. (2007). Inactivation of Bacillus anthracis spores by liquid biocides in the presence of food residue. Appl. Microbiol. 73 6370–6377. 10.1128/Aem.00974-07 17720823
20. Kenters N. Huijskens E. G. W. de Wit S. C. J. van Rosmalen J. Voss A. (2017). Effectiveness of cleaning-disinfection wipes and sprays against multidrug-resistant outbreak strains. Am. J. Infect. Control 45 E69–E73. 10.1016/j.ajic.2017.04.290 28571980
21. Leggett M. J. McDonnell G. Denyer S. P. Setlow P. Maillard J. Y. (2012). Bacterial spore structures and their protective role in biocide resistance. J. Appl. Microbiol. 113 485–498. 10.1111/j.1365-2672.2012.05336.x 22574673
22. Loshon C. A. Melly E. Setlow B. Setlow P. (2001). Analysis of the killing of spores of Bacillus subtilis by a new disinfectant, Sterilox. J. Appl. Microbiol. 91 1051–1058. 10.1046/j.1365-2672.2001.01473.x 11851813
23. McDonnell G. Russell A. D. (1999). Antiseptics and disinfectants: activity, action, and resistance. Clin. Microbiol. Rev. 12 147–179.
24. Melly E. Cowan A. E. Setlow P. (2002). Studies on the mechanism of killing of Bacillus subtilis spores by hydrogen peroxide. J. Appl. Microbiol. 93 316–325. 10.1046/j.1365-2672.2002.01687.x 12147081
25. Moeller R. Setlow P. Reitz G. Nicholson W. L. (2009). Roles of small, acid-soluble spore proteins and core water content in survival of Bacillus subtilis spores exposed to environmental solar UV radiation. Appl. Environ. Microbiol. 75 5202–5208. 10.1128/AEM.00789-09 19542328
26. Mott T. M. Shoe J. L. Hunter M. Woodson A. M. Fritts K. A. Klimko C. P. et al. (2017). Comparison of sampling methods to recover germinated Bacillus anthracis and Bacillus thuringiensis endospores from surface coupons. Appl. Microbiol. 122 1219–1232. 10.1111/jam.13418 28191745
27. Murdoch L. E. Bailey L. Banham E. Watson F. Adams N. M. T. Chewins J. (2016). Evaluating different concentrations of hydrogen peroxide in an automated room disinfection system. Lett. Appl. Microbiol. 63 178–182. 10.1111/lam.12607 27324207
28. Nicholson W. L. Munakata N. Horneck G. Melosh H. J. Setlow P. (2000). Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol. Mol. Biol. Rev. 64 548–572. 10.1128/Mmbr.64.3.548-572.2000 10974126
29. Otter J. A. French G. L. (2009). Survival of nosocomial bacteria and spores on surfaces and inactivation by hydrogen peroxide vapor. J. Clin. Microbiol. 47 205–207. 10.1128/Jcm.02004-08 18971364
30. Piggot P. J. Hilbert D. W. (2004). Sporulation of Bacillus subtilis. Cur. Opin. Microbiol. 7 579–586. 10.1016/j.mib.2004.10.001 15556029
31. Pottage T. Macken S. Walker J. T. Bennett A. M. (2012). Meticillin-resistant Staphylococcus aureus is more resistant to vaporized hydrogen peroxide than commercial Geobacillus stearothermophilus biological indicators. J. Hosp. Infect. 80 41–45. 10.1016/j.jhin.2011.11.001 22137066
32. Raber E. Burklund A. (2010). Decontamination options for Bacillus anthracis-contaminated drinking water determined from spore surrogate studies. Appl. Environ. Microbiol. 76 6631–6638. 10.1128/Aem.01136-10 20709855
33. Rastogi V. K. Wallace L. Smith L. S. Ryan S. P. Martin B. (2009). Quantitative method to determine sporicidal decontamination of building surfaces by gaseous fumigants, and issues related to laboratory-scale studies. Appl. Environ. Microbiol. 75 3688–3694. 10.1128/AEM.02592-08 19346341
34. Riesenman P. J. Nicholson W. L. (2000). Role of the spore coat layers in Bacillus subtilis spore resistance to hydrogen peroxide, artificial UV-C, UV-B, and solar UV radiation. Appl. Environ. Microbiol. 66 620–626. 10.1128/Aem.66.2.620-626.2000 10653726
35. Rios-Castillo A. G. Gonzalez-Rivas F. Rodriguez-Jerez J. J. (2017). Bactericidal efficacy of hydrogen peroxide-based disinfectants against gram-positive and gram-negative bacteria on stainless steel surfaces. J. Food Sci. 82 2351–2356. 10.1111/1750-3841.13790 28833105
36. Rogers J. V. Sabourin C. L. Choi Y. W. Richter W. R. Rudnicki D. C. Riggs K. B. et al. (2005). Decontamination assessment of Bacillus anthracis, Bacillus subtilis, and Geobacillus stearothermophilus spores on indoor surfaces using a hydrogen peroxide gas generator. J. Appl. Microbiol. 99 739–748. 10.1111/j.1365-2672.2005.02686.x 16162224
37. Russell A. D. (1990). Bacterial spores and chemical sporicidal agents. Clin. Microbiol. Rev. 3 99–119. 10.1128/CMR.3.2.99
38. Ryan S. P. Lee S. D. Calfee M. W. Wood J. P. McDonald S. Clayton M. et al. (2014). Effect of inoculation method on the determination of decontamination efficacy against Bacillus spores. World J. Microbiol. Biotechnol. 30 2609–2623. 10.1007/s11274-014-1684-2 24928258
39. Sagripanti J. L. Bonifacino A. (1999). Bacterial spores survive treatment with commercial sterilants and disinfectants. Appl. Environ. Microbiol. 65 4255–4260. 10473448
40. Schmitt K. Zacchia N. A. (2012). Total decontamination cost of the anthrax letter attacks. Biosecur. Bioterror. 10 98–107. 10.1089/bsp.2010.0053 22313022
41. Setlow B. Atluri S. Kitchel R. Koziol-Dube K. Setlow P. (2006). Role of dipicolinic acid in resistance and stability of spores of Bacillus subtilis with or without DNA-protective alpha/beta-type small acid-soluble proteins. J. Bacteriol. 188 3740–3747. 10.1128/JB.00212-06 16707666
42. Setlow P. (1992). I will survive - protecting and repairing spore DNA. J. Bacteriol. 174 2737–2741. 10.1128/jb.174.9.2737-2741.1992 1569005
43. Setlow P. (2006). Spores of Bacillus subtilis: their resistance to and killing by radiation, heat and chemicals. J. Appl. Microbiol. 101 514–525. 10.1111/j.1365-2672.2005.02736.x 16907802
44. Szabo J. G. Meiners G. Heckman L. Rice E. W. Hall J. (2017). Decontamination of Bacillus spores adhered to iron and cement-mortar drinking water infrastructure in a model system using disinfectants. J. Environ. Manag. 187 1–7. 10.1016/j.jenvman.2016.11.024 27865123
45. Tennen R. Setlow B. Davis K. L. Loshon C. A. Setlow P. (2000). Mechanisms of killing of spores of Bacillus subtilis by iodine, glutaraldehyde and nitrous acid. J. Appl. Microbiol. 89 330–338. 10.1046/j.1365-2672.2000.01114.x 10971767
46. Tomasino S. F. Rastogi V. K. Wallace L. Smith L. S. Hamilton M. A. Pines R. M. (2010). Use of alternative carrier materials in AOAC official method(SM) 2008.05. J. AOAC Int. 93 259–276.
47. van Bokhorst-van de Veen H. Xie H. Esveld E. Abee T. Mastwijk H. Nierop Groot M. (2015). Inactivation of chemical and heat-resistant spores of Bacillus and Geobacillus by nitrogen cold atmospheric plasma evokes distinct changes in morphology and integrity of spores. Food Microbiol. 45 26–33. 10.1016/j.fm.2014.03.018 25481059
48. Watanabe T. Furukawa S. Hirata J. Koyama T. Ogihara H. Yamasaki M. (2003). Inactivation of Geobacillus stearothermophilus spores by high-pressure carbon dioxide treatment. Appl. Environ. Microbiol. 69 7124–7129. 10.1128/aem.69.12.7124-7129.2003
49. Wood J. P. Calfee M. W. Clayton M. Griffin-Gatchalian N. Touati A. Ryan S. et al. (2016). A simple decontamination approach using hydrogen peroxide vapour for Bacillus anthracis spore inactivation. J. Appl. Microbiol. 121 1603–1615. 10.1111/jam.13284 27569380
50. Wood J. P. Choi Y. W. Rogers J. V. Kelly T. J. Riggs K. B. Willenberg Z. J. (2011). Efficacy of liquid spray decontaminants for inactivation of Bacillus anthracis spores on building and outdoor materials. J. Appl. Microbiol. 110 1262–1273. 10.1111/j.1365-2672.2011.04980.x 21332900
51. Wood J. P. Meyer K. M. Kelly T. J. Choi Y. W. Rogers J. V. Riggs K. B. et al. (2015). Environmental persistence of Bacillus anthracis and Bacillus subtilis spores. PLoS One 10:e0138083. 10.1371/journal.pone.0138083 26372011
52. Yi Y. Hao L. M. Ma S. R. Wu J. H. Wang T. Lin S. et al. (2016). A pilot study on using chlorine dioxide gas for disinfection of gastrointestinal endoscopes. J. Zhejiang Univ. Sci. B 17 526–536. 10.1631/jzus.B1500327 27381729
53. Young S. B. Setlow P. (2004). Mechanisms of killing of Bacillus subtilis spores by Decon and OxoneTM, two general decontaminants for biological agents. J. Appl. Microbiol. 96 289–301. 10.1046/j.1365-2672.2004.02159.x 14723690