Keywords
Decontamination
Disinfectant
Sterilization
Efficacy testing
How to Cite
Abstract
Surrogate species are commonly used to evaluate the ability of decontamination, sterilization, and/or disinfectant methods to sanitize bio-contaminated surfaces, equipment, facilities, soil, or water. As new decontamination technologies become commercialized there is an ongoing need to evaluate them using field studies, or on-site for large, stationary systems, to determine if they are more environmentally friendly, less expensive, or more effective than the current sanitation practices. This surrogate review compares potential surrogate species such as MS2 bacteriophage, Clostridium difficile, Bacillus subtilis, and Cytisus scoparius for their ability to accurately estimate the efficacy of decontamination, sterilization methods or commercial systems when evaluated under field conditions. Evaluation of decontamination systems, using field or on-site studies conducted under real-world conditions provides realistic estimates of sanitation and insights into potential risks to health or the environment. Multi-stage decontamination systems, or semi-sterilization methods, such as concentrated, or high-level, disinfectants, pressure washing equipment with steam, or extended ultra-violet (UV-C) radiation, require hard-to-kill surrogates, such as B. subtilis, to determine effective treatments. Use of multiple surrogates for decontamination or sterilization research alleviates several concerns about selecting a single surrogate species that may only perform well only under specific treatments or environmental conditions.
References
Busta FF and Ordal ZJ. Heat-activation Kinetics of Endospores of Bacillus subtilis. J Food Sci 1964; 29(3): 345- 353. https://doi.org/10.1111/j.1365-2621.1964.tb01742.x
Sinclair RG. Criteria for Selection of Surrogates Used to Study the Fate and Control of Pathogens in the Environment. Appl Environ Microbiol 2012; 78(6): 1969-1977. https://doi.org/10.1128/AEM.06582-11
Environmental Protection Agency (EPA). Product Performance Test Guidelines PSCPP 10.2200: Disinfectants for Use on Hard Surfaces Efficacy Data Recommendations 2012. https: //nepis.epa.gov/
Buttner MP, Cruz P, Stetzenback LD, Klima-Comba AK, Stevens VL, Cronin TD. Determination of the efficacy of two building decontamination strategies by surface sampling with culture and quantitative PCR analysis. Appl Environ Micobiol 2004; 70(8): 4740-4747. https://doi.org/10.1128/AEM.70.8.4740-4747.2004
Tomasino SF. Development and assessment of disinfectant efficacy test methods for regulatory purposes. Am J Infec Cont 2013; 41: 72-76. https://doi.org/10.1016/j.ajic.2012.11.007
Hellawell JM. Biological Indicators of Freshwater Pollution and Environmental Management. Springer Science & Business Media 2012; Dec 6.
McDonnell G, Burke P. Disinfection: is it time to reconsider Spaulding? J Hosp Inf 2011; 78(3): 163-70. https://doi.org/10.1016/j.jhin.2011.05.002
University of Colorado Boulder. Disinfectants and Sterilization Methods. Environmental Health and Safety 2008; https: //ehs.colorado.edu/resources/disinfectants-andsterilization-methods/
Powell JF. The sporulation and germination of a strain of Bacillus megatherium. Microbiology 1951; 5(5): 993-1000. https://doi.org/10.1099/00221287-5-5-993
Shin GA. and Sobsey M. Reduction of Norwalk Virus, Poliovirus 1, and Bacteriophage MS2 by Ozone Disinfection of Water. Appl Environ Microbiol 2003; 69(7): 3975-3978. https://doi.org/10.1128/AEM.69.7.3975-3978.2003
Hosseini SRS, Dovon MRE, Yavarmanesh M, Abbaszadegan M. Thermal inactivation of MS2 bacteriophage as a surrogate of enteric viruses in cow milk. J Consum Prot Food Saf 2017; 12(4): 341-347. https://doi.org/10.1007/s00003-017-1119-8
Dawson DJ, Paish A, Staffell LM, Seymour IJ., Appleton H. Survival of Viruses on Fresh Produce, Using MS2 as a Surrogate for Norovirus. J Appl Microbiol 2005; 98(1): 203- 209. https://doi.org/10.1111/j.1365-2672.2004.02439.x
Freed J. Harvesting and Marketing Scotch Broom (Cytisus scoparius). Oregon State University Extension 1998; EC 1467.
USDA. Life History, Habitat, Spread and Impacts of Scotch Broom. Natural Resources Conservation Service Montana 2017; https://www.nrcs.usda.gov/wps/portal/nrcs/detail/mt/ technical/ecoscience/invasive/?cid=nrcs144p2_056821.
Mack RN. Plant nautralizations and invasions in the Eastern United States 1634-1860. Annals Missouri Bot Gard 2003; 90(1): 77-90. https://doi.org/10.2307/3298528
Zouhar K. Cytisus scoparius, C. striatus. Fire Effects Information System. U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station, Fire Sciences Laboratory 2005.
Tarrega R, Calvo L, Trabaud L. Effect of High Temperatures on Seed Germination of Two Woody Leguminosae. Springer 1992; 102(2): 139-147. https://doi.org/10.1007/BF00044730
Herranz JM, Ferrandis P, Martinez-Sanchez JJ. Influence of heat on seed germination of seven Mediterranean Leguminosae species. Plant Ecol 1998; 136: 95-103. https://doi.org/10.1023/A:1009702318641
Bossard C. Seed germination in the exotic shrub Cytisus scoparious (Scotch Broom) in California. Madrono 1993; 40(1): 47-61.
Burhnam CD, Carroll KC. Diagnosis of Clostridium difficle Infection: An Ongoing Conundrum for Clinicians and for Clinical Laboratores. Clin Microbio Rev 2013; 26(3): 604-630. https://doi.org/10.1128/CMR.00016-13
Bakri MM. Investigating the presence of Clostridium difficle in vegetables in Jazan markets, Saudi Arabia Sky. J Microbiol Res 2016; 4(7): 60-64.
Gould H, Limbago B. Clostridium difficle in Food and Domestic Animals: A New Foodborne Pathogen? Clin Infect Dis 2010; 51(5): 577-582. https://doi.org/10.1086/655692
Saif NA, Brazier JS. The distribution of Clostridium difficile in the environment of South Wales. J Med Microbiol 1996; 45: 133-137. https://doi.org/10.1099/00222615-45-2-133
Moono P, Li, SC, Riley TV. High prevalence of toxigenic Clostridium difficle in public space lawns in Western Australia. Scientific Reports 2017. https://doi.org/10.1038/srep41196
Rodriquez-Palacios A, Stampfli HR, Duffield T. Clostridium difficle PCR ribotypes in calves. Emerg. Infect. Dis 2006; 12(11): 1730-1736. https://doi.org/10.3201/eid1211.051581
Songer JG, Trinh HT, Killgore GE, Thompson AD, McDonald LC, Limbago BM. Clostridium difficile in retail meat products. Emerg Infect Dis 2009; 15(5): 819-821. https://doi.org/10.3201/eid1505.081071
Center for Disease Control and Prevention (CDC). Nearly half a million Americans suffer from C. difficle infections in a single year 2015. https://www.cdc.gov/media/dpk/ healthcare-associated-infection/deadly-diarrhea/dpk-deadlydiarrhea.html
Burns DA, Heap JT, Minton NP. Clostridium difficle spore germination: an update. Res Microbiol 2010; 161(9): 730- 734. https://doi.org/10.1016/j.resmic.2010.09.007
Davies MP, Anderson M, Hilton AC. The housefly Musca domestica as a mechanical vector of Clostrdium difficle. J Hosp Infect 2016; 94(3): 263-267. https://doi.org/10.1016/j.jhin.2016.08.023
Lynch MF, Tauxe RV, Hedberg CW. The growing burden of foodborne outbreaks due to contaminated fresh produce: risks and opportunities. Epidemiol Infect 2009; 137(3): 307- 315. https://doi.org/10.1017/S0950268808001969
Perez J, Springthorpe VS, Sattar SA. Activity of Selecting Oxidizing Microbes Against the Spore of Clostridium difficle: Relevance to Environmental Control. Am J Infec Cont 2005; (33)5: 320-325. https://doi.org/10.1016/j.ajic.2005.04.240
Omidbakhsh N. Theoretical and Experimental Aspects of Microbial Activities of Hard Surface Disinfectants: Are their Label Claims Based on Testing Under Field Conditions? Journal of AOAC International 2010; 93(6): 1944-51. https://doi.org/10.1093/jaoac/93.6.1944
Speight S, Moy A, Macken S, Chitnis R, Hoffman PN, Davies A, Bennett A, Walker JT. Evaluation of the sporicidal activity of different chemical disinfectants used in hospitals against Clostridium difficle. J Hosp Infect 2011; (79)1: 18-22. https://doi.org/10.1016/j.jhin.2011.05.016
British Standards Institute. Chemical disinfectantsquantitative suspension test for the evaluation of sporicidal activity of chemical disinfectants used in food industrial, domestic and institutional areas-test method and requirements 2002.
Environmental Protection Agency (EPA). Determining the Efficacy of Liquid and Fumigants in Systematic Decontamination Studies for Bacillus anthracis Using Multiple Test Methods 2010. www.epa.gov/ord
Votava M, Slitrova B. Comparison of susceptibility of spores of Bacillus subtilis and Czech strains of Clostridium difficle to disinfectants. Epidemiol Mikrobiol Imunol 2009; 58(1): 36-42.
Oie S, Obayashi A, Yamasaki H, Furukawa H, Kenri T, Takahashi M, Kawamoto K, Makino SI. Disinfection methods for spores of Bacillus atrophaeus, B. anthracis, Clostridium tetani, C. botulinum and C. difficile. Biological and Pharmaceutical Bulletin 2011; 34(8): 1325-9. https://doi.org/10.1248/bpb.34.1325
Humphreys PN. (2011) Testing Standards for Sporicides. J Hosp Infect 2011; 77: 193-198. https://doi.org/10.1016/j.jhin.2010.08.011
Kirk E. Bacillus subtilis. Missouri S&T Microbiology 2009; http://web.mst.edu/~djwesten/MoW/BIO221_2009/B_subtilis. html
Greenberg DL, Busch JD, Keim P, Wagner DM. Identifying experimental surrogates for Bacillus anthracis spores: a review. Investigative Genetics 2010; 1(1): 4. https://doi.org/10.1186/2041-2223-1-4
Montville TJ, Dengrove R, De Siano T, Bonnet M, Schaffner DW. Thermal resistance of spores from virulent strains of Bacillus anthracis and potential surrogates. Journal of food protection 2005; 68(11): 2362-6. https://doi.org/10.4315/0362-028X-68.11.2362
Andersen BM, Rasch M, Hochlin K, Jensen FH, Wismar P, Fredriksen JE. Decontamination of rooms, medical equipment and ambulances using an aerosol of hydrogen peroxide disinfectant. J Hosp Infect 2006; 62(2): 149. https://doi.org/10.1016/j.jhin.2005.07.020
Sella SR, Vandenberghe LP, Soccol CR. Bacillus atrophaeus: main characteristics and biotechnological applications–a review. Critical reviews in biotechnology 2015; 35(4): 533-45. https://doi.org/10.3109/07388551.2014.922915
Lundahl G. A method of increasing test range and accuracy of bioindicators: Geobacillus stearothermophilus spores. PDA J Pharm Sci Tech 2003; 57(4): 249-62.
Durand L, Planchon S, Guinebretiere MH, Carlin F, Remize F. Genotypic and phenotypic characterization of foodborne Geobacillus stearothermophilus. Food Microb 2015; (1)45: 103-10. https://doi.org/10.1016/j.fm.2014.01.015
Montville TJ, Dengrove R, De Siano T, Bonnet M, Schaffner DW. Thermal Resistance of Spores from Virulent Strains of Bacillus anthracis and Potential Surrogates 2005; 68(11): 2362-6. https://doi.org/10.4315/0362-028X-68.11.2362
Palenik CJ, Adams ML, Miller CH. Effectiveness of steam autoclaving on the contents of sharps containers. Amer Dentistry 1990; 3(6): 239-44.
Lemieux P, Sieber R, Osborne A, Woodard A. Destruction of spores on building decontamination residue in a commercial autoclave. Appl Environ Microb 2006; 72(12): 7687-93. https://doi.org/10.1128/AEM.02563-05
Head DS, Cenkowski S, Holley R, Blank G. Effects of superheated steam on Geobacillus stearothermophilus spore viability. J Appl Microb 2008; 104(4): 1213-20. https://doi.org/10.1111/j.1365-2672.2007.03647.x
Unger-Bimczok B, Kottke V, Hertel C, Rauschnabel J. The influence of humidity, hydrogen peroxide concentration, and condensation on the inactivation of Geobacillus stearothermophilus spores with hydrogen peroxide vapor. J Pharm Innov 2008; 3(2): 123-33. https://doi.org/10.1007/s12247-008-9027-1
Rogers JV, Choi YW, Richter WR, Rudnicki DC, Joseph DW, Sabourin CL, Taylor ML, Chang JC. Formaldehyde gas inactivation of Bacillus anthracis, Bacillus subtilis, and Geobacillus stearothermophilus spores on indoor surface materials. J Appl Microb 2007; 103(4): 1104-12. https://doi.org/10.1111/j.1365-2672.2007.03332.x
Rogers JV, Sabourin CL, Choi YW, Richter WR, Rudnicki DC, Riggs KB, Taylor ML, Chang J. Decontamination assessment of Bacillus anthracis, Bacillus subtilis, and Geobacillus stearothermophilus spores on indoor surfaces using a hydrogen peroxide gas generator. J Appl Microb 2005; 99(4): 739-48. https://doi.org/10.1111/j.1365-2672.2005.02686.x
Liato V, Labrie S, Viel C, Benali M, Aïder M. Study of the combined effect of electro-activated solutions and heat treatment on the destruction of spores of Clostridium sporogenes and Geobacillus stearothermophilus in model solution and vegetable puree. Anaerobe 2015; 1(35): 11-21. https://doi.org/10.1016/j.anaerobe.2015.06.004
Pinho SC, Nunes OC, Lobo-da-Cunha A, Almeida MF. Inactivation of Geobacillus stearothermophilus spores by alkaline hydrolysis applied to medical waste treatment. Journal of environmental management 2015; 15(161): 51-6. https://doi.org/10.1016/j.jenvman.2015.06.045
Canno R, Borucki MK. Revival and identification of bacterial spores in 25-to 40-million year old Dominican amber. Science 1995; 2(268): 1265. https://doi.org/10.1126/science.7538699
Tan IS, Ramamurthi KS. Spore formation in Bacillus subtilis. Environ Microbiol Rep 2014; 6(3): 212-225. https://doi.org/10.1111/1758-2229.12130
Nicholson WL, Munakata N, Horneck G, Melosh HJ, Setlow P. Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol. Mol Biol Rev 2000; 64548-572. https://doi.org/10.1128/MMBR.64.3.548-572.2000
Setlow P. Spores of Bacillus subtilis: Their Resistance to and Killing by Radiation, Heat, and Chemicals". Journal of Applied Microbiology 2006; 101(3): 514-525. https://doi.org/10.1111/j.1365-2672.2005.02736.x
McKenny PT, Driks A, Eichenberger P. The Bacillus subtilis endospore: assembly and functions of the multi-layered coat. Nat Rev 2013; (11): 33-44. https://doi.org/10.1038/nrmicro2921
Setlow P. Spore germination. Curr. Opin. Microbiol 2003; 6550-556.
Cornell University. Bacterial Endospores. College of Agri Life Sci; Dep Microb 2007. https://micro.cornell.edu/research/ epulopiscium/bacterial-endospores
Coleman WH, Chen D, Li R, Crown AE, Setlow P. How Moist Heat Kills Spores of Bacillus subtilis. J Bacteriology 2007; 189(23): 8458-8466. https://doi.org/10.1128/JB.01242-07
Cheung HY. Endospores as Biological Indicator for the Validation of Sterilization Process. Research Gate 2012; 19(4): 156-162.
Spicher G, Peters J. Suitability of Bacillus subtilis and Bacillus stearothermophilus spores as test organism bioindicators for detecting superheating of steam. Zebtrakbk Hyg Umwektned 1997; 199 (5): 462-474.
Gillis JR. Spore News: Biological Indicator for Monitoring Low Temperature Steam Sterilization. Mesa Labs 2004; 1(2).
Zhou W, Orr MW, Jian G, Watt SK, Lee VT, Zachariah MR. Inactivation of bacterial spores subjected to sub-second thermal stress. Chem Eng J 2015; 279: 578-588. https://doi.org/10.1016/j.cej.2015.05.021
Chang JC, Ossoff SF, Lobe DC, Dorfman MH, Dumais CM, Qualls RG, Johnson JD. UV inactivation of pathogenic and indicator microorganism. Appl Environ Microbiol 1985; 49(6): 1361-1365. https://doi.org/10.1128/AEM.49.6.1361-1365.1985
Teksoy A. Alkan U, Eleren SC, Topac BS, Saqban FO, Baskaya HS. Comparison of indicator bacteria inactivation by the ultraviolet and the ultraviolet/hydrogen peroxide disinfection process in humic waters. J Water Health 2011; 9(4): 659-669. https://doi.org/10.2166/wh.2011.205
Akude MA, Okada E, Gonzalez JF, Haure PM, Murialdo SE. Bacillus subtilis as a bioindicators for estimating pentachlorophenol toxicity and concentration. J Ind Microbiol Biotechnol 2009; 36(5): 765-768. https://doi.org/10.1007/s10295-009-0550-y
Stoeckel M, Abduh SBM, Aamer A, Hinrichs J. Inactivation of Bacillus spores in batch vs continuous heating systems at sterilization temperatures. Int J Dairy Tech 2014; 67: 1-8. https://doi.org/10.1111/1471-0307.12134
Ghosh S, Setlow P. Isolation and Characterization of Superdormant Spores of Bacillus Species. J Bacteriol 2009; 191: 1787-1797. https://doi.org/10.1128/JB.01668-08
Warth AD. Relationship between the Heat Resistance of Spores and the Optimum and Maximum Growth Temperatures of Bacillus Species. Am Soc Microbiol 1978; (134)3: 699-705. https://doi.org/10.1128/JB.134.3.699-705.1978
Popham DL, Sengupta S, Setlow P. Heat, Hydrogen Peroxide, and UV Resistance of Bacillus subtilis Spores with Increased Core Water Content and with or without Major DNA Binding Proteins. Appl Environ Microbiol 1995; 61(10): 3633-3638. https://doi.org/10.1128/AEM.61.10.3633-3638.1995
Ghosh S, Zhang P, Li YQ, Setlow P. Superdormant spores of Bacillus species have elevated wet-heat resistance and temperature requirements for heat activation. J Bacteriol 2009; 191: 5584-5591. https://doi.org/10.1128/JB.00736-09
Perez-Valdespino A, Ghosh S, Cammett E, Kong L, Li Y, Setlow P. Isolation and Characterization of Bacillus subtillis spores that are Superdormant for Germination With Dodecylamine or Ca2+-dipicolinic acid. J. App. Microbio 2013; 114: 1109-1119. https://doi.org/10.1111/jam.12125
Markland S. Super Dormant Bacteria: What Are They? LabRoots 2015; https://www.labroots.com/trending/ microbiology/1875/super-dormant-bacteria-what-are-they
Adrion AC, Scheffrahn RH, Serre S, Lee SD. Impact of sporicidal fumigation with methyl bromide or methyl iodide on electronic equipment. Journal of environmental management 2019; 1(231): 1021-7. https://doi.org/10.1016/j.jenvman.2018.10.118
Serre S, Mickelsen L, Calfee MW, Wood JP, Gray Jr MS, Scheffrahn RH, Perez R, Kern Jr WH, Daniell N. Whole‐building decontamination of Bacillus anthracis Sterne spores by methyl bromide fumigation. J Appl Microb 2016; 120(1): 80-9. https://doi.org/10.1111/jam.12974
Bettin K, Clabots C, Mathie P, Willard K, Gerding DN. Effectiveness of liquid soap vs. chlorhexidine gluconate for the removal of Clostridium difficile from bare hands and gloved hands. Inf Cont Hosp Epid 1994; 15(11): 697-702. https://doi.org/10.2307/30148335
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