Efficacy of a Next Generation Quaternary Ammonium Chloride Sanitizer on Staphylococcus and Pseudomonas Biofilms and Practical Application in a Food Processing Environment
Abstract
:1. Introduction
2. Materials and Methods
2.1. Bacterial Strains, Growth and Storage Conditions
2.2. Growth of Enhanced Biofilms in Microplates
2.3. Microplate Biofilm Sanitizer Assay
2.4. Enumerating Biofilm Levels from Workers’ Boots
2.5. Identifying Biofilm Bacteria from Workers’ Boots: 16S rRNA PCR and Sequencing
2.6. Comparison of New-Generation QAC (Decon7) with Early-Generation QAC (Bi-Quat) Sanitizer
2.7. Statistical Analysis
3. Results and Discussion
3.1. Generating Microplate Biofilms of Strains of Staphylococcus and Pseudomonas
3.2. Efficacy of Decon7 on Staphylococcus sp. and Pseudomonas sp. Biofilms
3.3. Efficacy of Decon7 on Natural Biofilms on Workers’ Boots from a Food Processing Abatoir
3.4. Recovery and Identification of Bacteria from Biofilms from Workers’ Boots in a Food Processing Abattoir
3.5. Sensitivity of Bacteria from Biofilm from Workers’ Boots to Dual-Quat (Bi-Quat) vs. Quad-Quat (Decon7) Sanitizers
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Achinas, S.; Charalampogiannis, N.; Euverink, G.J. A brief recap of microbial adhesion and biofilms. Appl. Sci. 2019, 9, 2801. [Google Scholar] [CrossRef] [Green Version]
- Donlan, R.M. Biofilms: Microbial life on surfaces. Emerg. Infect. Dis. 2002, 8, 881–890. [Google Scholar] [CrossRef]
- Limoli, D.H.; Jones, C.J.; Wozniak, D.J. Bacterial extracellular polysaccharides in biofilm formation and function. Microb. Biofilms 2015, 223–247. [Google Scholar] [CrossRef] [Green Version]
- Flemming, H.C.; Wingender, J. The biofilm matrix. Nat. Rev. Microbiol. 2010, 8, 623–633. [Google Scholar] [CrossRef] [PubMed]
- Stewart, P.S. Diffusion in biofilms. J. Bacteriol. 2003, 185, 1485–1491. [Google Scholar] [CrossRef] [Green Version]
- Stewart, P.S.; Franklin, M.J. Physiological heterogeneity in biofilms. Nat. Rev. Microbiol. 2008, 6, 199–210. [Google Scholar] [CrossRef]
- Sauer, K.; Camper, A.K.; Ehrlich, G.D.; Costerton, J.W.; Davies, D.G. Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J. Bacteriol. 2002, 184, 1140. [Google Scholar] [CrossRef] [Green Version]
- Solano, C.; Echeverz, M.; Lasa, I. Biofilm dispersion and quorum sensing. Curr. Opin. Microbiol. 2014, 18, 96–104. [Google Scholar] [CrossRef] [Green Version]
- Annous, B.A.; Fratamico, P.M.; Smith, J.L. Quorum sensing in biofilms: Why bacteria behave the way they do. J. Food Sci. 2009, 74, R24–R37. [Google Scholar] [CrossRef]
- Kleerebezem, M.; Quadri, L.E.N.; Kuipers, O.P.; De Vos, W.M. Quorum sensing by peptide pheromones and two-component signal-transduction systems in Gram-positive bacteria. Mol. Microbiol. 1997, 24, 895–904. [Google Scholar] [CrossRef] [Green Version]
- Antunes, L.C.M.; Ferreira, R.B.R.; Buckner, M.M.C.; Finlay, B.B. Quorum sensing in bacterial virulence. Microbiology 2010, 156, 2271–2282. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bai, A.J.; Rai, V.R. Bacterial quorum sensing and food industry. Compr. Rev. Food Sci. Food Saf. 2011, 10, 183–193. [Google Scholar] [CrossRef]
- Lynch, M.J.; Swift, S.; Kirke, D.F.; Keevil, C.W.; Dodd, C.E.R.; Williams, P. The regulation of biofilm development by quorum sensing in Aeromonas hydrophila. Environ. Microbiol. 2002, 4, 18–28. [Google Scholar] [CrossRef]
- Zhao, X.; Yu, Z.; Ding, T. Quorum-sensing regulation of antimicrobial resistance in bacteria. Microorganisms 2020, 8, 425. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Holah, J.T. Chapter 9—Cleaning and disinfection practices in food processing. In Hygiene in Food Processing, 2nd ed.; Lelieveld, H.L.M., Holah, J.T., Napper, D., Eds.; Woodhead Publishing: Cambridge, UK, 2014; pp. 259–304. [Google Scholar]
- Wilson, D.I. Challenges in cleaning: Recent developments and future prospects. Heat Transf. Eng. 2005, 26, 51–59. [Google Scholar] [CrossRef]
- Grinstead, D. Chapter 12—Cleaning and sanitation in food processing environments for the prevention of biofilm formation, and biofilm removal. In Biofilms in the Food and Beverage Industries; Fratamico, P.M., Annous, B.A., Gunther, N.W., Eds.; Woodhead Publishing: Cambridge, UK, 2009; pp. 331–358. [Google Scholar]
- Wirtanen, G.; Salo, S. Disinfection in food processing—Efficacy testing of disinfectants. Rev. Environ. Sci. Bio/Technol. 2003, 2, 293–306. [Google Scholar] [CrossRef]
- Gamble, R.; Muriana, P.M. Microplate fluorescence assay for measurement of the ability of strains of Listeria monocytogenes from meat and meat-processing plants to adhere to abiotic surfaces. Appl. Environ. Microbiol. 2007, 73, 5235–5244. [Google Scholar] [CrossRef] [Green Version]
- Aryal, M.; Muriana, P.M. Microplate lethality assay to determine the efficacy of commercial sanitizers for inactivation of Listeria monocytogenes, Escherichia coli O157:H7, and Salmonella spp. in extended biofilms. Int. Assoc. Food Prot. Annu. Meet. 2018. Abstract #P1-63. Available online: https://iafp.confex.com/iafp/2018/meetingapp.cgi/Paper/18715 (accessed on 25 May 2021).
- Aryal, M.; Pranatharthiharan, P.; Muriana, P.M. Optimization of a microplate assay for generating Listeria monocytogenes, E. coli O157:H7, and Salmonella biofilms and enzymatic recovery for enumeration. Foods 2019, 8, 541. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, F.; Xian, Z.; Kwon, H.J.; Yoo, J.; Burall, L.; Chirtel, S.J.; Hammack, T.S.; Chen, Y. Comparison of three neutralizing broths for environmental sampling of low levels of Listeria monocytogenes desiccated on stainless steel surfaces and exposed to quaternary ammonium compounds. BMC Microbiol. 2020, 20, 333. [Google Scholar] [CrossRef] [PubMed]
- Dey, B.P.; Engley, F.B. Methodology for recovery of chemically treated Staphylococcus aureus with neutralizing medium. Appl. Environ. Microbiol. 1983, 45, 1533. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Henning, C.; Vijayakumar, P.; Adhikari, R.; Jagannathan, B.; Gautam, D.; Muriana, P.M. Isolation and taxonomic identity of bacteriocin-producing lactic acid bacteria from retail foods and animal sources. Microorganisms 2015, 3, 80–93. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bhusal, A.; Muriana, P.M. Isolation and characterization of nitrate reducing bacteria for conversion of vegetable-derived nitrate to ‘natural nitrite’. Appl. Microbiol. 2021, 1, 11–23. [Google Scholar] [CrossRef]
- Turner, S.; Pryer, K.M.; Miao, V.P.W.; Palmer, J.D. Investigating Deep Phylogenetic Relationships among Cyanobacteria and Plastids by Small Subunit rRNA Sequence Analysis1. J. Eukaryot. Microbiol. 1999, 46, 327–338. [Google Scholar] [CrossRef]
- Pitulle, C.; Citron, D.M.; Bochner, B.; Barbers, R.; Appleman, M.D. Novel bacterium isolated from a lung transplant patient with cystic fibrosis. J. Clin. Microbiol. 1999, 37, 3851–3855. [Google Scholar] [CrossRef] [Green Version]
- Coton, E.; Coton, M. Multiplex PCR for colony direct detection of Gram-positive histamine- and tyramine-producing bacteria. J. Microbiol. Methods 2005, 63, 296–304. [Google Scholar] [CrossRef] [PubMed]
- Kumar, S.; Stecher, G.; Li, M.; Knyaz, C.; Tamura, K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 2018, 35, 1547–1549. [Google Scholar] [CrossRef] [PubMed]
- Garver, K.I.; Muriana, P.M. Purification and partial amino acid sequence of curvaticin FS47, a heat-stable bacteriocin produced by Lactobacillus curvatus FS47. Appl. Environ. Microbiol. 1994, 60, 2191–2195. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Muriana, P.M.; Klaenhammer, T.R. Purification and partial characterization of lactacin F, a bacteriocin produced by Lactobacillus acidophilus 11088. Appl. Environ. Microbiol. 1991, 57, 114–121. [Google Scholar] [CrossRef] [Green Version]
- Kushwaha, K.; Muriana, P.M. Adherence characteristics of Listeria strains isolated from three ready-to-eat meat processing plants. J. Food Prot. 2009, 72, 2125–2131. [Google Scholar] [CrossRef]
- Tiong, H.K.; Hartson, S.D.; Muriana, P.M. Comparison of surface proteomes of adherence variants of Listeria monocytogenes using LC-MS/MS for identification of potential surface adhesins. Pathogens 2016, 5, 40. [Google Scholar] [CrossRef] [Green Version]
- Veasey, S.; Muriana, P.M. Evaluation of electrolytically-generated hypochlorous acid (‘Electrolyzed Water’) for sanitation of meat and meat-contact surfaces. Foods 2016, 5, 42. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Otto, M. Staphylococcal biofilms. In Bacterial Biofilms; Romeo, T., Ed.; Springer: Berlin/Heidelberg, Germany, 2008; pp. 207–228. [Google Scholar]
- Møretrø, T.; Hermansen, L.; Holck, A.L.; Sidhu, M.S.; Rudi, K.; Langsrud, S. Biofilm formation and the presence of the intercellular adhesion locus ica among staphylococci from food and food processing environments. Appl. Environ. Microbiol. 2003, 69, 5648. [Google Scholar] [CrossRef] [Green Version]
- Chen, Q.; Xie, S.; Lou, X.; Cheng, S.; Liu, X.; Zheng, W.; Zheng, Z.; Wang, H. Biofilm formation and prevalence of adhesion genes among Staphylococcus aureus isolates from different food sources. MicrobiologyOpen 2020, 9, e00946. [Google Scholar] [CrossRef] [Green Version]
- Zhang, Z.; Schwartz, S.; Wagner, L.; Miller, W. A greedy algorithm for aligning DNA sequences. J. Comput. Biol. 2000, 7, 203–214. [Google Scholar] [CrossRef]
- Janda, J.M.; Abbott, S.L. 16S rRNA gene sequencing for bacterial identification in the diagnostic laboratory: Pluses, perils, and pitfalls. J. Clin. Microbiol. 2007, 45, 2761. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Petti, C.A. Detection and identification of microorganisms by gene amplification and sequencing. Clin. Infect. Dis. 2007, 44, 1108–1114. [Google Scholar] [PubMed]
- Rossi-Tamisier, M.; Benamar, S.; Raoult, D.; Fournier, P.E. Cautionary tale of using 16S rRNA gene sequence similarity values in identification of human-associated bacterial species. Int. J. Syst. Evol. Microbiol. 2015, 65, 1929–1934. [Google Scholar] [CrossRef] [PubMed]
- Wang, R.; Zhou, Y.; Kalchayanand, N.; Harhay, D.M.; Wheeler, T.L. Effectiveness and functional mechanism of a multicomponent sanitizer against biofilms formed by Escherichia coli O157:H7 and five Salmonella serotypes prevalent in the meat industry. J. Food Prot. 2020, 83, 568–575. [Google Scholar] [CrossRef]
- Aryal, M.; Muriana, P.M. Efficacy of commercial sanitizers used in food processing facilities for inactivation of Listeria monocytogenes, E. coli O157:H7, and Salmonella biofilms. Foods 2019, 8, 639. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gilbert, P.; Moore, L.E. Cationic antiseptics: Diversity of action under a common epithet. J. Appl. Microbiol. 2005, 99, 703–715. [Google Scholar] [CrossRef]
- Juven, B.J.; Pierson, M.D. Antibacterial effects of hydrogen peroxide and methods for its detection and quantitation. J. Food Prot. 1996, 59, 1233–1241. [Google Scholar] [CrossRef]
- Buffet-Bataillon, S.; Tattevin, P.; Bonnaure-Mallet, M.; Jolivet-Gougeon, A. Emergence of resistance to antibacterial agents: The role of quaternary ammonium compounds—A critical review. Int. J. Antimicrob. Agents 2012, 39, 381–389. [Google Scholar] [CrossRef] [PubMed]
- Sidhu, M.S.; Sørum, H.; Holck, A. Resistance to quaternary ammonium compounds in food-related bacteria. Microb. Drug Resist. 2002, 8, 393–399. [Google Scholar] [CrossRef] [PubMed]
- Heir, E.; Sundheim, G.; Holck, A.L. The qacG gene on plasmid pST94 confers resistance to quaternary ammonium compounds in staphylococci isolated from the food industry. J. Appl. Microbiol. 1999, 86, 378–388. [Google Scholar] [CrossRef] [PubMed]
- Wassenaar, T.; Ussery, D.; Nielsen, L.; Ingmer, H. Review and phylogenetic analysis of qac genes that reduce susceptibility to quaternary ammonium compounds in Staphylococcus species. Eur. J. Microbiol. Immunol. 2015, 5, 44. [Google Scholar] [CrossRef] [Green Version]
- Wang, C.; Cai, P.; Guo, Y.; Mi, Z. Distribution of the antiseptic-resistance genes qacEDelta1 in 331 clinical isolates of Pseudomonas aeruginosa in China. J. Hosp. Infect. 2007, 66, 93–95. [Google Scholar] [CrossRef] [PubMed]
- Son, H.-J.; Park, G.-T.; Cha, M.-S.; Heo, M.-S. Solubilization of insoluble inorganic phosphates by a novel salt- and pH-tolerant Pantoea agglomerans R-42 isolated from soybean rhizosphere. Bioresour. Technol. 2006, 97, 204–210. [Google Scholar] [CrossRef] [PubMed]
- Lu, J.; Nogi, Y.; Takami, H. Oceanobacillus iheyensis gen. nov., sp. nov., a deep-sea extremely halotolerant and alkaliphilic species isolated from a depth of 1050 m on the Iheya Ridge. FEMS Microbiol. Lett. 2001, 205, 291–297. [Google Scholar] [CrossRef]
- Singh, H.; Kaur, M.; Jangra, M.; Mishra, S.; Nandanwar, H.; Pinnaka, A.K. Antimicrobial properties of the novel bacterial isolate Paenibacilllus sp. SMB1 from a halo-alkaline lake in India. Sci. Rep. 2019, 9, 11561. [Google Scholar] [CrossRef]
- An, S.-Y.; Asahara, M.; Goto, K.; Kasai, H.; Yokota, A. Terribacillus saccharophilus gen. nov., sp. nov. and Terribacillus halophilus sp. nov., spore-forming bacteria isolated from field soil in Japan. Int. J. Syst. Evol. Microbiol. 2007, 57, 51–55. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Abdel-Rahman, M.A.; Hassan, S.E.-D.; Azab, M.S.; Mahin, A.-A.; Gaber, M.A. High improvement in lactic acid productivity by new alkaliphilic bacterium using repeated batch fermentation integrated with increased substrate concentration. BioMed Res. Int. 2019, 2019, 7212870. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Abdel-Rahman, M.A.; Hassan, S.E.-D.; Alrefaey, H.M.A.; El-Belely, E.F.; Elsakhawy, T.; Fouda, A.; Desouky, S.G.; Khattab, S.M.R. Subsequent improvement of lactic acid production from beet molasses by Enterococcus hirae ds10 using different fermentation strategies. Bioresour. Technol. Rep. 2021, 13, 100617. [Google Scholar] [CrossRef]
- Bischoff, M.; Bauer, J.; Preikschat, P.; Schwaiger, K.; Mölle, G.; Hölzel, C. First Detection of the Antiseptic Resistance Gene qacA/B in Enterococcus faecalis. Microb. Drug Resist. 2011, 18, 7–12. [Google Scholar] [CrossRef] [PubMed]
- Bassey, D.E.; Grigson, S.J.W. Degradation of benzyldimethyl hexadecylammonium chloride by Bacillus niabensis and Thalassospira sp. isolated from marine sediments. Toxicol. Environ. Chem. 2011, 93, 44–56. [Google Scholar] [CrossRef]
- Russell, A.D. Bacterial resistance to disinfectants: Present knowledge and future problems. J. Hosp. Infect. 1999, 43, S57–S68. [Google Scholar] [CrossRef]
- Jones, M.V.; Herd, T.M.; Christie, H.J. Resistance of Pseudomonas aeruginosa to amphoteric and quaternary ammonium biocides. Microbios 1989, 58, 49–61. [Google Scholar]
- Tabata, A.; Nagamune, H.; Maeda, T.; Murakami, K.; Miyake, Y.; Kourai, H. Correlation between resistance of Pseudomonas aeruginosa to quaternary ammonium compounds and expression of outer membrane protein OprR. Antimicrob. Agents Chemother. 2003, 47, 2093–2099. [Google Scholar] [CrossRef] [Green Version]
- Buffet-Bataillon, S.; Tattevin, P.; Maillard, J.-Y.; Bonnaure-Mallet, M.; Jolivet-Gougeon, A. Efflux pump induction by quaternary ammonium compounds and fluoroquinolone resistance in bacteria. Future Microbiol. 2016, 11, 81–92. [Google Scholar] [CrossRef]
- Mulder, I.; Siemens, J.; Sentek, V.; Amelung, W.; Smalla, K.; Jechalke, S. Quaternary ammonium compounds in soil: Implications for antibiotic resistance development. Rev. Environ. Sci. Bio/Technol. 2018, 17, 159–185. [Google Scholar] [CrossRef] [Green Version]
Organism | Culture Collection Designation | Strain Designation | Source |
---|---|---|---|
Pseudomonas aeruginosa | PMM 626 | P1 | Isolated from processed egg facility |
Pseudomonas aeruginosa | PMM 627 | P2 | Isolated from processed egg facility |
Staphylococcus aureus | PMM 174 | C1 | Isolated from cow udders |
Staphylococcus aureus | PMM 169 | C8 | Isolated from cow udders |
Staphylococcus equorium | PMM 854 | HS-7 | Isolated from hotdogs |
Bacillus sp. | PMM 435 | MNS1 | This study; abattoir worker boot |
Oceanobacillus sp. | PMM 436 | MNS2 | This study; abattoir worker boot |
Terribacillus sp. | PMM 437 | MNS4 | This study; abattoir worker boot |
Bacillus sp. | PMM 438 | MNS5 | This study; abattoir worker boot |
Paenibacillus sp. | PMM 439 | MNS6 | This study; abattoir worker boot |
Pseudomonas sp. | PMM 440 | KS1A2 | This study; abattoir worker boot |
Pseudomonas sp. | PMM 433 | KS1A3 | This study; abattoir worker boot |
Bacillus sp. | PMM 441 | KS1B1 | This study; abattoir worker boot |
Pseudomonas sp. | PMM 432 | KS1B2 | This study; abattoir worker boot |
Pantoea sp. | PMM 430 | KS1B3 | This study; abattoir worker boot |
Pantoea sp. | PMM 428 | KS2A3 | This study; abattoir worker boot |
Pseudomonas sp. | PMM 431 | KS2B1 | This study; abattoir worker boot |
Pseudomonas sp. | PMM 434 | KS2B2 | This study; abattoir worker boot |
Aerococcus sp. | PMM 426 | KS3A3 | This study; abattoir worker boot |
Pantoea sp. | PMM 429 | KS3B1 | This study; abattoir worker boot |
Enterococcus sp. (hirae) | PMM 442 | KS3B2 | This study; abattoir worker boot |
Enterococcus sp. (hirae) | PMM 443 | KS3B3 | This study; abattoir worker boot |
Enterococcus sp. | PMM 427 | KS3B4 | This study; abattoir worker boot |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Shah, K.; Muriana, P.M. Efficacy of a Next Generation Quaternary Ammonium Chloride Sanitizer on Staphylococcus and Pseudomonas Biofilms and Practical Application in a Food Processing Environment. Appl. Microbiol. 2021, 1, 89-103. https://0-doi-org.brum.beds.ac.uk/10.3390/applmicrobiol1010008
Shah K, Muriana PM. Efficacy of a Next Generation Quaternary Ammonium Chloride Sanitizer on Staphylococcus and Pseudomonas Biofilms and Practical Application in a Food Processing Environment. Applied Microbiology. 2021; 1(1):89-103. https://0-doi-org.brum.beds.ac.uk/10.3390/applmicrobiol1010008
Chicago/Turabian StyleShah, Kundan, and Peter M. Muriana. 2021. "Efficacy of a Next Generation Quaternary Ammonium Chloride Sanitizer on Staphylococcus and Pseudomonas Biofilms and Practical Application in a Food Processing Environment" Applied Microbiology 1, no. 1: 89-103. https://0-doi-org.brum.beds.ac.uk/10.3390/applmicrobiol1010008