Susceptibility of Staphylococcus aureus Isolated from Different Raw Meat Products to Disinfectants

Year 2024, , 10 - 18, 30.05.2024

Fatma Özdemir , Seza Arslan

https://doi.org/10.26650/EurJBiol.2024.1373950

Abstract

Objective: Staphylococcus aureus, a severe public health hazard, causes foodborne diseases from the consumption of contaminated food. Various antimicrobials and disinfectants are used throughout the food chain to reduce microbial contamination or eliminate microorganisms on food contact surfaces. However, little is known about the susceptibility of disinfectants to food pathogens, including S. aureus, which can develop resistance to antimicrobials and cause severe diseases.
Materials and Methods: The antimicrobial activity of triclosan, cetyltrimethylammonium bromide (CTAB), acetic acid, citric acid, and lactic acid against 50 S. aureus isolates, including multidrug-resistant (MDR) isolates originating from ground beef, chicken, and fish, was investigated using the broth microdilution method.
Results: The minimal inhibitory concentrations (MICs) of triclosan, CTAB, acetic acid, citric acid, and lactic acid against the isolates were 0.125-16 μg/mL, 0.25-32 μg/mL, 102.5-26250 μg/mL, 187.5-12000 μg/mL, and 703-22500 μg/mL, respectively. Almost all MDR isolates showed resistance to triclosan. There was a statistically significant difference in MICs between triclosan and organic acids, as well as between CTAB and organic acids (p < 0.05). However, a statistically significant difference was not observed in triclosan and CTAB, as well as in acetic acid and lactic acid (p > 0.05). Pearson correlation coefficient revealed a strong relationship between triclosan and multidrug resistance. Based on the multiple linear regression analysis, triclosan had a positive effect on multidrug resistance (p < 0.05).
Conclusion: This research gives helpful information on the susceptibility of disinfectants to S. aureus, particularly to resistant S. aureus isolates from meats, which may help to recommend proper disinfectant use in food production.

Keywords

Staphylococcus aureus, triclosan, cetyltrimethylammonium bromide, organic acids, minimum inhibitory concentration

References

• Götz F, Bannerman T, Schleifer KH. The genera Staphylococcus and Macrococcus. In: Dworkin M, Falkow S,E, Rosenberg E, Schleifer KH, Stackebrandt E, eds. The Prokaryotes. 3rd ed. New York, N.Y.: Springer; 2006:5-75. google scholar
• Bhunia AK. Foodborne microbial pathogens: Mechanisms and pathogenesis. New York, N.Y.: Springer; 2008. google scholar
• Ray B. Fundamental Food Microbiology. 3rd ed. Boca Raton, Florida: CRC press; 2004. google scholar
• Bloomfield SF, Exner M, Fara GM, Nath KJ, Scott EA. Hygiene procedures in the home and their effectiveness: A review of the scientific evidence base. International Scientific Forum on Home Hygiene. 2013. https://ifh-homehygiene.org/review-best-practice/hygiene-procedures-home-and-their-effectiveness-review-scientific-evidence-base/. google scholar
• Donaghy JA, Jagadeesan B, Goodburn K, et al. Relationship of sanitizers, disinfectants, and cleaning agents with antimicrobial resistance. J Food Prot. 2019;82(5):889-902. google scholar
• Beuchat LR. Surface decontamination of fruits and vegetables eaten raw: A review. World Health Organization. 1998. google scholar
• Lepaus BM, Rdcha JS, Sadjse JFB. Organic acids and hydro-gen peroxide can replace chlorinated compounds as sanitizers on strawberries, cucumbers and rocket leaves. Food Sci Technol. 2020;40:242-249. google scholar
• Suller MTE, Russell AD. Triclosan and antibiotic resistance in Staphylococcus aureus. J Antimicrob Chemother. 2000;46:11-18. google scholar
• Sheldon AT. Antiseptic “Resistance”: Real or perceived threat? Clin Infect Dis. 2005;40:1650-1656. google scholar
• Jones RD, Jampani HB, Newman JL, Lee AS. Triclosan: A review of effectiveness and safety in health care settings. Am J Infect Control. 2000;28:184-196. google scholar
• Glaser A. The ubiquitous triclosan: A common antibacterial agent exposed. Pesticides and You NCODM. 2004;24(3):12-17. google scholar
• Yao K, Wen K, Shan W, Jiang H, Shao B. An immunoaffinity purification method for the simultaneous analysis triclocarban and triclosan in foodstuffs by liquid chromatography tandem mass spectrometry. J Agric Food Chem. 2019;67:9088-9095. google scholar
• Azzouz A, Colon LP, Hejji L, Ballesteros E. Determination of alkylphenols, phenylphenols, bisphenol A, parabens, organophos-phorus pesticides and triclosan in different cereal-based foodstuffs by gas chromatography-mass spectrometry. Anal Bioanal Chem. 2020;412:2621-2631. google scholar
• Coia JE, Duckworth GJ, Edwards DI, et al. Guidelines for the con-trol and prevention of meticillin-resistant Staphylococcus aureus (MRSA) in healthcare facilities. J Hosp Infect. 2006;63S:S1-S44. google scholar
• Ciusa ML, Furi L, Knight D, et al. A novel resistance mechanism to triclosan that suggests horizontal gene transfer and demon-strates a potential selective pressure for reduced biocide suscepti-bility in clinical strains of Staphylococcus aureus. Int J Antimicrob Agents. 2012;40:210-220. google scholar
• Fan F, Yan K, Wallis NG, et al. Defining and combating the mecha-nisms of triclosan resistance in clinical isolates of Staphylococcus aureus. Antimicrob Agents Chemother. 2002;46(11):3343-3347. google scholar
• Beier RC, Poole TL, Brichta-Harhay DM, et al. Disinfectant and antibiotic susceptibility profiles of Escherichia coli O157:H7 strains from cattle carcasses, feces, and hides and ground beef from the United States. J Food Prot. 2013;76:6-17. google scholar
• Beier RC, Foley SL, Davidson MK, et al. Characterization of antibiotic and disinfectant susceptibility profiles among Pseudomonas aeruginosa veterinary isolates recovered during 1994-2003. J Appl Microbiol. 2014;118:326-342. google scholar
• Beier RC, Duke SE, Ziprin RL, et al. Antibiotic and disinfectant susceptibility profiles of vancomycin-resistant Enterococcus faecium (VRE) isolated from community wastewa-ter in Texas. Bull Environ Contam Toxicol. 2008;80:188-194. google scholar
• Beier RC, Callaway TR, Andrews K, et al. Disinfec-tant and antimicrobial susceptibility profiles of Salmonella strains from feedlot water-sprinkled cattle: Hides and feces. J Food Chem Nanotechnol. 2017;3:50-59. google scholar
• McBain AJ, Ledder RG, Moore LE, Catrenich CE, Gilbert P. Effects of quaternary-ammonium-based formulations on bacte-rial community dynamics and antimicrobial susceptibility. Appl Environ Microbiol. 2004;70(6):3449-3456. google scholar
• To MS, Favrin S, Romanova N, Griffiths MW. Postadap-tational resistance to benzalkonium chloride and subsequent physicochemical modifications of Listeria monocytogenes. Appl Environ Microbiol. 2002;68(11):5258-5264. google scholar
• Nakata K, Tsuchido T, Matsumura Y. Antimicrobial cationic sur-factant, cetyltrimethylammonium bromide, induces superoxide stress in Escherichia coli cells. J Appl Microbiol. 2011;110:568-579. google scholar
• Beier RC, Andrews K, Hume ME, et al. Disinfectant and antimicrobial susceptibility studies of Staphylococcus aureus strains and ST398-MRSA and ST5-MRSA strains from swine mandibular lymph node tissue, commercial pork sausage meat and swine feces. Microorganisms. 2021;9:2401. doi.org/10.3390/microorganisms9112401. google scholar
• Humayoun SB, Hiott LM, Gupta SK, et al. An assay for de-termining the susceptibility of Salmonella isolates to commer-cial and household biocides. PloS one. 2018;13(12):e0209072. doi.org/10.1371/journal.pone.0209072. google scholar
• Burns J, McCoy CP, Irwin NC. Synergistic activity of weak or-ganic acids against uropathogens. J Hosp Infect. 2021;111:78-88. google scholar
• Bai Y, Ding X, Zhao Q, et al. Development of an organic acid compound disinfectant to control food-borne pathogens and its ap-plication in chicken slaughterhouses. Poult Sci. 2022;101:101842. doi.org/10.1016/j.psj.2022.101842. google scholar
• In YW, Kim JJ, Kim HJ, Oh SW. Antimicrobial activities of acetic acid, citric acid and lactic acid against Shigella species. J Food Saf. 2013; 33:79-85. google scholar
• Pangprasit N, Srithanasuwan A, Suriyasathaporn W, et al. An-tibacterial activities of acetic acid against major and minor pathogens isolated from mastitis in dairy cows. Pathogens. 2020; 9:961. doi:10.3390/pathogens9110961. google scholar
• Beier RC, Byrd JA, Andrews K, et al. Disinfectant and an-timicrobial susceptibility studies of the foodborne pathogen Campylobacter jejuni isolated from the litter of broiler chicken houses. Poult Sci. 2021;100:1024-1033. google scholar
• Hussain G, Rahman A, Hussain T, Uddin S, Ali T. Citric and lactic acid effects on the growth inhibition of E. coli and S. typhymurium on beef during storage. Sarhad J Agric. 2015;31(3):183-190. google scholar
• Al-Rousan WM, Olaimat AN, Osaili TM, Al-Nabulsi AA, Ajo RY, Holley RA. Use of acetic and citric acids to in-hibit Escherichia coli O157:H7, Salmonella Typhimurium and Staphylococcus aureus in tabbouleh salad. Food Microbiol. 2018;73:61-66. google scholar
• Brakstad OG, Aasbakk K, Maeland JA. Detection of Staphylococcus aureus by polymerase chain reaction amplifica-tion of the nuc gene. J Clin Microbiol. 1992;30(7):1654-1660. google scholar
• Bannerman TL, Peacock SJ. Staphylococcus, Micrococcus, and other catalase-positive cocci. In: Versalovic J, Carroll KC, Funke G, Jorgensen JH, Landry ML, Warnock DW, eds. Manual of clin-ical microbiology, Washington, D.C: ASM Press; 2011:308-330. google scholar
• Clinical and Laboratory Standards Institute (CLSI), Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; Ninth edition, M7-A9, in, Wayne, PA, USA, 2012. google scholar
• Clinical and Laboratory Standards Institute (CLSI), Performance standards for antimicrobial susceptibility testing; 32nd edition, in, Malvern, PA, USA, 2022. google scholar
• Andrews JM. Determination of minimum inhibitory concentra-tions. J Antimicrob Chemother. 2001;48:5-16. google scholar
• Heath RJ, Rock CO. A triclosan-resistant bacterial enzyme. Nature. 2000;406:145-146. google scholar