Abstract
This present study aims to determine the lowest concentration effects of the assayed different antibiotics; antimicrobial agents alone and their combinations with nisin were investigated to prevent the biofilm formation and break down the biofilm structure of Salmonella. While the combination of nisin and EDTA showed a synergistic effect against Salmonella strain, chlorhexidine digluconate and streptomycin with nisin showed a partial synergetic effect; citric acid and sulfonamides with nisin showed an indifferent effect. The use of citric acid and chlorhexidine digluconate alone was very effective in Salmonella inhibition. While the citric acid combined with other agents had not much effect, the use of chlorhexidine digluconate combined with nisin and EDTA inactivated the total initial count within 24 h. Significantly, when citric acid and sulfonamides are used alone, they reduce by 64% and 44%, respectively. When they used nisin + EDTA, this ratio increased to 83% and 84%, respectively. For the prevention of biofilm, the most suitable conditions were determined as 97% biofilm inhibition. The results of this study can be used as a guide for the emergence of new approaches to ensure the food safety and quality of the food industry.
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References
Anriany Y, Sahu SN, Wessels KR, McCann LM, Joseph SW (2006) Alteration of the rugose phenotype in waaG and ddhC mutants of Salmonella enterica serovar Typhimurium DT104 is associated with inverse production of curli and cellulose. Appl Environ Microbiol 72(7):5002–5012. https://doi.org/10.1128/AEM.02868-05
Arnold JW, Bailey GW (2000) Surface finishes on stainless steel reduce bacterial attachment and early biofilm formation: scanning electron and atomic force microscopy study. Poultry Sci 79(12):1839–1845. https://doi.org/10.1093/ps/79.12.1839
Balcázar JL, Subirats J, Borrego CM (2015) The role of biofilms as environmental reservoirs of antibiotic resistance. Front Microbiol 6:1216. https://doi.org/10.3389/fmicb.2015.01216
Berger CN, Sodha SV, Shaw RK, Griffin PM, Pink D, Hand P, Frankel G (2010) Fresh fruit and vegetables as vehicles for the transmission of human pathogens. Environ Microbiol 12(9):2385–2397. https://doi.org/10.1111/j.1462-2920.2010.02297.x
Ceri H, Olson ME, Stremick C, Read RR, Morck D, Buret A (1999) The calgary biofilm device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J Clin Microbiol 37(6):1771–1776. https://doi.org/10.1128/jcm.37.6.1771-1776.1999
Chaudhary M, Payasi A (2012) Comparative efficacy of antibiotics in biofilms eradication formed by ESBL and non ESBL producing micro-organisms. Int J Drug Dev Res 4(2):138–142
Chavant P, Martinie B, Meylheuc T, Bellon-Fontaine MN, Hebraud M (2002) Listeria monocytogenes LO28: surface physicochemical properties and ability to form biofilms at different temperatures and growth phases. Appl Environ Microbiol 68:728–737. https://doi.org/10.1128/aem.68.2.728-737.2002
Chia TWR, Goulter RM, McMeekin T, Dykes GA, Fegan N (2009) Attachment of different Salmonella serovars to materials commonly used in a poultry processing plant. Food Microbiol 26(8):853–859. https://doi.org/10.1016/j.fm.2009.05.012
CLSI (2008) Clinical and Laboratory Standards Institute (CLSI). Performance standards for antimicrobial susceptibility testing: 18th informational supplement. CLSI, M100-S18 Clinical and Laboratory Standards Institute, Pennsylvania, p 940
De Vuyst L, Leroy F (2007) Bacteriocins from lactic acid bacteria: production, purification, and food applications. J Mol Microbiol Biotechnol 13:194–199. https://doi.org/10.1159/000104752
Ebrahimi A, Hemati M, Dehkordi SH et al (2014) Chlorhexidine digluconate effects on planktonic growth and biofilm formation in some field isolates of animal bacterial pathogens. Jundishapur J Nat Pharm Prod 9(2):e14298. https://doi.org/10.17795/jjnpp-14298
EFSA (2012) Scientific Opinion on a review on the European Union Summary Reports on trends and sources zoonoses, zoonotic agents and food-borne outbreaks in 2009 and 2010—specifically for the data on Salmonella, Campylobacter, verotoxigenic Escherichia coli, Listeria monocytogens. EFSA J. https://doi.org/10.2903/j.efsa.2012.2726
Eliopoulos GM, Moellering RC (1996) Antimicrobial combinations. In: Lorian V (ed) Antibiotic in laboratory medicine, 4th edn. Williams and Wilkins, Baltimore, pp 330–396
Gibson DL, White AP, Snyder SD, Martin S et al (2006) Salmonella produces an O-antigen capsule regulated by AgfD and important for environmental persistence. J Bacteriol 188(22):7722–7730. https://doi.org/10.1128/JB.00809-06
Gill AO, Holley RA (2003) Interactive inhibition of meat spoilage and pathogenic bacteria by lysozyme, nisin and EDTA in the presence of nitrite and sodium chloride at 24°C. Int J Food Microbiol 80(3):251–259. https://doi.org/10.1016/S0168-1605(02)00171-X
Joseph B, Otta SK, Karunasagar I, Karunasagar I (2001) Biofilm formation by Salmonella spp. on food contact surfaces and their sensitivity to sanitizers. Int J Food Microbiol 64(3):367–372. https://doi.org/10.1016/s0168-1605(00)00466-9
Karaca B, Buzrul S, Tato V, Akçelik N, Akçelik M (2013) Modeling and predicting the biofilm formation of different Salmonella strains. J Food Safety 33:503–508. https://doi.org/10.1111/jfs.12082
Khan A, Vu KD, Riedl B, Lacroix M (2015) Optimization of the antimicrobial activity of nisin, Na-EDTA and pH against gram-negative and gram-positive bacteria. LWT Food Sci Technol 61(1):124–129. https://doi.org/10.1016/j.lwt.2014.11.035
Khare AK, Biswas AK, Sahoo J (2014) Comparison study of chitosan, EDTA, eugenol and peppermint oil for antioxidant and antimicrobial potentials in chicken noodles and their effect on colour and oxidative stability at ambient temperature storage. LWT Food Sci Technol 55(1):289–293. https://doi.org/10.1016/j.lwt.2013.08.024
Kiffer CR, Sinto SJL, S, et al (2005) In vitro synergy test of meropenem and sulbactam against clinical isolates of Acinetobacter baumannii. Diagn Microbiol Infect Dis 52(4):317–322. https://doi.org/10.1016/j.diagmicrobio.2005.03.003
Ledeboer NA, Frye JG, McClelland M, Jones BD (2006) Salmonella enterica serovar typhimurium requires the Lpf, Pef, and Tafi fimbriae for biofilm formation on HEp-2 tissue culture cells and chicken intestinal epithelium. Infect Immun 74(6):3156–3169. https://doi.org/10.1128/IAI.01428-05
Lianou A, Koutsoumanis KP (2012) Strain variability of the biofilm-forming ability of Salmonella enterica under various environmental conditions. Int J Food Microbiol 160:171–178. https://doi.org/10.1016/j.ijfoodmicro.2012.10.002
Mani-López E, García HS, López-Malo A (2012) Organic acids as antimicrobials to control Salmonella in meat and poultry products. Food Res Int 45:713–721. https://doi.org/10.1016/j.foodres.2011.04.043
Misselwitz B, Kreibich SK, Rout S, Stecher B, Periaswamy B, Hardt WD (2011) Salmonella enterica serovar typhimurium binds to HeLa cells via Fim-mediated reversible adhesion and irreversible type three secretion system 1-mediated docking. Infect Immun 79(1):330–341. https://doi.org/10.1128/IAI.00581-10
Møretrø T, Heir E, Nesse LL, Vestby LK, Langsrud S (2012) Control of Salmonella in food related environments by chemical disinfection. Food Res Int 45:532–544. https://doi.org/10.1016/j.foodres.2011.02.002
Ogasawara H, Yamamoto K, Ishihama A (2011) Role of the biofilm master regulator CsgD in cross-regulation between biofilm formation and flagellar synthesis. J Bacteriol 193(10):2587–2597. https://doi.org/10.1128/JB.01468-10
Prouty AM, Gunn JS (2003) Comparative analysis of Salmonella enterica serovar typhimurium biofilm formation on gallstones and on glass. Infect Immun 71(12):7154–7158. https://doi.org/10.1128/IAI.71.12.7154-7158.2003
Prudencio CV, Mantovani HC, Cecon PR, Vanetti MCD (2014) Differences in the antibacterial activity of nisin and bovicin HC5 against Salmonella Typhimurium under different temperature and pH conditions. J App Microbiol 118:18–26. https://doi.org/10.1111/jam.12680
Raetz CRH, Whitfield C (2002) Lipopolysaccharide endotoxins. Annu Rev Biochem 71:635–700. https://doi.org/10.1146/annurev.biochem.71.110601.135414
Sedlacek MJ, Walker C (2007) Antibiotic resistance in an in vitro subgingival biofilm model. Oral Microbiol Immunol 22(5):333–339. https://doi.org/10.1111/j.1399-302X.2007.00366.x
Sheldon AT (2005) Antiseptic “resistance”: real or perceived threat? Clin Infect Dis 40(11):1650–1656. https://doi.org/10.1086/430063
Singh AP, Prabha V, Rishi P (2013) Value addition in the efficacy of conventional antibiotics by nisin against Salmonella. PLOS ONE 8(10):e76844. https://doi.org/10.1371/journal.pone.0076844
Steenackers H, Hermans K, Vanderleyden J, de Keersmaecker SCJ (2012) Salmonella biofilms: an overview on occurrence, structure, regulation and eradication. Food Res Int 45(2):502–531. https://doi.org/10.1016/j.foodres.2011.01.038
Stepanovic S, Vukovic D, Dakic I, Savic B, Svabic-Vlahovic M (2000) A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Methods 40:175–179. https://doi.org/10.1016/s0167-7012(00)00122-6
Stepanovic S, Irkovi I, Ranin L, Svabi-Vlahovi M (2004) Biofilm formation by Salmonella spp. and Listeria monocytogenes on plastic surface. Lett Appl Microbiol 38(5):428–432. https://doi.org/10.1111/j.1472-765X.2004.01513.x
Stewart PS, Rayner J, Roe F, Rees WM (2001) Biofilm penetration and disinfection efficacy of alkaline hypochlorite and chlorosulfamates. J Appl Microbiol 91:525–532. https://doi.org/10.1046/j.1365-2672.2001.01413.x
Teplitski M, Barak JD, Schneider KR (2009) Human enteric pathogens in produce: un-answered ecological questions with direct implications for food safety. Curr Opin Biotechnol 20(2):166–171. https://doi.org/10.1016/j.copbio.2009.03.002
Tong Z, Zhou L, Jiang W et al (2011) An in vitro synergetic evaluation of the use of nisin and sodium fluoride or chlorhexidine against Streptococcus mutans. Peptides 32:2021–2026. https://doi.org/10.1016/j.peptides.2011.09.002
Vaara M (1992) Agents that increase the permeability of the outer membrane. Microbiol Rev 56:395–411. https://doi.org/10.1128/mmbr.56.3.395-411.1992
Wan Norhana MN, Poole SE, Deeth HC, Dykes GA (2012) Effects of nisin, EDTA and salts of organic acids on Listeria monocytogenes, Salmonella and native microflora on fresh vacuum packaged shrimps stored at 4 °C. Food Microbiol 31(1):43–50. https://doi.org/10.1016/j.fm.2012.01.007
White AP, Gibson DL, Kim W, Kay WW, Surette MG (2006) Thin aggregative fimbriae and cellulose enhance long-term survival and persistence of Salmonella. J Bacteriol 188:3219–3227. https://doi.org/10.1128/JB.188.9.3219-3227.2006
Wong HS, Townsend KM, Fenwick SG, Trengove RD, O’Handley RM (2010) Comparative susceptibility of planktonic and 3-day-old Salmonella Typhimurium biofilms to disinfectants. J Appl Microbiol 108:2222–2228. https://doi.org/10.1111/j.1365-2672.2009.04630.x
Woodward MJ, Sojka M, Sprigings KA, Humphrey TJ (2000) The role of SEF14 and SEF17 fimbriae in the adherence of Salmonella enterica serotype Enteritidis to inanimate surfaces. J Med Microbiol 49:481–487. https://doi.org/10.1099/0022-1317-49-5-481
Xu H, Zou Y, Lee H, Ahn J (2010) Effect of NaCl on the biofilm formation by foodborne pathogens. J Food Sci 75(9):580–585. https://doi.org/10.1111/j.1750-3841.2010.01865.x
Yang Y, Miks-Krajnik M, Zheng Q, Lee SB, Lee SC, Yuk H (2016) Biofilm formation of Salmonella Enteritidis under food-related environmental stress conditions and its subsequent resistance to chlorine treatment. Food Microbiol 54:98–105. https://doi.org/10.1016/j.fm.2015.10.010
Yuksel FN, Buzrul S, Akcelik M, Akcelik N (2018) Inhibition and eradication of Salmonella typhimurium biofilm using P22 bacteriophage, EDTA and nisin. Biofouling 34:1046–1054. https://doi.org/10.1080/08927014.2018.1538412
Zogaj X, Nimtz M, Rohde M, Bokranz W, Römling U (2001) The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol Microbiol 39(6):1452–1463. https://doi.org/10.1046/j.1365-2958.2001.02337.x
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Özdemir, F.N., Buzrul, S., Özdemir, C. et al. Determination of an effective agent combination using nisin against Salmonella biofilm. Arch Microbiol 204, 167 (2022). https://doi.org/10.1007/s00203-022-02766-4
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DOI: https://doi.org/10.1007/s00203-022-02766-4