Attachment and survival of bacteria on apples with the creation of a kinetic mathematical model
Tóm tắt
The estimation of growth or inactivation of bacterial population in fruits during preservation and storage provides useful information for the improvement of the safety of fresh-cut fruits and vegetables. This paper addressed the attachment to the surface and the growth in the flesh of apple fruits of four bacterial cultures (Escherichia coli, Bacillus cereus, Staphylococcus aureus and Pseudomonas aeruginosa). The growth of the bacterial cultures in apple flesh was monitored at particular time intervals, and Gompertz parameters, i.e. maximum number of bacteria (Pm), the maximum growth rate of bacteria rp,m, and lag time tl, were used to determine the growth kinetics. After the immersion, the highest number of P. aeruginosa and the lowest number of B. cereus adhered to the apples. After washing and swabbing, E. coli was reduced from the surface of apples to the highest extent (by 3.34 log cfu g−1), while the number of B. cereus was reduced to the lowest extent (1.66 log cfu g−1). Fitted curves of the Gompertz model corresponded quite well to the measured values of the number of microorganisms with R2 = 0.92–0.98. The values of the standard error (0.17–0.37) and extremely low p values of the Fischer test (p < 0.0001) indicated strict dependence between the model predicted and the maximum population density. The predicted values of the maximum number of microorganisms (Pm) correspond almost exactly to the actual values. A similar conclusion can be drawn for the maximum growth rate of microorganisms (rp,m), with the measured value being slightly higher than predicted values.
Tài liệu tham khảo
Juhneviča K, Skudra G, Skudra L (2011) Evaluation of microbiological contamination of apple fruit stored in a modified atmosphere. Environ Exper Biol 9:53–59. https://doi.org/10.22364/eeb
Fatema N, Acharjee M, Noor R (2013) Microbiological profiling of imported apples and demonstration of bacterial survival capacity through in vitro challenge test. Am J Microbiol Res 1(4):98–104. https://doi.org/10.12691/ajmr-1-4-6
Abadias M, Canamas TP, Asensio A, Anguera M, Vinas I (2006) Microbial quality of commercial “Golden Delicious” apples throughout production and shelf-life in Lleida (Catalonia, Spain). Int J Food Microiol 108(3):404–409. https://doi.org/10.1016/j.ijfoodmicro.2005.12.011
Harris LJ, Farber JN, Beuchat LR, Parish ME, Suslow TV, Garrett EH, Busta FF (2003) Outbreak associated with fresh produce: incidence, growth, and survival of pathogens in fresh and fresh-cut produce. Compr Rev Food Sci Food Saf 2(Supplement):78–141. https://doi.org/10.1111/j.1541-4337.2003.tb00031.x
Heaton JC, Jones K (2008) Microbial contamination of fruit and vegetables and behaviour of enteropathogens in the phyllosphere: a review. J Appl Microbiol 104(3):613–625. https://doi.org/10.1111/j.1365-2672.2007.03587.x
Burnett SL, Chen J, Beuchat LR (2000) Attachment of Escherichia coli O157:H7 to the surfaces and internal structures of apples as detected by confocal scanning laser microscopy. Appl Environ Micro 66(11):4679–4687. https://doi.org/10.1128/aem.66.11.4679-4687.2000
Alberto MR, Canavosio MAR, de Nadra MCM (2006) Antimicrobial effect of polyphenols from apple skins on human bacterial pathogens. Electron J Biotechnol 9(3):205–209. https://doi.org/10.2225/vol9-issue3-fulltext-1
Zhang T, Wei X, Miao Z, Hassan H, Song Y, Fan M (2016) Screening for antioxidant and antibacterial activities of phenolics from Golden Delicious apple pomace. Chem Cent J 10:47. https://doi.org/10.1186/s13065-016-0195-7
Tjørve KMC, Tjørve E (2017) The use of Gompertz models in growth analyses, and new Gompertz-model approach: an addition to the Unified-Richards family. PLoS One 12(6):e0178691. https://doi.org/10.1371/journal.pone.0178691
Zwietering MH, Jongenburger I, Rombouts FM, Van’t Riet K (1990) Modeling of the bacterial growth curve. Appl Environ Micro 56(6):1875–1881
Belda-Galbis CM, Pina-Pérez MC, Espinosa J, Marco-Celdrán A, Martínez A, Rodrigo D (2014) Use of the modified Gompertz equation to assess the Stevia rebaudiana Bertoni antilisterial kinetics. Food Microbiol 38:56–61. https://doi.org/10.1016/j.fm.2013.08.009
Srimachai T, Nuithitikul K, O-thong S, Kongjan P, Panpong K (2015) Optimization and kinetic modeling of ethanol production from oil palm frond juice in batch fermentation. Energy Procedia 79:111–118. https://doi.org/10.1016/j.egypro.2015.11.490
Papuga S, Savić A, Kisin Z (2018) Matematičko modelovanje proizvodnje etanola u toku fermentacije medovine. GHTERS 14:15–22. https://doi.org/10.7251/GHTE1814015P
Yoon J-H, Lee S-Y (2017) Review: comparison of the effectiveness of decontaminating strategies for fresh fruits and vegetables and related limitations. Crit Rev Food Sci Nutr 58(18):3189–3208. https://doi.org/10.1080/10408398.2017.1354813
Službeni list SFRJ (1983) Pravilnik o metodama uzimanja uzoraka i vršenja hemijskih i fizičkih analiza radi kontrole kvaliteta proizvoda od voća i povrća, 29/83
Kukrić Z, Jašić M, Samelak I (2013) Biohemija hrane-biološki aktivne komponente. Tehnološki fakultet Banjaluka, Tehnološki fakultet Tuzla
Wolfe K, Liu RH (2003) Apple peels as a value added food ingredient. J Agric Food Chem 51(6):1676–1683. https://doi.org/10.1021/jf020782a
Liyana-Pathirana CM, Shahidi F (2005) Antioxidant activity of commercial soft and hard wheat (Triticum aestivum L.) as affected by gastric pH conditions. J Agric Food Chem 53:2433–2440. https://doi.org/10.1021/jf049320i
Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 26(9–10):1231–1237. https://doi.org/10.1016/s0891-5849(98)00315-3
Benzie IFF, Strain JJ (1996) Ferric reducing ability of plasma (FRAP) as a measure of antioxidant power: the FRAP assay. Anal Biochem 239(1):70–76. https://doi.org/10.1006/abio.1996.0292
Kawakami H, Kittaka K, Sato Y, Kikuchi Y (2010) Bacterial attachment and initiation of biofilms on the surface of copper containing stainless steel. ISIJ Int 50(1):133–138. https://doi.org/10.2355/isijinternational.50.133
Tomita K, Sawai J (2017) Preincubation of Escherichia coli ATCC 25922 with NaCl increases its attachment to lettuce surfaces compared with other chemicals. Biocontrol Sci 22(3):137–143. https://doi.org/10.4265/bio.22.137
Balouiri M, Sadiki M, Ibnsouda SK (2016) Methods for in vitro evaluating antimicrobial activity: a review. Pharma Anal 6:71–79. https://doi.org/10.1016/j.jpha.2015.11.005
European Committee for Antimicrobial Susceptibility Testing (EUCAST) (2000) Determination of minimum inhibitory concentrations (MICs) of antibacterial agents by agar dilution
Liao C-H, Sapers GM (2000) Attachment and growth of Salmonella Chester on apple fruits and in vivo response of attached bacteria to sanitizer treatments. J Food Prot 63(7):876–883. https://doi.org/10.4315/0362-028x-63.7.876
Pietrysiak E, Ganjyial MG (2018) Apple peel morphology and attachment of Listeria innocua through aqueous environment as shown by scanning electron microscopy. Food Control 92:362–369. https://doi.org/10.1016/j.foodcont.2018.04.049
Herigstad B, Hamilton M, Heersink J (2001) How to optimize the drop plate method for enumerating bacteria. J Microbiol Meth 44:121–129. https://doi.org/10.1016/S0167-7012(00)00241-4
Lee LH, Zainal N, Azman AS, Eng SH, Goh BH, Yin WF, Ab Mutalib NS, Chan KG (2014) Diversity and antimicrobial activity of Actinobacteria isolated from tropical mangrove sediments in Malaysia. The Scientific World Journal:1–14. https://doi.org/10.1155/2014/698178
Ravi Kumar G, Prashant A (2015) Evaluation of antioxidant activity of apple peel and pulp extracts by using different solvents. Chem Sci Trans 4(3):723–727. https://doi.org/10.7598/cst2015.1041
Venkatesan T, Young-Woong C, Young-Kyoon K (2019) Impact of different extraction solvents on phenolic content and antioxidant potential of Pinus densiflora bark extract. Biomed Res Int:1–14. https://doi.org/10.1155/2019/3520675
Chinnici F, Bendini A, Gaiani A, Riponi C (2004) Radical scavenging activities of peels and pulps from cv. Golden Delicious apples as related to their phenolic composition. J Agric Food Chem 52:4684–4689. https://doi.org/10.1021/jf049770a
Khanizadeh S, Tsao R, Rekika D, Yang R, Charles M, Rupasinghe V (2008) Polyphenol composition and total antioxidant capacity of selected apple genotypes for processing. J Food Compos Anal 21:396–401. https://doi.org/10.1016/j.jfca.2008.03.004
Cowan MM (1999) Plant products as antimicrobial agents. Clin Microbiol Rev 12:564–582
Altuner EM, Çetin B, Çökmüş C (2010) Tortella tortulosa (Hedw.) Limp. özütlerinin antimikrobiyal aktivitesi. Kastamonu Üniversitesi Orman Fakültesi Dergisi 10(2):111–116
Valgas SM, DeSouza EFA, Smânia et al. (2007) Screening methods to determine antibacterial activity of natural products. Braz J Microbiol 38:369–380. https://doi.org/10.1590/S1517-83822007000200034
Caesar LK, Cech NB (2019) Synergy and antagonism in natural product extract: when 1 + 1 does not equal 2. Nat Prod Rep 36:869–888. https://doi.org/10.1039/C9NP00011A
Koolen HHF, da Silva FMA, Gozzo FC, de Souza AQL, de Souza ADI (2013) Antioxidant, antimicrobial activities and characterization of phenolic compounds from Buriti (Mauritia flexuosa L. f.) by UPLC-ESI-MS/MS. Food Res Int 51:467–473. https://doi.org/10.1016/j.foodres.2013.01.039
Sapers GM, Miller RL, Mattrazzo AM (1999) Effectiveness of sanitizing agents in inactivating Escherichia coli in Golden Delicious apples. J Food Sci 64(4):734–737. https://doi.org/10.1111/j.1365-2621.1999.tb15121.x
Wang H, Feng H, Liang W, Luo Y, Malyarchuk V (2009) Effect of surface roughness on retention and removal of Escherichia coli O157:H7 on surfaces of selected fruits. J Food Sci 74(1):E8–E14. https://doi.org/10.1111/j.1750-3841.2008.00998.x
Vanchaecke E, Remon JP, Moors M, Reas F, De Rudder D, Van Peteghem A (1990) Kinetics of Pseudomonas aeruginosa adhesion to 304 and 316-L stainless steel: role of cell surface hydrophobicity. Appl Environ Micro 56(3):788–795
Klausen M, Heydorn A, Ragas P, Lambertsen L, Aeas-Jørgensen A, Molin S, Tolker-Nielsen T (2003) Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants. Mol Microbiol 48(6):1511–1534. https://doi.org/10.1046/j.1365-2958.2003.03525.x
Choi N-Y, Bae Y-M, Lee S-Y (2015) Cell surface properties and biofilm formation of pathogenic bacteria. Food Sci Biotechnol 24(6):2257–2264. https://doi.org/10.1007/s10068-015-0301-y
Zhao X, Zhao F, Wang J, Zhong N (2017) Biofilm formation and control strategies of foodborne pathogens: food safety perspectives. RSC Adv 7:36670–36683. https://doi.org/10.1039/c7ra02497e
Crouzet M, Claverol S, Lomenech A-M, Le Sénéchal C, Costaglioli P, Barhte C, Garbay B, Bonneu M, Vilain S (2017) Pseudomonas aeruginosa cells attached to a surface display a typical proteome early as 20 minutes of incubation. PLoS One 1(7):e0180341. https://doi.org/10.1371/journal.pone.0180341
Palmer J, Flint S, Brooks J (2007) Bacterial cell attachment, the beginning of a biofilm. J Ind Microbiol Biot 34:577–588. https://doi.org/10.1007/s10295-007-0234-4
Elhariry HM (2011) Attachment strength and biofilm forming ability of Bacillus cereus on green-leafy vegetables: cabbage and lettuce. Food Microbiol 28(7):1266–1274. https://doi.org/10.1016/j.fm.2011.05.004
Herrera JJR, Cabo ML, Gonzalez A, Pazos I, Pastoriza L (2007) Adhesion and detachment kinetics of several strains of Staphylococcus aureus subsp. aureus under three different experimental conditions. Food Microbiol 24(6):585–591. https://doi.org/10.1016/j.fm.2007.01.001
Jeronimo HMA, Queiroga RCRE, Costa ACV, Barbosa IM, Conceicao ML, Souza EL (2012) Adhesion and biofilm formation by Staphylococcus aureus from food processing plants as affected by growth medium, surface type and incubation temperature. Braz J Pharm Sci 48(4):737–745. https://doi.org/10.1590/S1984-82502012000400018
Meira QGS, Barbosa IM, Athayde AJAA, Siqueira-Junior JP, Souza EL (2012) Influence of temperature and surface kind on biofilm formation by Staphylococcus aureus from food-contact surface and sensitivity to sanitizers. Food Control 25(1):469–475. https://doi.org/10.1016/j.foodcont.2011.11.030
Morikawa M (2006) Beneficial biofilm formation by industrial bacteria Bacillus subtilis and related species. J Biosci Bioeng 101(1):1–8. https://doi.org/10.1263/jbb.101.1