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Attachment and survival of bacteria on apples with the creation of a kinetic mathematical model

  • Food Microbiology - Research Paper
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Abstract

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.

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References

  1. 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

    Article  Google Scholar 

  2. 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

    Article  Google Scholar 

  3. 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

    Article  CAS  Google Scholar 

  4. 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

    Article  Google Scholar 

  5. 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

    Article  CAS  PubMed  Google Scholar 

  6. 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

    Article  CAS  Google Scholar 

  7. 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

    Article  CAS  Google Scholar 

  8. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Zwietering MH, Jongenburger I, Rombouts FM, Van’t Riet K (1990) Modeling of the bacterial growth curve. Appl Environ Micro 56(6):1875–1881

    Article  CAS  Google Scholar 

  11. 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

    Article  PubMed  Google Scholar 

  12. 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

    Article  CAS  Google Scholar 

  13. 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

    Article  Google Scholar 

  14. 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

    Article  CAS  PubMed  Google Scholar 

  15. 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

  16. Kukrić Z, Jašić M, Samelak I (2013) Biohemija hrane-biološki aktivne komponente. Tehnološki fakultet Banjaluka, Tehnološki fakultet Tuzla

  17. 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

    Article  CAS  PubMed  Google Scholar 

  18. 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

    Article  CAS  PubMed  Google Scholar 

  19. 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

    Article  CAS  PubMed  Google Scholar 

  20. 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

    Article  CAS  PubMed  Google Scholar 

  21. 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

    Article  CAS  Google Scholar 

  22. 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

    Article  CAS  PubMed  Google Scholar 

  23. 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

    Article  Google Scholar 

  24. European Committee for Antimicrobial Susceptibility Testing (EUCAST) (2000) Determination of minimum inhibitory concentrations (MICs) of antibacterial agents by agar dilution

  25. 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

    Article  CAS  PubMed  Google Scholar 

  26. 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

    Article  Google Scholar 

  27. 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

    Article  CAS  Google Scholar 

  28. 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

  29. 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

    Article  CAS  Google Scholar 

  30. 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

  31. 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

    Article  CAS  PubMed  Google Scholar 

  32. 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

    Article  CAS  Google Scholar 

  33. Cowan MM (1999) Plant products as antimicrobial agents. Clin Microbiol Rev 12:564–582

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Altuner EM, Çetin B, Çökmüş C (2010) Tortella tortulosa (Hedw.) Limp. özütlerinin antimikrobiyal aktivitesi. Kastamonu Üniversitesi Orman Fakültesi Dergisi 10(2):111–116

    Google Scholar 

  35. 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

  36. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. 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

    Article  CAS  Google Scholar 

  38. 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

    Article  CAS  Google Scholar 

  39. 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

    Article  CAS  PubMed  Google Scholar 

  40. 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

    Article  Google Scholar 

  41. 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

    Article  CAS  PubMed  Google Scholar 

  42. 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

    Article  CAS  Google Scholar 

  43. 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

    Article  CAS  Google Scholar 

  44. 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

    Article  CAS  Google Scholar 

  45. 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

    Article  CAS  Google Scholar 

  46. 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

    Article  PubMed  Google Scholar 

  47. 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

    Article  CAS  PubMed  Google Scholar 

  48. 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

    Article  Google Scholar 

  49. 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

    Article  CAS  Google Scholar 

  50. 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

    Article  CAS  PubMed  Google Scholar 

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Funding

This study is a result of the research conducted within the Project (19/6-020/961-19/14) financially supported by the Ministry for Scientific and Technological Development, Higher Education and Information Society of the Republic of Srpska.

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Authors and Affiliations

  1. Faculty of Technology, University of Banja Luka, Banja Luka, Bosnia and Herzegovina

    Aleksandar Savić, Ljiljana Topalić-Trivunović, Ana Velemir & Saša Papuga

  2. Veterinary Institute of Republic of Srpska “Dr. Vaso Butozan”, Banja Luka, Bosnia and Herzegovina

    Vesna Kalaba

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  1. Aleksandar Savić
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  2. Ljiljana Topalić-Trivunović
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  3. Ana Velemir
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  4. Saša Papuga
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Contributions

A.S., Lj-T-T, A.V., S.P. and V.K. conceived and designed the experiments; performed the experiments; analysed the data; contributed reagents, materials and analytical tools; and wrote the paper.

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Correspondence to Ana Velemir.

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Savić, A., Topalić-Trivunović, L., Velemir, A. et al. Attachment and survival of bacteria on apples with the creation of a kinetic mathematical model. Braz J Microbiol 52, 837–846 (2021). https://doi.org/10.1007/s42770-021-00425-2

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