Enzyme-based approaches to control microbial biofilms in dairy processing environments: A review

Main Article Content

S. F. Gonçalves
S. H. I. Lee
A. Mousavi Khaneghah
C. A. F. Oliveira

Keywords

biofilm, enzyme-based preparations, industrial hygiene, surface contamination

Abstract

In this review, formation of biofilms and the available data on enzyme-based preparations to control microbial biofilms in dairy processing environments are presented. Mature biofilms, especially those formed by pathogenic bacteria, have increased resistance to biocides, hence stressing the importance of stringent hygienic procedures. Proteases, amylases, cellulases and DNAses are among the most recently studied enzymes that could be associated with the main biocides used in the dairy industry to increase the effect of removal of biofilm. However, additional studies should be conducted to select the best cost-benefit combinations of selected enzymes and biocides to remove efficiently biofilms in dairy processing environments.

Abstract 1079 | PDF Downloads 630 HTML Downloads 147 XML Downloads 26

References

Ahmed, A.M. and Shimamoto, T., 2014. Isolation and molecular characterization of Salmonella enterica, Escherichia coli O157:H7 and Shigella spp. from meat and dairy products in Egypt. International Journal of Food Microbiology 168: 57–62. 10.1016/j.ijfoodmicro.2013.10.014

Akrami-Mohajeri, F., Derakhshan, Z., Ferrante, M., Hamidiyan, N., Soleymani, M., Conti, G.O., et al., 2018. The prevalence and antimicrobial resistance of Listeria spp in raw milk and traditional dairy products delivered in Yazd, central Iran (2016). Food and Chemical Toxicology 114: 141–144. 10.1016/j.fct.2018.02.006

Alonso, V.P.P. and Kabuki, D.Y., 2019. Formation and dispersal of biofilms in dairy substrates. International Journal of Dairy Technology 70: 1–6. 10.1111/1471-0307.12587

Araújo, P.A., Machado, I., Meireles, A., Leikness, T., Mergulhão, F., Melo, L.F. et al., 2017. Combination of selected enzymes with cetyltrimethylammonium bromide in biofilm inactivation, removal and regrowth. Food Research International 95: 101–107. 10.1016/j.foodres.2017.02.016

Assaf, J.C., El Khoury, A., Chokr, A., Louka, N. and Atoui, L., 2019. A novel method for elimination of aflatoxin M1 in milk using Lactobacillus rhamnosus GG biofilm. International Journal of Dairy Technology 72: 248–256. 10.1111/1471-0307.12578

Augustin, M., Ali-Vehmas, T. and Atroshi, F., 2004. Assessment of enzymatic cleaning agents and disinfectants against bacterial biofilms. Journal of Pharmacy and Pharmaceutical Sciences 7: 55–64. Available at: https://sites.ualberta.ca/~csps/JPPS7(1)/F.Atroshi/biofilm.pdf

Borrajo, P., Pateiro, M., Gagaoua, M., Franco, D., Zhang, W. and Lorenzo, J.M., 2020. Evaluation of the antioxidant and antimicrobial activities of porcine liver protein hydrolysates obtained using alcalase, bromelain, and papain. Applied Sciences 10: 2290. 10.3390/app10072290

Bottone, E.J., 2010. Bacillus cereus, a volatile human pathogen. Clinical Microbiology Review 23: 382–398. 10.1128/CMR.00073-09

Bridier, A., Briandet, R., Thomas, V. and Dubois-Brissonnet, F., 2011. Resistance of bacterial biofilms to disinfectants: a review. Biofouling 27: 1017–1032. 10.1080/08927014.2011.626899

Cha, Y., Son, B. and Ryu, S., 2019. Effective removal of staphylococcal biofilms on various food contact surfaces by Staphylococcus aureus phage endolysin LysCSA13. Food Microbiology 84: 103245. 10.1016/j.fm.2019.103245

Chen, Y., Burall, L.S., Macarisin, D., Pouillot, R., Strain, E., De Jesus, A.J., et al., 2016. Prevalence and level of Listeria monocytogenes in ice cream linked to a listeriosis outbreak in the United States. Journal of Food Protection 79: 1828–1832. 10.4315/0362-028x.jfp-16-208

Cherif-Antar, A., Moussa–Boudjemâa, B., Didouh, N., Medjahdi, K., Mayo, B. and Flórez, A B., 2016. Diversity and biofilm-forming capability of bacteria recovered from stainless steel pipes of a milk-processing dairy plant. Dairy Science and Technology 96: 27–38. 10.1007/s13594-015-0235-4

Colagiorgi, A., Bruini, I., Di Ciccio, P.A., Zanardi, E., Ghidii, S. and Ianieri, A., 2017. Listeria monocytogenes biofilms in the wonderland of food industry. Pathogens 6: 41. 10.3390/pathogens6030041

Combrouse, T., Sadovskaya, I., Faille, C., Kol, O., Guérardel, Y. and Midelet-Bourdin, G., 2013. Quantification of the extracellular matrix of the Listeria monocytogenes biofilms of different phylogenic lineages with optimization of culture conditions. Journal of Applied Microbiology 114: 1120–1131. 10.1111/jam.12127

Coughlan, L.M., Cotter, P.D., Hill, C. and Alvarez-Ordóñez, A., 2016. New weapons to fight old enemies: novel strategies for the (bio) control of bacterial biofilms in the food industry. Frontiers in Microbiology 7: 1641. 10.3389/fmicb.2016.01641

Craigen, B., Dashiff, A. and Kadouri D.E., 2011. The use of commercially available alpha-amylase compounds to inhibit and remove Staphylococcus aureus biofilms. The Open Microbiology Journal 5: 21–31. 10.2174/1874285801105010021

Cusato, S., Gameiro, A.H., Sant’ana, A.S., Corassin, C.H., Cruz, A.G., Faria, J.A.F. and Oliveira, C.A.F., 2014. Assessing the costs involved in the implementation of GMP and HACCP in a small dairy factory. Quality Assurance and Safety of Crops & Foods 6: 135–139. 10.3920/QAS2012.0195

Di Ciccio, P., Vergara, A., Festino, A.R., Paludi, D., Zanardi, E., Ghidini, S. and Ianieri, A., 2015. Biofilm formation by Staphylococcus aureus on food contact surfaces: relationship with temperature and cell surface hydrophobicity. Food Control 50: 930–936. 10.1016/j.foodcont.2014.10.048

Dominciano, L.C.C., Lee, S.H.I., Corassin, C.H., De Martinis, E.C.P. and Oliveira, C.A.F., 2016. Effects of oleuropein and peracetic acid as sanitizing agents for inactivation of Listeria monocytogenes biofilms. The Open Conference Proceedings Journal 7: 1–6. 10.2174/2210289201607010001

Ehling-Schulz, M., Lereclus, D. and Koehler, T.M., 2019. The Bacillus cereus group: Bacillus species with pathogenic potential. Microbiology Spectrum 7: 875–902. 10.1128/microbiolspec.GPP3-0032-2018

Fleming, H.C., Wingender, J., Szewzyk, U., Steinberg, P., Rice, S.A. and Kjelleberg, S., 2016. Biofilms: an emergent form of bacterial life. Nature Reviews Microbiology 14: 563–575. 10.1038/nrmicro.2016.94

Gopal, N., Ross, P.R., Beresford, T.P., Fenelon, M.A. and Cotter, P.D., 2015. The prevalence and control of Bacillus and related spore-forming bacteria in the dairy industry. Frontiers in Microbiology 6: 1418. 10.3389/fmicb.2015.01418

Grande, R., Di Giulio, M., Bessa, L.J., Di Campli, E., Baffoni, M., Guarnieri, S. et al., 2011. Extracellular DNA in Helicobacter pylori biofilm: a backstairs rumor. Journal of Applied Microbiology 110: 490–498. 10.1111/j.1365-2672.2010.04911.x

Guerrero-Navarro, A.E., Rios-Castillo, A.G., Ripolles-Avilla, C., Hascoet, A.S., Felipe, X. and Rodriguez-Jereza, J.J., 2019. Development of a dairy fouling model to assess the efficacy of cleaning procedures using alkaline and enzymatic products. Food Science and Technology 106: 44–49. 10.1016/j.lwt.2019.02.057

Gutiérrez, D., Delgado, S., Vázquez-Sánchez, D., Martínez, B., Cabo, M.L., Rodríguez, A., et al., 2012. Incidence of Staphylococcus aureus and analysis of associated bacterial communities on food industry surfaces. Applied and Environmental Microbiology 78: 8547–8554. 10.1128/AEM.02045-12

Høiby, N., 2017. A short history of microbial biofilms and biofilm infections. Journal of Pathology, Microbiology and Immunology 125: 272–275. 10.1111/apm.12686

Hooshdar, P., Kermanshahi, R.K., Ghadam, P. and Khosravi-Darani, K., 2020. A review on production of exopolysaccharide and biofilm in probiotics like lactobacilli and methods of analysis. Biointerface Research in Applied Chemistry 10: 6058–6075. 10.33263/BRIAC105.60586075

Jakobsen, R.A., Heggebø, R., Sunde, E.B. and Skjervheim, M., 2011. Staphylococcus aureus and Listeria monocytogenes in Norwegian raw milk cheese production. Food Microbiology 3: 492–496. 10.1016/j.fm.2010.10.017

Jamali, H., Paydar, M., Radmehr, B., Ismail, S. and Dadrasnia, A., 2015. Prevalence and antimicrobial resistance of Staphylococcus aureus isolated from raw milk and dairy products. Food Control 54: 383–388. 10.1016/j.foodcont.2015.02.013

Jeong, D., Kim, D.-H., Song, K.-Y. and Seo, K.-H., 2018. Antimicrobial and anti-biofilm activities of Lactobacillus kefiranofaciens DD2 against oral pathogens. Journal of Oral Microbiology 10: 1472985. 10.1080/20002297.2018.1472985

Kadam, S.R., Besten, H.M.W., Veen, S., Zwieteringb, M.H., Moezelaar, R. and Abee, T., 2013. Diversity assessment of Listeria monocytogenes biofilm formation: impact of growth condition, serotype and strain origin. International Journal of Food Microbiology 165: 259–264. 10.1016/j.ijfoodmicro.2013.05.025

Kim, N.-N., Kim, W.J. and Kang, S.-S., 2019. Anti-biofilm effect of crude bacteriocin derived from Lactobacillus brevis DF01 on Escherichia coli and Salmonella Typhimurium. Food Control 98: 274–280. 10.1016/j.foodcont.2018.11.004

Koohy, H., Down, T.A. and Hubbard, T.J., 2013. Chromatin accessibility data sets show bias due to sequence specificity of the DNAse I enzyme. PLoS One 8: 1–9. 10.1371/journal.pone.0069853

Kwon, M., Hussain, M.S. and Oh, D.H., 2017. Biofilm formation of Bacillus cereus under food-processing-related conditions. Food Science and Biotechnology 26: 1103–1111. 10.1007/s10068-017-0129-8

Lee, S.H.I., Barancelli, G.V., Camargo, T.M., Corassin, C.H., Rosim, R.E., Cruz, A.G., et al., 2017a. Biofilm-producing ability of Listeria monocytogenes isolates from Brazilian cheese processing plants. Food Research International 91: 88–91. 10.1016/j.foodres.2016.11.039

Lee, S.H.I., Barancelli, G.V., Rosim, R.E., Corassin, C.H., Coppa, C.F.S.C. and Oliveira, C.A.F., 2017b. Effect of peracetic acid on biofilms formed by Listeria monocytogenes strains isolated from a Brazilian cheese processing plant. Brazilian Journal of Pharmaceutical Sciences 53: 1–7. 10.1590/s2175-97902017000300071

Lee, S.H.I., Cappato, L.P., Corassin, C.H., Cruz, A.G. and Oliveira, C.A.F., 2016. Effect of peracetic acid on biofilms formed by Staphylococcus aureus and Listeria monocytogenes isolated from dairy plants. Journal of Dairy Science 99: 2384–2390. 10.3168/jds.2015-10007

Lee, S.H.I., Mangolin, B.L.C., Gonçalves, J.L., Neef, D.V., Silva, M.P., Cruz, A.G. et al., 2014. Biofilm-producing ability of Staphylococcus aureus isolates from Brazilian dairy farms. Journal of Dairy Science 97: 1812–1816. 10.3168/jds.2013-7387

Lim, E.S., Koo, O.K., Kim, M.J. and Kim, J.-S., 2019. Bio-enzymes for inhibition and elimination of Escherichia coli O157:H7 bioflm and their synergistic effect with sodium hypochlorite. Scientific Reports 9: 9920. 10.1038/s41598-019-46363-w

Mansouri-Najand, L., Kianpour, M., Sami, M. and Jajarmi, M., 2015. Prevalence of Listeria monocytogenes in raw milk in Kerman, Iran. Veterinary Research Forum 6: 223–226. Available at: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4611976/pdf/vrf-6-223.pdf

Marchand, S., De Block, J., De Jonghe, A., Coorevits, A., Heyndrickx, M. and Herman, L., 2012. Biofilm formation in milk production and processing environments; influence on milk quality and safety. Comprehensive Reviews in Food Science and Food Safety 11: 133–147. 10.1111/j.1541-4337.2011.00183.x

Mazaheri, T., Ripolles-Avilla, C., Hascoet, A.S. and Rodriguez-Jerez, J.J., 2020. Effect of an enzymatic treatment on the removal of mature Listeria monocytogenes biofilms: a quantitative and qualitative study. Food Control 114: 107266. 10.1016/j.foodcont.2020.107266

Meng, L., Zhang, Y., Liu, H., Zhao, S., Wang, J. and Zheng, N., 2017. Characterization of Pseudomonas spp. and associated proteolytic properties in raw milk stored at low temperatures. Frontiers in Microbiology 8: 2158. 10.3389/fmicb.2017.02158

Mnif, S., Jardak, M., Yaich, A. and Aifa, S., 2020. Enzyme-based strategy to eradicate monospecies Macrococcus caseolyticus biofilm contamination in dairy industries. International Dairy Journal 100: 104560. 10.1016/j.idairyj.2019.104560

Mohamed, S.H., Mohamed, M.S.M., Khalil, M.S., Mohamed, W.S. and Mabrouk, M.I., 2018. Antibiofilm activity of papain enzyme against pathogenic Klebsiella pneumoniae. Journal of Applied Pharmaceutical Science 8: 163–168. 0.7324/japs.2018.8621

Mullan, W.M.A., 2019. Are we closer to understanding why viable cells of Mycobacterium avium subsp. paratuberculosis are still being reported in pasteurized milk? International Journal of Dairy Technology 72: 332–344. 10.1111/1471-0307.12617

Nahar, S., Mizan, M.K.R., Ha, A. J.-W. and Ha, S.-D., 2018. Advances and future prospects of enzyme-based biofilm prevention approaches in the food industry. Comprehensive Reviews in Food Science and Food Safety 17: 1484–1502. 10.1111/1541-4337.12382

Owusu-Kwarteng, J., Wuni, A., Akabanda, F., Tano-Debrah, K. and Jespersen, L., 2017. Prevalence, virulence factor genes and antibiotic resistance of Bacillus cereussensu lato isolated from dairy farms and traditional dairy products. BMC Microbiology 17: 65. 10.1186/s12866-017-0975-9

Oxaran, V., Dittmann, K.K., Lee, S.H.I., Chaul, L.T., Oliveira, C.A.F., Corassin, C.H., et al., 2018. Behavior of foodborne pathogens, Listeria monocytogenes and Staphylococcus aureus, in mixed-species biofilm exposed to biocides. Applied and Environmental Microbiology 84: e020038-18. 10.1128/AEM.02038-18

Puga, C.H., Rodríguez-Lopez, P., Cabo, M.L., SanJose, C. and Orgaz, B., 2018. Enzymatic dispersal of dual-species biofilms carrying Listeria monocytogenes and other associated food industry bacteria. Food Control 94: 222–228. 10.1016/j.foodcont.2018.07.017

Ripolles-Avila, C., Ramos-Rubio, M., Hascoet, A.S., Castillo, M. and Rodriguez-Jerez, J.J., 2020. New approach for the removal of mature biofilms formed by wild strains of Listeria monocytogenes isolated from food contact surfaces in an Iberian pig processing plant. International Journal of Food Microbiology 323: 108595. https10.1016/j.ijfoodmicro.2020.108595

Rodríguez-López, P., Carballo-Justo, A., Draper, L.A. and Cabo, M.L., 2016. Removal of Listeria monocytogenes dual-species biofilms using combined enzyme benzalkonium chloride treatments. Biofouling 33: 45–58. 10.1080/08927014.2016.1261847

Rodríguez-López, P., Rodriguez-Herrera, J.J., Vazquez-Sanchez, D. and Cabo, M.L., 2018. Current knowledge on Listeria monocytogenes biofilms in food-related environments: incidence, resistance to biocides, ecology and biocontrol. Foods 7: 85. 10.3390/foods7060085

Rossi, C., Serio, A., Chaves-López, C., Anniballi, F., Auricchi, B., Goffredo, E. et al., 2018. Biofilm formation, pigment production and motility in Pseudomonas spp. isolated from the dairy industry. Food Control 86: 241–248. 10.1016/j.foodcont.2017.11.018

Ryser, E.T., 2011. Pathogens in milk: Listeria monocytogenes. In: Fuquay, J.W. (ed.) Encyclopedia of dairy sciences, 2nd ed. Academic Press, London, pp. 1650–1655.

Sadekuzzaman, M., Yang, S., Mizan, M.F.R. and Ha, S.D., 2015. Current and recent advanced strategies for combating biofilms. Comprehensive Reviews in Food Science and Food Safety 14: 491–509. 10.1111/1541-4337.12144

Saggu, S.K., Jha, G. and Mishra, P.C., 2019. Enzymatic degradation of biofilm by metalloprotease from Microbacterium sp. Sks10. Frontiers in Bioengineering and Biotechnology 7: 192. 10.3389/fbioe.2019.00192

Sáringer, S., Akula, R.A., Szerlauth, A. and Szilagy, I., 2019. Papain adsorption on latex particles: charging, aggregation, and enzymatic activity. The Journal of Physical Chemistry B 123: 9984–9991. 10.1021/acs.jpcb.9b08799

Shi, X. and Zhu, X., 2009. Biofilm formation and food safety in food industries. Trends in Food Science and Technology 20: 407–413. 10.1016/j.tifs.2009.01.054

Silva, E.P. and De Martinis, E.C., 2013. Current knowledge and perspectives on biofilm formation: the case of Listeria monocytogenes. Applied Microbiology and Biotechnology 97: 957–968. 10.1007/s00253-012-4611-1

Song, Y.J., Yu, H.H., Kim, Y.J., Lee, N.-K. and Paik, H.-D., 2020. The use of papain for the removal of biofilms formed by pathogenic Staphylococcus aureus and Campylobacter jejuni. Food Science and Technology 127: 109383. 10.1016/j.lwt.2020.109383

Srey, S., Jahid, I.K. and Ha, S.D., 2013. Biofilm formation in food industries: a food safety concern. Food Control 31: 572–585. 10.1016/j.foodcont.2012.12.001

Sundarram, A. and Murthy, T.P.K., 2014. α-Amylase production and applications: a review. Journal of Applied and Environmental Microbiology 2: 166–175. 10.12691/jaem-2-4-10

Thallinger, B., Prasetyo, E.N., Nyanhongo, G.S. and Guebitz, G.M., 2013. Antimicrobial enzymes: an emerging strategy to fight microbes and microbial biofilms. Biotechnology Journal 8: 97–109. 10.1002/biot.201200313

Unlu, A., Sar, T., Seker, G., Erman, A.G., Kalpar, E. and Akbas, M.Y., 2018. Biofilm formation by Staphylococcus aureus strains and their control by selected phytochemicals. International Journal of Dairy Technology 71: 637–646. 10.1111/1471-0307.12520

Vidic, J., Chaix, C., Manzano, M. and Heyndrickx, M., 2020. Food sensing: detection of Bacillus cereus spores in dairy products. Biosensors 10: 15. 10.3390/bios10030015

Wang, H., Wang, H., Xing, T., Wu, N., Xu, X. and Zhou, G., 2016. Removal of Salmonella biofilm formed under meat processing environment by surfactant in combination with bio-enzyme. Food Science and Technology 66: 298–304. 10.3389/fmicb.2018.00898

Watters, C., Burton, T., Kirui, D.K. and Millenbaugh, N.J., 2016. Enzymatic degradation of in vitro Staphylococcus aureus biofilms supplemented with human plasma. Infection and Drug Resistance 9: 71–78. 10.2147/IDR.S103101

Yeganeh, M., Hosseini, H., Mehrabian, S., Torbati, E.S. and Zamir, S.M., 2017. Antibiofilm effects of Lactobacilli against ciprofloxacin-resistant uropathogenic Escherichia coli strains in pasteurized milk. Applied Food Biotechnology 4: 241–250. 10.22037/afb.v4i3.15014