Main Article Content
Biofilms are a significant concern in the food industry because of their potential to enhance bacterial survival and cause foodborne outbreaks. Escherichia coli (E. coli) is among the leading pathogens responsible for foodborne outbreaks and this can be attributed to its ability to form biofilms in food containers and food preparatory surfaces. The purpose of this study was to investigate the antibacterial and antibiofilm properties of garlic, ginger and mint and their potential to inhibit E.coli and biofilm formation. Disc diffusion assays and 96-well plate crystal violet-based methods were used to achieve these objectives. The plant extracts were diluted from 1 mg/ml to 0.1 mg/ml and incubated 25°C and 37°C to investigate the antimicrobial and antibiofilm effects on E. coli. The findings of this study showed that low temperatures induced the formation of E. coli biofilms and all tested extracts contain a broad spectrum of antibacterial and antibiofilm properties. This study provided new insights on the combined antimicrobial and antibiofilm properties of garlic, ginger and mint against planktonic cells and biofilms of E. coli MG 1655 and highlight the potential use of these extracts in the food industry to prevent biofilm formation by E. coli.
Agarwal V, Lal P, Pruthi V. Prevention of Candida albicans biofilm by plant oils. Mycopathologia, 2008, 165(1), 13-19. https://doi.org/10.1007/s11046-007-9077-9
Al-Sum BA, Al-Arfaj AA. Antimicrobial activity of the aqueous extract of mint plant. Science Journal of Clinical Medicine, 2013, 2(3), 110-113. https://doi.org/10.11648/j.sjcm.20130203.19
Ankri S, Mirelman D. Antimicrobial properties of allicin from garlic. Microbes and Infection, 1999, 1(2), 125-129. https://doi.org/10.1016/S1286-4579(99)80003-3
Bakht J, Muhammad T, Ali H, Islam A, Shafi M. Effect of different solvent extracted sample of Allium sativum (Linn) on bacteria and fungi. African Journal of Biotechnology, 2011, 10(31), 5910-5915. https://doi.org/10.5897/AJB11.232
Bakri I, Douglas C. Inhibitory effect of garlic extract on oral bacteria. Archives of Oral Biology, 2005, 50(7), 645-651. https://doi.org/10.1016/j.archoralbio.2004.12.002
Barnhart MM, Chapman MR. Curli biogenesis and function. Annual Review of Microbiology, 2006, 60, 131-147. https://doi.org/10.1146/annurev.micro.60.080805.142106
Bayer A, Kirby W, Sherris J, Turck M. Antibiotic susceptibility testing by a standardized single disc method. American Journal of Clinical Pathology, 1966, 45(4), 493-496. https://doi.org/10.1093/ajcp/45.4_ts.493
Bazargani MM, Rohloff J. Antibiofilm activity of essential oils and plant extracts against Staphylococcus aureus and Escherichia coli biofilms. Food Control, 2016, 61, 156-164. https://doi.org/10.1016/j.foodcont.2015.09.036
Block E. The chemistry of garlic and onions. Scientific American, 1985, 252(3), 114-121. https://doi.org/10.1038/scientificamerican0385-114
Castonguay M-H, Van der Schaaf S, Koester W, Krooneman J, Van der Meer W, Harmsen H, Landini P. Biofilm formation by Escherichia coli is stimulated by synergistic interactions and co-adhesion mechanisms with adherence-proficient bacteria. Research in Microbiology, 2006, 157(5), 471-478. https://doi.org/10.1016/j.resmic.2005.10.003
Cavallito CJ, Bailey JH. Allicin, the antibacterial principle of Allium sativum. I. Isolation, physical properties and antibacterial action. Journal of the American Chemical Society, 1944, 66(11), 1950-1951. https://doi.org/10.1021/ja01239a048
Ceylan O, Ugur A, Sarac N, Sahin MD. The antimicrobial and antibiofilm activities of Mentha x piperita L. essential oil. Journal of BioScience & Biotechnology, 2014. http://www.jbb.uni-plovdiv.bg/documents/27807/728057/SE-2014-23-27.pdf
Chaieb K, Kouidhi B, Jrah H, Mahdouani K, Bakhrouf A. Antibacterial activity of Thymoquinone, an active principle of Nigella sativa and its potency to prevent bacterial biofilm formation. BMC Complementary and Alternative Medicine, 2011, 11(1), 1-6. http://www.biomedcentral.com/1472-6882/11/29
Cos P, Tote K, Horemans T, Maes L. Biofilms: an extra hurdle for effective antimicrobial therapy. Current Pharmaceutical Design, 2010, 16(20), 2279-2295. https://doi.org/10.2174/138161210791792868
Donlan RM. Biofilms: microbial life on surfaces. Emerging Infectious Diseases, 2002, 8(9), 881. https://doi.org/10.3201/eid0809.020063
Ekwenye U, Elegalam N. Antibacterial activity of ginger (Zingiber officinale) roscoe and garlic (Allium sativum) extracts on Escherichia coli and Salmonella typhi. 2005. http://docsdrive.com/pdfs/medwelljournals/ijmmas/2005/411-417.pdf
Galie S, García-Gutiérrez C, Miguélez EM, Villar CJ, Lombó F. Biofilms in the food industry: health aspects and control methods. Frontiers of Microbiology, 2018, 9:898. https://doi.org/10.3389/fmicb.2018.00898
Gull I, Saeed M, Shaukat H, Aslam SM, Samra ZQ, Athar AM. Inhibitory effect of Allium sativum and Zingiber officinale extracts on clinically important drug resistant pathogenic bacteria. Annals of Clinical Microbiology and Antimicrobials, 2012, 11(1), 1-6. https://doi.org/10.1007/s002530100722
Harris J, Cottrell S, Plummer S, Lloyd D. Antimicrobial properties of Allium sativum (garlic). Applied Microbiology and Biotechnology, 2001, 57(3), 282-286. https://doi.org/10.1007/s002530100722
Iwalokun B, Ogunledun A, Ogbolu D, Bamiro S, Jimi-Omojola J. In vitro antimicrobial properties of aqueous garlic extract against multidrug-resistant bacteria and Candida species from Nigeria. Journal of Medicinal Food, 2004, 7(3), 327-333. http://www.sld.cu/galerias/pdf/sitios/mednat/in_vitro_antimicrobial_properties_of_aqueous_garlic_extract_against_multidrug-resistant_bacteria.pdf
Jang H-J, Lee H-J, Yoon D-K, Ji D-S, Kim J-H, Lee C-H. Antioxidant and antimicrobial activities of fresh garlic and aged garlic by-products extracted with different solvents. Food Science Biotechnology, 2018, 27(1), 219-225. https://doi.org/10.1007/s10068-017-0246-4
John N.R, Gala V.C, Sawant C.S. Inhibitory effects of plant extracts on multi-species dental biofilm formation in vitro. International Journal of Pharmacy and Biological Science, 2013, 4(2), 487-495.
Kwieciński J, Eick S, Wójcik K. Effects of tea tree (Melaleuca alternifolia) oil on Staphylococcus aureus in biofilms and stationary growth phase. International Journal of Antimicrobial Agents, 2009, 33(4), 343-347. https://doi.org/10.1016/j.ijantimicag.2008.08.028
Lee J-H, Cho HS, Joo SW, Chandra Regmi S, Kim J-A, Ryu C-M, Ryu SY, Cho MH, Lee J. Diverse plant extracts and trans-resveratrol inhibit biofilm formation and swarming of Escherichia coli O157: H7. Biofouling, 2013, 29(10), 1189-1203. https://doi.org/10.1007/s10068-017-0246-4
Liu C, Yang X, Yao Y, Huang W, Sun W, Ma Y. Determination of antioxidant activity in garlic (Allium sativum) extracts subjected to boiling process in vitro. Journal of Food and Nutrition Research, 2014, 2(7), 383-387. https://doi.org/10.12691/jfnr-2-7-9
Mah T-FC, O'Toole GA. Mechanisms of biofilm resistance to antimicrobial agents. Trends in Microbiology, 2001, 9(1), 34-39. https://doi.org/10.1016/S0966-842X(00)01913-2
Malu S, Obochi G, Tawo E, Nyong B. Antibacterial activity and medicinal properties of ginger (Zingiber officinale). Global Journal of Pure and Applied Sciences, 2009, 15(3-4). https://doi.org/10.4314/gjpas.v15i3-4.48561
Mendonça RCS, Morelli AMF, Pereira JAM, de Carvalho MM, de Souza NL. Prediction of Escherichia coli O157: H7 adhesion and potential to form biofilm under experimental conditions. Food Control, 2012, 23(2), 389-396. https://doi.org/10.1016/j.foodcont.2011.08.004
Modarresi-Chahardehi A, Ibrahim D, Fariza-Sulaiman S, Mousavi L. Screening antimicrobial activity of various extracts of Urtica dioica. Revista de Biologia Tropical, 2012, 60(4), 1567-1576. https://doi.org/10.1016/j.foodcont.2011.08.004
Narisawa N, Furukawa S, Ogihara H, Yamasaki M. Estimation of the biofilm formation of Escherichia coli K-12 by the cell number. Journal of Bioscience and Bioengineering, 2005, 99(1), 78-80.
Natta L, Orapin K, Krittika N, Pantip B. Essential oil from five Zingiberaceae for anti food-borne bacteria. International Food Research Journal, 2008, 15(3), 337-346. https://doi.org/10.1263/jbb.99.78
Nikolić M, Vasić S, Đurđević J, Stefanović O, Čomić L. Antibacterial and anti-biofilm activity of ginger (Zingiber officinale (Roscoe)) ethanolic extract. Kragujevac Journal of Science, 2014(36), 129-136. https://doi.org/10.5937/kgjsci1436129n
Nostro A, Guerrini A, Marino A, Tacchini M, Di Giulio M, Grandini A, Akin M, Cellini L, Bisignano G, Saraçoğlu HT. In vitro activity of plant extracts against biofilm-producing food-related bacteria. International Journal of Food Microbiology, 2016, 238, 33-39. https://doi.org/10.1016/j.ijfoodmicro.2016.08.024
O'Gara EA, Hill DJ, Maslin DJ. Activities of garlic oil, garlic powder, and their diallyl constituents against Helicobacter pylori. Applied Environmental Microbiology, 2000, 66(5), 2269-2273. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC101489/pdf/am002269.pdf
Ryu J-H, Beuchat LR. Biofilm formation by Escherichia coli O157: H7 on stainless steel: effect of exopolysaccharide and curli production on its resistance to chlorine. Applied Environmental Microbiology, 2005, 71(1), 247-254. https://doi.org/10.1128/AEM.71.1.247-254.2005
Ryu J-H, Kim H, Beuchat LR. Attachment and biofilm formation by Escherichia coli O157: H7 on stainless steel as influenced by exopolysaccharide production, nutrient availability, and temperature. Journal Food Protection, 2004, 67(10), 2123-2131.
Sandasi M, Leonard C, Viljoen A. The effect of five common essential oil components on Listeria monocytogenes biofilms. Food Control, 2008, 19(11), 1070-1075. https://doi.org/10.1016/j.foodcont.2007.11.006
Sandasi M, Leonard C, Viljoen A. The in vitro antibiofilm activity of selected culinary herbs and medicinal plants against Listeria monocytogenes. Lett Applied Microbiology, 2010, 50(1), 30-35. https://doi.org/10.1111/j.1472-765X.2009.02747.x
Sarker SD, Nahar L, Kumarasamy Y. Microtitre plate-based antibacterial assay incorporating resazurin as an indicator of cell growth, and its application in the in vitro antibacterial screening of phytochemicals. Methods, 2007, 42(4):321-324. https://doi.org/10.1016/j.ymeth.2007.01.006
Sebiomo A, Awofodu A, Awosanya A, Awotona F, Ajayi A. Comparative studies of antibacterial effect of some antibiotics and ginger (Zingiber officinale) on two pathogenic bacteria. Journal of Microbiology and Antimicrobials, 2011, 3(1), 18-22. https://academicjournals.org/journal/JMA/article-abstract/0864D829693
Shi X, Zhu X. Biofilm formation and food safety in food industries. Trends Food Science Technology, 2009, 20(9), 407-413. https://doi.org/10.1016/j.tifs.2009.01.054
Shilpa S, Thomas R. Antimicrobial properties of Allium sativum (garlic) against commonly encountered gastrointestinal pathogens. Advances in Plant Sciences, 2010, 23(2):387-389.
Silhan J, Corfitzen CB, Albrechtsen H-J. Effect of temperature and pipe material on biofilm formation and survival of Escherichia coli in used drinking water pipes: a laboratory-based study. Water Science and Technology, 2006, 54(3), 49-56.
Simões M, Simões LC, Vieira MJ. A review of current and emergent biofilm control strategies. LWT-Food Science Technology, 2010, 43(4), 573-583. https://doi.org/10.1016/j.lwt.2009.12.008
Singh R, Shushni MA, Belkheir A. Antibacterial and antioxidant activities of Mentha piperita L. Arabian Journal of Chemistry, 2015, 8(3), 322-328. https://doi.org/10.1016/j.arabjc.2011.01.019
Sivropoulou A, Kokkini S, Lanaras T, Arsenakis M. Antimicrobial activity of mint essential oils. Journal of Agriculture Food Chemistry, 1995, 43(9), 2384-2388. Retrieved from: https://pubs.acs.org/sharingguidelines
Szabó E, Skedsmo A, Sonnevend A, Al-Dhaheri K, Emödy L, Usmani A, Pal T. Curli expression of enterotoxigenic Escherichia coli. Folia Microbiology, 2005, 50(1), 40. https://doi.org/10.1007/BF02931292
Trachoo N. Biofilms and the food industry. Biofilms, 2003, 25(6), 808.
Valeriano C, De Oliveira TLC, De Carvalho SM, das Graças Cardoso M, Alves E, Piccoli RH. The sanitizing action of essential oil-based solutions against Salmonella enterica serotype Enteritidis S64 biofilm formation on AISI 304 stainless steel. Food Control, 2012, 25(2), 673-677. https://doi.org/10.1099/mic.0.026419-0
Van Houdt R, Michiels CW. Role of bacterial cell surface structures in Escherichia coli biofilm formation. Research in Microbiology, 2005, 156(5-6), 626-633. https://doi.org/10.1016/j.resmic.2005.02.005
Vejborg RM, Klemm P. Cellular chain formation in Escherichia coli biofilms. Microbiology, 2009, 155(5), 1407-1417. https://doi.org/10.1099/mic.0.026419-0
Villanueva VD, Font J, Schwartz T, Romani AM. Biofilm formation at warming temperature, acceleration of microbial colonization and microbial interactive effects. Biofouling, 2011, 27(1), 59-71. https://doi.org/10.1080/08927014.2010.538841
White-Ziegler CA, Um S, Perez NM, Berns AL, Malhowski AJ, Young S. Low temperature (23 C) increases expression of biofilm-, cold-shock-and RpoS-dependent genes in Escherichia coli K-12. Microbiology, 2008, 154(1), 148-166. https://doi.org/10.1099/mic.0.2007/012021-0
WHO Estimates of the Burden of foodborne disease http://www.who.int/foodsafety/areas_work/foodborne-diseases/ferg/en/
Wolde T, Kuma H, Trueha K, Yabeker A. Anti-bacterial activity of garlic extract against human pathogenic bacteria. Journal of Pharmacovigilance, 2018, 6(1), 1-5. https://doi.org/10.4172/2329-6887.1000253
This work is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License.
Copyright Licensing Agency
Institutions based in the EU with a valid photocopying and/or digital license with the Copyright Licensing Agency may copy excerpts from books and journals published by the Academic Publishing House of UFT Plovdiv under the terms of their license.
Copyright Clearance Center
Institutions based in the US with a valid photocopying and/or digital license with the Copyright Clearance Center may copy excerpts from books and journals published by the Academic Publishing House of UFT Plovdiv under the terms of their license.
Other Territories: Please contact your local reproduction rights organization.
If you have any questions about the permitted uses of a specific article, please contact us.
Permissions Department of Academic Publishing House of UFT Plovdiv
Plovdiv 4002, 26 Maritsa Blvd., Bulgaria
Tel.: +359 (32) 603-802
Fax: +359 (32) 644-102