Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Utilization of Piper betle L. Extract for Inactivating Foodborne Bacterial Biofilms on Pitted and Smooth Stainless Steel Surfaces

  • Songsirin Ruengvisesh (Department of Microbiology, Faculty of Science, King Mongkut's University of Technology Thonburi (KMUTT)) ;
  • Pattarapong Wenbap (Department of Microbiology, Faculty of Science, King Mongkut's University of Technology Thonburi (KMUTT)) ;
  • Peetitas Damrongsaktrakul (Department of Microbiology, Faculty of Science, King Mongkut's University of Technology Thonburi (KMUTT)) ;
  • Suchanya Santiakachai (Department of Microbiology, Faculty of Science, King Mongkut's University of Technology Thonburi (KMUTT)) ;
  • Warisara Kasemsukwimol (Department of Microbiology, Faculty of Science, King Mongkut's University of Technology Thonburi (KMUTT)) ;
  • Sirilak Chitvittaya (Department of Microbiology, Faculty of Science, King Mongkut's University of Technology Thonburi (KMUTT)) ;
  • Yossakorn Painsawat (Department of Microbiology, Faculty of Science, King Mongkut's University of Technology Thonburi (KMUTT)) ;
  • Isaratat Phung-on (Maintenance Technology Center, Institute for Scientific & Technological Research & Services (ISTRS), KMUTT) ;
  • Pravate Tuitemwong (Department of Microbiology, Faculty of Science, King Mongkut's University of Technology Thonburi (KMUTT))
  • Received : 2023.01.02
  • Accepted : 2023.02.14
  • Published : 2023.06.28
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Abstract

Biofilms are a significant concern in the food industry. The utilization of plant-derived compounds to inactivate biofilms on food contact surfaces has not been widely reported. Also, the increasing negative perception of consumers against synthetic sanitizers has encouraged the hunt for natural compounds as alternatives. Therefore, in this study we evaluated the antimicrobial activities of ethanol extracts, acetone extracts, and essential oils (EOs) of seven culinary herbs against Salmonella enterica serotype Typhimurium and Listeria innocua using the broth microdilution assay. Among all tested extracts and EOs, the ethanol extract of Piper betle L. exhibited the most efficient antimicrobial activities. To evaluate the biofilm inactivation effect, S. Typhimurium and L. innocua biofilms on pitted and smooth stainless steel (SS) coupons were exposed to P. betle ethanol extract (12.5 mg/ml), sodium hypochlorite (NaClO; 200 ppm), hydrogen peroxide (HP; 1100 ppm), and benzalkonium chloride (BKC; 400 ppm) for 15 min. Results showed that, for the untreated controls, higher sessile cell counts were observed on pitted SS versus smooth SS coupons. Overall, biofilm inactivation efficacies of the tested sanitizers followed the trend of P. betle extract ≥ BKC > NaClO > HP. The surface condition of SS did not affect the biofilm inactivation effect of each tested sanitizer. The contact angle results revealed P. betle ethanol extract could increase the surface wettability of SS coupons. This research suggests P. betle extract might be utilized as an alternative sanitizer in food processing facilities.

Keywords

Acknowledgement

This research was funded by the Thailand Research Fund (Grant No. MRG6280095). The authors would like to thank Miss Parichatr Aupawan and Mr. Sanong Kinkasorn for their assistance with sample preparation. Also, the authors would like to acknowledge Thai-China Flavors and Fragrances Industry Co., Ltd. and AEC Industrial Services Co., Ltd. for their kind supplies of EO samples and stainless steel coupons, respectively.

References

  1. Centers for Disease Control and Prevention (CDC). 2018. Estimates of Foodborne Illness in the United States. Available from https://www.cdc.gov/foodborneburden/index.html. Accessed Dec. 22, 2022.
  2. Bureau of Epidemiology. 2018. Food Poisoning. Available from http://www.boe.moph.go.th/boedb/surdata/disease.php?dcontent=old&ds=03. Accessed July 1, 2022.
  3. Chmielewski RAN, Frank JF. 2003. Biofilm formation and control in food processing facilities. Compr. Rev. Food Sci. Food Saf. 2: 22-32. https://doi.org/10.1111/j.1541-4337.2003.tb00012.x
  4. Coughlan LM, Cotter PD, Hill C, Alvarez-Ordonez A. 2016. New weapons to fight old enemies: Novel strategies for the (bio)control of bacterial biofilms in the food industry. Front. Microbiol. 7. 1641.
  5. Jadhav S, Shah R, Bhave M, Palombo EA. 2013. Inhibitory activity of yarrow essential oil on Listeria planktonic cells and biofilms. Food Control 29: 125-130. https://doi.org/10.1016/j.foodcont.2012.05.071
  6. Valeriano C, de Oliveira TLC, de Carvalho SM, Cardoso MdG, Alves E, Piccoli RH. 2012. The sanitizing action of essential oil-based solutions against Salmonella enterica serotype Enteritidis S64 biofilm formation on AISI 304 stainless steel. Food Control 25: 673-677. https://doi.org/10.1016/j.foodcont.2011.12.015
  7. Wang H, Wang H, Xing T, Wu N, Xu X, Zhou G. 2016. Removal of Salmonella biofilm formed under meat processing environment by surfactant in combination with bio-enzyme. LWT-Food Sci. Technol. 66: 298-304. https://doi.org/10.1016/j.lwt.2015.10.049
  8. Simoes M, Simoes LC, Vieira MJ. 2010. A review of current and emergent biofilm control strategies. LWT-Food Sci. Technol.43: 573-583. https://doi.org/10.1016/j.lwt.2009.12.008
  9. Corcoran M, Morris D, De Lappe N, O'Connor J, Lalor P, Dockery P, et al. 2014. Commonly used disinfectants fail to eradicate Salmonella enterica biofilms from food contact surface materials. Appl. Environ. Microbiol. 80: 1507-1514. https://doi.org/10.1128/AEM.03109-13
  10. Krolasik J, Zakowska Z, Krepska M, Klimek L. 2010. Resistance of bacterial biofilms formed on stainless steel surface to disinfecting agent. Pol. J. Microbiol. 59: 281-287. https://doi.org/10.33073/pjm-2010-042
  11. Falco I, Verdeguer M, Aznar R, Sanchez G, Randazzo W. 2018. Sanitizing food contact surfaces by the use of essential oils. Innov. Food Sci. Emerg. Technol. 51: 220-228. https://doi.org/10.1016/j.ifset.2018.02.013
  12. Boguslaw P, Kowalski I. 2011. The influence of hypochlorite-based disinfectants on the pitting corrosion of welded joints of 316L stainless steel dairy reactor. Int. J. Electrochem. Sci. 6: 3913 - 3921. https://doi.org/10.1016/S1452-3981(23)18299-X
  13. Schmidt RH, Erickson DJ, Sims S, Wolff P. 2012. Characteristics of food contact surface materials: Stainless steel. Food Prot. Trends. 32: 574-584.
  14. Tantratian S, Srimangkornkaew N, Prakitchaiwattana C, Sanguandeekul R. 2022. Effect of different stainless steel surfaces on the formation and control of Vibrio parahaemolyticus biofilm. LWT 166: 113788.
  15. Mouritz AP. 2012. 21 - Corrosion of aerospace metals, pp. 498-520. In Mouritz AP (ed.), Introduction to Aerospace Materials, 1st Ed. Woodhead Publishing, Cambridge.
  16. Van Houdt R, Michiels CW. 2010. Biofilm formation and the food industry, a focus on the bacterial outer surface. J. Appl. Microbiol. 109: 1117-1131. https://doi.org/10.1111/j.1365-2672.2010.04756.x
  17. Rodrigues JBD, de Carvalho RJ, de Souza NT, Oliveira KD, Franco OL, Schaffner D, et al. 2017. Effects of oregano essential oil and carvacrol on biofilms of Staphylococcus aureus from food-contact surfaces. Food Control 73: 1237-1246. https://doi.org/10.1016/j.foodcont.2016.10.043
  18. Vidacs A, Kerekes E, Rajko R, Petkovits T, Alharbi NS, Khaled JM, et al. 2018. Optimization of essential oil-based natural disinfectants against Listeria monocytogenes and Escherichia coli biofilms formed on polypropylene surfaces. J. Mol. Liq. 255: 257-262. https://doi.org/10.1016/j.molliq.2018.01.179
  19. Bazargani MM, Rohloff J. 2016. Antibiofilm activity of essential oils and plant extracts against Staphylococcus aureus and Escherichia coli biofilms. Food Control 61: 156-164. https://doi.org/10.1016/j.foodcont.2015.09.036
  20. Varposhti M, Abdi Ali A, Mohammadi P, Saboora A. 2013. Effects of extracts and an essential oil from some medicinal plants against biofilm formation of Pseudomonas aeruginosa. J. Med. Microbiol. Infec. Dis. 1: 36-40.
  21. Hu M, Gurtler JB. 2017. Selection of surrogate bacteria for use in food safety challenge studies: A review. J. Food Prot. 80: 1506-1536. https://doi.org/10.4315/0362-028X.JFP-16-536
  22. Sasongko P, Laohankunjit N, Kerdchoechuen O. 2011. Evaluation of physicochemical properties of plant extracts from Persicaria odorata. Agricultural Sci. J. 42: 333-336.
  23. Damrongsaktrakul P, Ruengvisesh S, Rahothan A, Sukhumrat N, Tuitemwong P, Phung-on I. 2021. Removal of Salmonella Typhimurium biofilm from food contact surfaces using Quercus infectoria gall extract in combination with a surfactant. J. Microbiol. Biotechnol. 31: 439-446. https://doi.org/10.4014/jmb.2101.01014
  24. Asaduzzaman MD, Mohammad M, Islam MM. 2011. Effects of concentration of sodium chloride solution on the pitting corrosion behavior of AISI 304L austenitic stainless steel. Chem. Ind. Chem. Eng. Q 17: 477-483. https://doi.org/10.2298/CICEQ110406032A
  25. Yegin Y, Perez-Lewis KL, Liu S, Kerth CR, Cisneros-Zevallos L, Castillo A, et al. 2021. Antimicrobial-loaded polymeric micelles inhibit enteric bacterial pathogens on spinach leaf surfaces during multiple simulated pathogen contamination events. Front. Sustain. Food Syst. 5: 646980.
  26. Zezzi do Valle Gomes M, Nitschke M. 2012. Evaluation of rhamnolipid and surfactin to reduce the adhesion and remove biofilms of individual and mixed cultures of food pathogenic bacteria. Food Control 25: 441-447. https://doi.org/10.1016/j.foodcont.2011.11.025
  27. Tagrida M, Benjakul S. 2021. Betel (Piper betle L.) leaf ethanolic extracts dechlorophyllized using different methods: antioxidant and antibacterial activities, and application for shelf-life extension of Nile tilapia (Oreochromis niloticus) fillets. RSC Advances 11: 17630-17641. https://doi.org/10.1039/D1RA02464G
  28. Boontha S, Taowkaen J, Phakwan T, Worauuaichai T, Kanonnate P, Buranrat B, et al. 2019. Evaluation of antioxidant and anticancer effects of Piper betle L (Piperaceae) leaf extract on MCF-7 cells, and preparation of transdermal patches of the extract. J. Trop. For. Sci. 18: 1265-1272.
  29. Pin K, Luqman Chuah A, Rashih A, Md.Pisar M, Jamaludin F, Vimala S, et al. 2010. Antioxidant and anti-inflammatory activities of extracts of betel leaves (Piper betle) from solvents with different polarities. J. Trop. For. Sci. 22: 448-455.
  30. Zamakshshari N, Ahmed IA, Nasharuddin MNA, Mohd Hashim N, Mustafa MR, Othman R, et al. 2021. Effect of extraction procedure on the yield and biological activities of hydroxychavicol from Piper betle L. leaves. J. Appl. Res. Med. Aromat. Plants. 24: 100320.
  31. Nguyen LTT, Nguyen TT, Nguyen HN, Bui QTP. 2020. Simultaneous determination of active compounds in Piper betle Linn. leaf extract and effect of extracting solvents on bioactivity. Eng. Rep. 2: e12246.
  32. Ngo TV, Scarlett CJ, Bowyer MC, Ngo PD, Vuong QV. 2017. Impact of different extraction solvents on bioactive compounds and antioxidant capacity from the root of Salacia chinensis L. J. Food Qual. 2017: 9305047.
  33. Valle DL, Jr., Cabrera EC, Puzon JJ, Rivera WL. 2016. Antimicrobial activities of methanol, ethanol and supercritical CO2 extracts of Philippine Piper betle L. on clinical isolates of gram positive and gram negative bacteria with transferable multiple drug resistance. PLoS One 11: e0146349.
  34. Arawwawala LD, Arambewela LS, Ratnasooriya WD. 2014. Gastroprotective effect of Piper betle Linn. leaves grown in Sri Lanka. J. Ayurveda. Integr. Med. 5: 38-42. https://doi.org/10.4103/0975-9476.128855
  35. Arambewela LS, Arawwawala LD, Kumaratunga KG, Dissanayake DS, Ratnasooriya WD, Kumarasingha SP. 2011. Investigations on Piper betle grown in Sri Lanka. Phcog. Rev. 5: 159-163. https://doi.org/10.4103/0973-7847.91111
  36. Sengupta K, Mishra AT, Rao MK, Sarma KV, Krishnaraju AV, Trimurtulu G. 2012. Efficacy of an herbal formulation LI10903F containing Dolichos biflorus and Piper betle extracts on weight management. Lipids Health Dis. 11: 176.
  37. Chanudom L, Tangpong J. 2011. Total phenolic content, antioxidant and antimicrobial activities from 13 Thai traditional plants. Wichcha J. NSTRU 30: 1-11.
  38. American Society for Testing and Materials (ASTM). 2018. Standard guide for examination and evaluation of pitting corrosion. ASTM G46-94.
  39. Abrahim NN, Kanthimathi MS, Abdul-Aziz A. 2012. Piper betle shows antioxidant activities, inhibits MCF-7 cell proliferation and increases activities of catalase and superoxide dismutase. BMC Complement. Altern. Med. 12: 220.
  40. Saeloh D, Visutthi M. 2021. Efficacy of Thai plant extracts for antibacterial and anti-biofilm activities against pathogenic bacteria. Antibiotics 10: 1470.
  41. Syahidah A, Saad CR, Hassan MD, Rukayadi Y, Norazian MH, Kamarudin MS. 2017. Phytochemical analysis, identification and quantification of antibacterial active compounds in betel leaves, Piper betle methanolic extract. Pak. J. Biol. Sci. 20: 70-81. https://doi.org/10.3923/pjbs.2017.70.81
  42. Nayaka NMDMW, Sasadara MMV, Sanjaya DA, Yuda PESK, Dewi NLKAA, Cahyaningsih E, et al. 2021. Piper betle (L): Recent review of antibacterial and antifungal properties, safety profiles, and commercial applications. Molecules 26: 2321.
  43. Singh D, Narayanamoorthy S, Gamre S, Majumdar AG, Goswami M, Gami U, et al. 2018. Hydroxychavicol, a key ingredient of Piper betle induces bacterial cell death by DNA damage and inhibition of cell division. Free. Radic. Biol. Med. 120: 62-71. https://doi.org/10.1016/j.freeradbiomed.2018.03.021
  44. Abdallah M, Benoliel C, Drider D, Dhulster P, Chihib N-E. 2014. Biofilm formation and persistence on abiotic surfaces in the context of food and medical environments. Arch. Microbiol. 196: 453-472. https://doi.org/10.1007/s00203-014-0983-1
  45. Lomander A, Schreuders P, Russek-Cohen E, Ali L. 2004. Evaluation of chlorines' impact on biofilms on scratched stainless steel surfaces. Bioresour. Technol. 94: 275-283. https://doi.org/10.1016/j.biortech.2004.01.004
  46. Robbins JB, Fisher CW, Moltz AG, Martin SE. 2005. Elimination of Listeria monocytogenes biofilms by ozone, chlorine, and hydrogen peroxide. J. Food Prot. 68: 494-498. https://doi.org/10.4315/0362-028X-68.3.494
  47. Merchel Piovesan Pereira B, Tagkopoulos I. 2019. Benzalkonium chlorides: uses, regulatory status, and microbial resistance. Appl. Environ. Microbiol. 85: e00377-19.
  48. Kostaki M, Chorianopoulos N, Braxou E, Nychas GJ, Giaouris E. 2012. Differential biofilm formation and chemical disinfection resistance of sessile cells of Listeria monocytogenes strains under monospecies and dual-species (with Salmonella enterica) conditions. Appl. Environ. Microbiol. 78: 2586-2595. https://doi.org/10.1128/AEM.07099-11
  49. Akoachere JF, Tanih NF, Ndip LM, Ndip RN. 2009. Phenotypic characterization of Salmonella typhimurium isolates from food-animals and abattoir drains in Buea, Cameroon. J. Health Popul. Nutr. 27: 612-618.
  50. Nayak DN, Savalia CV, Kalyani IH, Kumar R, Kshirsagar DP. 2015. Isolation, identification, and characterization of Listeria spp. from various animal origin foods. Vet. World 8: 695-701. https://doi.org/10.14202/vetworld.2015.695-701
  51. Kim CY, Ryu G, Park H, Ryu K. 2017. Resistance of Staphylococcus aureus on food contact surfaces with different surface characteristics to chemical sanitizers. J. Food Saf. 37: e12354
  52. Kim H, Moon MJ, Kim CY, Ryu K. 2019. Efficacy of chemical sanitizers against Bacillus cereus on food contact surfaces with scratch and biofilm. Food Sci. Biotechnol. 28: 581-590. https://doi.org/10.1007/s10068-018-0482-2
  53. Caixeta DS, Scarpa TH, Brugnera DF, Freire DO, Alves E, de Abreu LR, et al. 2012. Chemical sanitizers to control biofilms formed by two Pseudomonas species on stainless steel surface. Cienc. Tecnol. Aliment. 32: 142-150. https://doi.org/10.1590/S0101-20612012005000008
  54. Meyer B. 2003. approaches to prevention, removal and killing of biofilms. Int. Biodeterior. Biodegradation 51: 249-253. https://doi.org/10.1016/S0964-8305(03)00047-7
  55. Marques S, Rezende J, Alves L, Silva B, Alves E, Abreu L, et al. 2007. Formation of biofilms by Staphylococcus aureus on stainless steel and glass surfaces and its resistance to some selected chemical sanitizers. Braz. J. Microbiol. 38: 538-543. https://doi.org/10.1590/S1517-83822007000300029
  56. Iniguez-Moreno M, Gutierrez-Lomeli M, Avila-Novoa MG. 2021. Removal of mixed-species biofilms developed on food contact surfaces with a mixture of enzymes and chemical agents. Antibiotics 10: 931.
  57. Dayan J, Mireles K, Massicotte R, Dagher F, Yahia LH. 2016. Clinical and medical investigations effect of disinfectants on wettability and surface tension of metallic and polymeric surfaces found in hospitals. Clin. Med. Invest. 1: 48-55.