Novel Clean Label Approach: Assessment of Antimicrobial Potential of Combined Use of Aromatic and Medicinal Plants and Bacteriocin against Salmonella enterica, Bacillus cereus and Staphylococcus aureus in Model Sausages
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Abstract
The growing demand for clean-label products has intensified research into natural antimicrobial agents for food preservation. Essential oils (EOs) and crude extracts (CEs) from aromatic and medicinal plants (AMPs), along with bacteriocins, offer promising alternatives to synthetic preservatives. This study evaluated the efficacy of EO or CE from nine AMPs and their association with bacteriocin OS1 against Salmonella enterica, Bacillus cereus, and Staphylococcus aureus in a refrigerated sausage model. Sausage batches were treated with EOs of rosemary, thyme, clove, nutmeg, laurel, garlic, blue gum, and CEs of saffron and safflower, and/or bacteriocin, and stored for 15 days at 8°C. The data were analyzed using Spearman correlation analysis, variance analysis, and the Mann-Whitney test. Based on statistical analysis, bacteriocin OS1 alone (at 200 AU/g) minimally affected S. enterica counts, with 0.03-0.23 Log CFU/g reduction, and moderately reduced B. cereus (0.31-0.54 Log CFU/g) over the storage period. Notably, S. aureus displayed no susceptibility to OS1. The three populations demonstrated significant and variable sensitivity to the tested AMPs. Rosemary-EO showed the highest reduction in S. enterica and B. cereus, while S. aureus was most susceptible to garlic-EO. The combination of rosemary-EO and OS1, as well as laurel-EO and OS1, showed a synergistic effect, significantly reducing B. cereus and S. enterica. Furthermore, S. aureus exhibited greater resistance to AMPs, whether alone or combined with bacteriocin. These findings highlight species-dependent interactions between certain AMP extracts and bacteriocins validated within a sausage matrix, providing a natural food preservation approach aligned with consumer demand for clean-label products.
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Al-Hazmi NE. Antibacterial activity and mechanism of action of crude aqueous extracts from agricultural waste against foodborne pathogenic bacteria. Trop J. Nat Prod Res. 2022; 6(6): 906-909. Doi: 10.26538/tjnpr/v6i6.14
Al-Shaheeb ZA, Thabit ZA, Oraibi AG, Baioumy AA, Abedelmaksoud TG. Salmonella enterica species isolated from local foodstuff and patients suffering from foodborne illness: Surveillance, antimicrobial resistance and molecular detection. Theory Pract Meat Process. 2023; 8(2): 112-123. Doi: 10.21323/2414-438X-2023-8-2-112-123
Algammal AM, Eid HM, Alghamdi S, Ghabban H, Alatawy R, Almanzalawi EA, Alqahtani TM, Elfouly SG, Mohammed GM, Hetta HF, El-Tarabili RM. Meat and meat products as potential sources of emerging MDR Bacillus cereus: groEL gene sequencing, toxigenic and antimicrobial resistance. BMC Microbiol. 2024; 24(50): 1-13 Doi: 10.1186/s12866-024-03204-9
Karbowiak M, Szymański P, Zielińska D. Synergistic effect of combination of various microbial hurdles in the biopreservation of meat and meat products-systematic review. Foods. 2023; 12(7): 1430. Doi: 10.3390/ foods12071430
Collier SA, Deng L, Adam EA, Benedict KM, Beshearse EM, Blackstock AJ, Beach MJ. Estimate of burden and direct healthcare cost of infectious waterborne disease in the United States. Emerg Infect Dis. 2021; 27(1): 140-149. Doi: 10.3201/eid2701.190676.
Scallan E, Hoekstra RM, Mahon BE, Jones TF, Griffin PM. An assessment of the human health impact of seven leading foodborne pathogens in the United States using disability adjusted life years. Epidemiol Infect. 2015; 143(13): 2795–2804. Doi: 10.1017/S0950268814003185
EFSA and ECDC (European Food Safety Authority and European Centre for Disease Prevention and Control). The European Union One Health 2022 Zoonoses Report. EFSA J. 2023; 21(12): e8442. Doi: 10.2903/j.efsa.2023.8442
Ehuwa O, Jaiswal AK, Jaiswal S. Salmonella, food safety and food handling practices. Foods. 2021; 10(5): 907. Doi: 10.3390/foods10050907
Mkangara M. Prevention and control of human Salmonella enterica infections: an implication in food safety. Int. J. Food Sci. 2023; 2023: 8899596. Doi: 10.1155/2023/8899596
Hilliard NJ, Schelonka RL, Waites KB. Bacillus cereus bacteremia in a preterm neonate. J. Clin Microbiol. 2003; 41(7): 3441–3444. Doi: 10.1128/JCM.41.7.3441-3444.2003
Fiedler G, Schneider C, Igbinosa EO, Kabisch J, Brinks E, Becker B, Stoll DA, Cho GS, Huch M, Franz CMAP. Antibiotics resistance and toxin profiles of Bacillus cereus-group isolates from fresh vegetables from German retail markets. BMC Microbiol. 2019; 19(1): 250. Doi: 10.1186/s12866-019-1632-221
Liang T, Liang Z, Wu S, Ding Y, Wu Q, Gu B. Global prevalence of Staphylococcus aureus in food products and its relationship with the occurrence and development of diabetes mellitus. Med Adv. 2023; 1(1): 53-78. Doi: 10.1002/med4.6
Deak T. Thermal treatment. In: Motarjemi Y, Lelieveld H (Eds.). Food Safety Management. Academic Press; 2014. 423-442 p. Doi: 10.1016/B978-0-12-381504-0.00017-2
Kaveh S, Hashemi SMB, Abedi E, Amiri MJ, Conte FL. Bio-preservation of meat and fermented meat products by lactic acid bacteria strains and their antibacterial metabolites. Sustainability. 2023; 15(13): 10154. Doi: 10.3390/su151310154
Ananou S, Lotfi S, Azdad O, Nzoyikorera N. Production, recovery and characterization of an enterocin with anti-listerial activity produced by Enterococcus hirae OS1. Appl Food Biotechnol. 2020; 7(2): 103-114. Doi: 10.22037/afb.v7i2.27582
Ananou S, Bouraqqadi M, Zouhri N, El Kinany S, Manni L. Control of Listeria monocytogenes in a fresh cheese using aromatic and medicinal plants and enterocin: a comparative study. Lett Appl Microbiol. 2023; 76(7). Doi: 10.1093/lambio/ovad076
Oussama BK, Fatima S, Djilali B, Rym B. The combined effect of Rosmarinus officinalis L essential oil and bacteriocin BacLP01 from Lactobacillus plantarum against Bacillus subtilis ATCC11778. Trop J Nat Prod Res. 2023; 7(3): 2551-2557. Doi: 10.26538/tjnpr/v7i3.14
Bukvicki D, D’Alessandro M, Rossi S, Siroli L, Gottardi D, Braschi G, Patrignani F, Lanciotti R. Essential oils and their combination with lactic acid bacteria and bacteriocins to improve the safety and shelf life of foods: a review. Foods. 2023; 12(17): 3288. Doi: 10.3390/foods12173288
Ananou S, Maqueda M, Martínez-Bueno M, Gálvez A, Valdivia E. Control of Staphylococcus aureus in sausages by enterocin AS-48. Meat Sci. 2005; 71(3): 549–556. Doi: 10.1016/j.meatsci.2005.04.039
Saraiva C, Silva AC, García-Díez J, cenci-Goga B, Grispoldi L, Silva AF, Almeida JM. Antimicrobial activity of Myrtus communis L. and Rosmarinus officinalis L. essential oils against Listeria monocytogenes in cheese. Foods. 2021; 10(5): 1106. Doi: 10.3390/foods10051106
Kasimin M E, Shamsuddin S, Molujin AM, Sabullah MK, Gansau J A, Jawan R. Enterocin: promising biopreservative produced by Enterococcus sp. Microorganisms. 2022; 10(4): 684. Doi: 10.3390/microorganisms10040684
Rashid M, Sharma S, Kaur A, Kaur A, Kaur S. Biopreservative efficacy of Enterococcus faecium-immobilised film and its enterocin against Salmonella enterica. AMB Express. 2023; 13(11). Doi: 10.1186/s13568-023-01516-z
Sharma K, Kaur S, Singh R, Kumar N. Classification and mechanism of bacteriocin induced cell death: a review. J. Microbiol Biotechnol Food Sci. 2021; 11(3): e3733. Doi: 10.15414/jmbfs.3733
Kuleaşan H, Çakmakçı ML. Effect of reuterin, produced by Lactobacillus reuteri on the surface of sausages to inhibit the growth of Listeria monocytogenes and Salmonella spp. Nahrung. 2002; 46: 408-410. Doi: 10.1002/1521-3803(20021101)46:6<408::AID-FOOD408>3.0.CO;2-T
Jofré A, Garriga M, Aymerich T. Inhibition of Salmonella sp. Listeria monocytogenes and Staphylococcus aureus in cooked ham by combining antimicrobials, high hydrostatic pressure, and refrigeration. Meat Sci. 2008; 78(1–2): 53-59. Doi: 10.1016/j.meatsci.2007.06.015.
Ananou S, Garriga M, Jofré A, Aymerich T, Gálvez A, Maqueda M, Martínez-Bueno M, Valdivia E. Combined effect of enterocin AS-48 and high hydrostatic pressure to control food-borne pathogens inoculated in low acid fermented sausages. Meat Sci. 2010; 84(4): 594-600. Doi: 10.1016/j.meatsci.2009.10.017
Chakchouk-Mtibaa A, Slim S, Ktari N, Sellem I, Najah S, Karray-Rebai I, Mellouli L. Biopreservative efficacy of bacteriocin BacFL31 in raw ground turkey meat in terms of microbiological, physicochemical, and sensory qualities. Biocontrol Sci. 2017; 22: 67-77. Doi: 10.4265/bio.22.67.
Chakchouk-Mtibaa A, Elleuch L, Smaoui S, Najah S, Sellem I, Abdelkafi S, Mellouli L. An antilisterial bacteriocin BacFL31 produced by Enterococcus faecium FL31 with a novel structure containing hydroxyproline residues. Anaerobe. 2014; 27: 1–6. Doi: 10.1016/j.anaerobe.2014.02.002.
Pérez-Ramos A, Madi-Moussa D, Coucheney F, Drider D. Current knowledge of the mode of action and immunity mechanisms of LAB-bacteriocins. Microorganisms. 2021; 9: 2107. Doi : 10.3390/microorganisms9102107
Ananou S, Maqueda M, Martínez-Bueno M, Valdivia E. Biopreservation, an ecological approach to improve the safety and shelf-life of foods. In: Méndez Vilas A (Eds.). Communicating Current Research and Educational Topics and Trends in Applied Microbiology. Badajoz, Spain: Formatex. 2007; 475-486p.
Da Costa RJ, Voloski FLS, Mondadori RG, Duval EH, Fiorentini ÂM. Preservation of meat products with bacteriocins produced by lactic acid bacteria isolated from meat. J. Food Qual. 2019; 1: 1-12. Doi: 10.1155/2019/4726510
Bošković I, Đukić D, Mandić L, Mašković P, Govedarica-Lučić A. Antioxidant and cytotoxic potential of selected plant species of the Boraginaceae family. Agric For. 2021; 67 (2): 53-61. Doi: 10.17707/AgricultForest.67.2.04
García-Díez J, Alheiro J, Pinto AL, Soares L, Falco V, Fraqueza MJ, Patarata L. Behaviour of food-borne pathogens on dry cured sausage manufactured with herbs and spices essential oils and their sensorial acceptability. Food Control. 2016; 59: 262-270. Doi: 10.1016/j.foodcont.2015.05.027.
Stojanović-Radić Z, Pejčić M, Joković N, Jokanović M, Ivić M, Šojić B, Škaljac S, Stojanović P, Mihajilov-Krstev T. Inhibition of Salmonella enteritidis growth and storage stability in chicken meat treated with basil and rosemary essential oils alone or in combination. Food Control. 2018; 90: 332-343. Doi: 10.1016/j.foodcont.2018.03.013
Luna-Guevara JJ, Rivera-Hernández M, Arenas-Hernández MMP, Luna-Guevara ML. Effect of essential oils of oregano (Origanum vulgare), thyme (Thymus vulgaris),orange (Citrus sinensis var. Valencia) in the vapor phase on the antimicrobial and sensory properties of a meat emulsion inoculated with Salmonella enterica. Food Res. 2021; 5: 306-312. Doi: 10.26656/fr.2017.5(1).488
Hyldgaard M, Mygind T, Meyer RL. Essential oils in food preservation: Mode of action, synergies, and interactions with food matrix components. Front Microbiol. 2012; 3(12). Doi: 10.3389/fmicb.2012.00012
Mercanoglu Taban B, Stavropoulou E, Kretli Winkelströter L, Bezirtzoglou E. Value-added effects of using aromatic plants in foods and human therapy. Food Sci Technol. 2022; 42. Doi: 10.1590/fst.43121
D’Aquila P, Paparazzo E, Crudo M, Bonacci S, Procopio A, Passarino G, Bellizzi D. Antibacterial activity and epigenetic remodeling of essential oils from Calabrian aromatic plants. J. Nutr. 2022; 14(2): 391. Doi: 10.3390/nu14020391
Zheng L, Guo H, Zhu M, Xie L, Jin J, Korma SA, Jin Q, Wang X, Cacciotti I. Intrinsic properties and extrinsic factors of food matrix system affecting the effectiveness of essential oils in foods: a comprehensive review. Crit Rev Food Sci Nutr. 2023; 64(21): 7363–7396. Doi: 10.1080/10408398.2023.2184767
Liao W, Badri W, Dumas E, Ghnimi S, Elaissari A, Saurel R, Gharsallaoui A. Nanoencapsulation of essential oils as natural food antimicrobial agents: an overview. Appl Sci. 2021; 11(13): 5778. Doi: 10.3390/app11135778
Rattanachaikunsopon P, Phumkhachorn P. Synergistic antimicrobial effect of nisin and p-cymene on Salmonella enterica serovar Typhi in vitro and on ready-to-eat food. Biosci Biotechnol Biochem. 2010; 74(3): 520–524. Doi: 10.1271/bbb.90708
Lee NK, Kim HW, Lee JY, Ahn DU, Kim CJ, Paik HD. Antimicrobial Effect of nisin against Bacillus cereus in beef jerky during storage. Korean J Food Sci Anim Resour. 2015; 35(2): 272–276. Doi: 10.5851/kosfa.2015.35.2.272
Enan G. Inhibition of Bacillus cereus ATCC 14579 by plantaricin UG1 in vitro and in food. Nahrung. 2000; 44: 364-367. Doi: 10.1002/1521-3803(20001001)44:5<364::AID-FOOD364>3.0.CO;2-0
Haraz S, Edris AB, Arab W, Lela R. Effect of thyme oil and nisin as antimicrobial in Bacillus cereus in chicken fillet butcher shops in Tanta city. Benha. Vet. Med. J. 2022; 43(1): 114-117. Doi: 10.21608/bvmj.2022.150128.1557
Jayaweera TSP, Jayasinghe JMCS, Madushanka DNN, Yasawathie DG, Ruwandeepika HAD. Assessment of the inhibitory effect of nisin (E234) on Salmonella typhimurium and Bacillus subtilis in chicken sausage. Asian Food Sci J. 2018; 2(3): 1–11. Doi: 10.9734/AFSJ/2018/41374
Salem A, Mohamed E, Selim E. Antimicrobial effect of some natural oils on Bacillus cereus in minced beef. Benha. Vet. Med. J. 2018; 34(2): 149-156. Doi: 10.21608/bvmj.2018.29424
Turgis M, Vu K, Dupont C, Lacroix M. Combined antimicrobial effect of essential oils and bacteriocins against foodborne pathogens and food spoilage bacteria. Food Res Int. 2012; 48(2): 696-702. Doi: 10.1016/j.foodres.2012.06.016
Ibrahim H, El Sabagh R, Abou El-Roos N, Abd El Fattah H. Antimicrobial effect of some essential oils on Staphylococcus aureus in minced meat. Benha. Vet. Med. J. 2016; 30(1): 183-191. Doi: 10.21608/bvmj.2016.31362
Amin A. Screening of antibacterial activity of cinnamon, clove and rosemary essential oils against common food borne pathogens in minced beef. Benha. Vet. Med. J. 2013; 25(2):151-164.
Pesavento G, Calonico C, Bilia AR, Barnabei M, Calesini F, Addona R, Mencarelli L, Carmagnini L, Di Martino MC, Lo Nostro A. Antibacterial activity of Oregano, Rosmarinus and Thymus essential oils against Staphylococcus aureus and Listeria monocytogenes in beef meatballs. Food Control. 2015; 54: 188-199; Doi: 10.1016/j.foodcont.2015.01.045
Ananou S, Baños A, Maqueda M, Martínez-Bueno M, Gálvez A, Valdivia E. Effect of combined physico-chemical treatments based on enterocin AS-48 on the control of Listeria monocytogenes and Staphylococcus aureus in a model cooked ham. Food Control. 2010; 21: 478–486. Doi: 10.1016/j.foodcont.2009.07.010.
Bastos MdoC, Coelho ML, Santos OC. Resistance to bacteriocins produced by Gram-positive bacteria. Microbiology. 2015; 161(4): 683-700. Doi: 10.1099/mic.0.082289-0
Kawada-Matsuo M, Le MN, Komatsuzawa H. Antibacterial peptides resistance in Staphylococcus aureus: various mechanisms and the association with pathogenicity. Genes. 2021; 12 (10): 1527. Doi: 10.3390/genes12101527
Gradisteanu Pircalabioru G, Popa LI, Marutescu L, Gheorghe I, Popa M, Czobor Barbu I, Cristescu R, Chifiriuc MC. Bacteriocins in the era of antibiotic resistance: rising to the challenge. Pharmaceutics. 2021; 13(2): 196. Doi : 10.3390/pharmaceutics13020196
Hiron A, Falord M, Valle J, De barbouillé M, Msadek T. Bacitracin and nisin resistance in Staphylococcus aureus: a novel pathway involving the BraS/BraR two-component system (SA2417/SA2418) and both the BraD/BraE and VraD/ VraE ABC transporters. Mol Microbiol. 2011; 81: 602–622. Doi: 10.1111/j.1365-2958.2011.07735.x