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Efficiency of certain vegetables under various storage conditions against the meat-borne Escherichia coli isolates

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Abstract

Given the extension of the shelf lives of various vegetables, individuals store their food for a long period by freezing it with a fast-pact lifstyle. A total of 17 Escherichia coli serovars were recovered from 200 meat samples in Egypt’s Qena governorate. The characterization of the isolates was performed by biochemical and serological tests, antibiotic susceptibility, and detection of virulence genes by PCR. The antibacterial properties of fresh and/or frozen garlic and lemon extract were tested against all E. coli isolates over 6 months, along with their antibiofilm activities. hly, stx1, stx2, and eaeA genes were detected in 12, 4, 3, and 2 serovars, respectively. Although 100% of E. coli isolates were multidrug resistant, they were susceptible to fresh and frozen garlic and lemon extract. Owing to botanical storage for 6 months, a dual decrese was reported in some antibacterial activities of botanical extract and their phytochemical contents. Furthermore, the high-performance liquid chromatographic analysis confirmed that both allicin and citric acid content (in garlic and lemon, respectively) are the most elevated compounds that were diminished following storage time. Fresh and frozen garlic extracts have reduced bacterial biofilm substantially throughout the 6 months of storage, ranging from 19.3 to 45% and 22.3–30.5%, respectively. While fresh and frozen lemon juice significantly decreased the biofilm of E. coli O1:H7 by 52.9 and 26.8% at zero time of storage only. Finally, prolonged storage affects both garlic and lemon extracts’ antimicrobial behavior and encourages fresh intake rather than frozen veggies.

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References

  • Abd El Tawab AA, El-Hofy FI, Maarouf AA, El-Said AA (2015) Bacteriological studies on some food borne bacteria isolated from chicken meat and meat products in Kaliobia Governorate. Benha Vet Med J 29:47–59

    Article  Google Scholar 

  • Adamczak A, Karpiński OM, TM, (2020) Antibacterial activity of some flavonoids and organic acids widely distributed in plants. J Clin Med 9(1):109

    Article  CAS  Google Scholar 

  • Ahmad SR, Gokulakrishnan P, Giriprasad R, Yatoo MA (2015) Fruit-based natural antioxidants in meat and meat products: a review. Crit Rev Food Sci Nutr 55:1503–1513

    Article  CAS  Google Scholar 

  • Alarcón-Flores MI, Romero-González R, Vidal JLM, Frenich AG (2014) Determination of phenolic compounds in artichoke, garlic and spinach by ultra-high-performance liquid chromatography coupled to tandem mass spectrometry. Food Anal Methods 7:2095–2106

    Article  Google Scholar 

  • Al-Chalabi R, Al-Ubaidy A, Al-Ibadi M (2010) Detection of urovirulence genes (eae, E-hly, α-hly) of uropathogenic Escherichia coli by specific PCR. J Biotechnol Res Cent 4:44–54

    Article  Google Scholar 

  • Al-Mutairi MF (2011) The incidence of Enterobacteriaceae causing food poisoning in some meat products. Adv J Food Sci Technol 3(2):116–121

    Google Scholar 

  • Ankri S, Mirelman D (1999) Antimicrobial properties of allicin from garlic. Microbes Infect 1(2):125–129

    Article  CAS  Google Scholar 

  • Aruoma OI, Landes B, Ramful-Baboolall D, Bourdon E, Neergheen-Bhujun V, Wagner KH, Bahorun T (2012) Functional benefits of citrus fruits in the management of diabetes. Prev Med 54:12–16

    Article  Google Scholar 

  • Barbieri R, Coppo E, Marchese A, Daglia M, Sobarzo-Sánchez E, Nabavi SF, Nabavi SM (2017) Phytochemicals for human disease: an update on plant-derived compounds antibacterial activity. Microbiol Res 196:44–68

    Article  CAS  Google Scholar 

  • Bauer AW (1966) Antibiotic susceptibility testing by a standardized single disc method. Am J Clin Pathol 45:149–158

    Article  Google Scholar 

  • Benkeblia N (2000) Phenylalanine ammonia-lyase, peroxidase, pyruvic acid and total phenolics variations in onion bulbs during long-term storage. LWT Food Sci Technol 33(2):112–116

    Article  CAS  Google Scholar 

  • Benkeblia N, Selselet-Attou G (1999) Effects of low temperatures on changes in oligosaccharides, phenolics and peroxidase in inner bud of onion (Allium cepa L.) during break of dormancy. Acta Agric Scand Sect B Plant Soil Sci 49:98–102

    CAS  Google Scholar 

  • Berti PL (2015) Antibacterial activity of Lemon (Citrus limon (L.) Burm.f) juice against porphyromonas gingivalis domonant periodontitis (in vitro). Dissertation, University of Muhamadiyah Surakarta

  • Beutin L, Krause G, Zimmermann S, Kaulfuss S, Gleier K (2004) Characterization of Shiga toxin-producing Escherichia coli strains isolated from human patients in Germany over a 3-year period. J Clin Microbiol 42(3):1099–1108

    Article  Google Scholar 

  • Beya MM, Netzel ME, Sultanbawa Y, Smyth H, Hoffman LC (2021) Plant-based phenolic molecules as natural preservatives in comminuted meats: a review. Antioxidants 10(2):263

    Article  CAS  Google Scholar 

  • Bisi-Johnson MA, Obi CL, Vasaikar SD, Baba KA, Hattori T (2011) Molecular basis of virulence in clinical isolates of Escherichia coli and Salmonella species from a tertiary hospital in the Eastern Cape, South Africa. Gut Pathog 3:9

    Article  Google Scholar 

  • Bitrus AA, Chuanchuen R, Luangtongkum T (2018) Emergence of colistin resistance in extended-spectrum beta lactamase producing Enterobacteriaceae isolated from food animals and its public health implication: a review. J Adv Vet Anim Res 5(1):1–11

    Article  Google Scholar 

  • Borges A, Abreu A, Malheiro J, Saavedra MJ, Simõe M (2013) Biofilm prevention and control by dietary phytochemicals. CECAV-Centro de Ciência Animal e Veterinária

  • Boudries H, Madani K, Touati N, Souagui S, Medouni S, Chibane M (2012) Pulp antioxidant activities, mineral contents and juice nutritional properties of Algerian Clementine Cultivars and Mandarin. Afr J Biotechnol 11(18):4267–4285

    Google Scholar 

  • Brudzinski L, Harrison MA (1998) Influence of incubation conditions on survival and acid tolerance response of Escherichia coli O157:H7 and non-O157:H7 isolates exposed to acetic acid. J Food Prot 61(5):542–546

    Article  CAS  Google Scholar 

  • Bugarel M, Beutin L, Martin A, Gill A, Fach P (2010) Micro-array for the identification of Shiga toxin-producing Escherichia coli (STEC) seropathotypes associated with hemorrhagic colitis and hemolytic uremic syndrome in humans. Int J Food Microbiol 142(3):318–329

    Article  Google Scholar 

  • Cavallito CJ, Bailey JH, Buck JS (1945) The antibacterial principle of Allium sativum. III. Its precursor and “essential oil of garlic.” J Am Chem Soc 67(6):1032–1033

    Article  CAS  Google Scholar 

  • Chandra H, Bishnoi P, Yadav A, Patni B, Mishra AP, Nautiyal AR (2017) Antimicrobial resistance andthe alternative resources with special emphasis on plant-based antimicrobials—a review. Plants 6:16

    Article  CAS  Google Scholar 

  • Chepkemoi S (2016) Handling practices, microbial quality and weight loss of beef in small and medium enterprise butcheries. In: Nairobi and Isiolo Counties, Kenya. Doctoral dissertation, University of Nairobi

  • Chuku EC (2014) Anti-fungal properties of ginger (Zingiber officinale) and garlic (Allium sativum) on smoked cat fish mycoflora. Niger J Mycol 6:48–57

    Google Scholar 

  • CLSI (2019) Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing, 29th edn. CLSI supplement M100, Wayne

  • Dandachi I, Chabou S, Daoud Z, Rolain JM (2018) Prevalence and emergence of extended-spectrum cephalosporin-, carbapenem-and colistin-resistant Gram negative bacteria of animal origin in the Mediterranean basin. Front Microbiol 9:2299

    Article  Google Scholar 

  • Datta S, Akter A, Shah IG, Fatema K, Islam TH, Bandyopadhyay A, Khan ZUM, Biswas D (2012) Microbiological quality assessment of raw meat and meat products, and antibiotic susceptibility of isolated Staphylococcus aureus. Agric Food Anal Bacteriol 2(3):187–194

    Google Scholar 

  • Dave D, Ghaly AE (2011) Meat spoilage mechanisms and preservation techniques: a critical review. Am J Agric Biol Sci 6:486–510

    Article  CAS  Google Scholar 

  • Dipineto L, Santaniello A, Fontanella M, Lagos K, Fioretti A, Menna LF (2006) Presence of Shiga toxin-producing Escherichia coli O157:H7 in living layer hens. Lett Appl Microbiol 43(3):293–295

    Article  CAS  Google Scholar 

  • Doulgeraki AI, Ercolini D, Villani F, Nychas GJE (2012) Spoilage microbiota associated to the storage of raw meat in different conditions. Int J Food Microbiol 157(2):130–141

    Article  Google Scholar 

  • Economou V, Gousia P (2015) Agriculture and food animals as a source of antimicrobial-resistant bacteria. Infect Drug Resist 8:49

    Article  Google Scholar 

  • Ekawati ER, Darmanto W (2019) Lemon (Citrus limon) juice has antibacterial potential against diarrhea-causing pathogen. IOP Conf Ser Earth Environ Sci 217:012023

    Article  Google Scholar 

  • Elamary R, Shibat El-hamed D, Sayed W, Salem W (2018) In vitro and in vivo molecular studies on some Escherichia coli serovars isolated from chicken. SVU Int J Vet Sci 1(2):33–49

    Google Scholar 

  • Elamary RB, Albarakaty FM, Salem WM (2020) Efficacy of Acacia nilotica aqueous extract in treating biofilm-forming and multidrug resistant uropathogens isolated from patients with UTI syndrome. Sci Rep 10(1):1–14

    Article  CAS  Google Scholar 

  • El-Azzouny MM, El-Demerdash AS, Seadawy HG, Abou-Khadra SH (2018) Antimicrobial effect of garlic (Allium sativum) and thyme (Zataria multiflora Boiss) extracts on some food borne pathogens and their effect on virulence gene expression. Cell Mol Biol (noisy-Le-Grand) 64(10):79–86

    Article  Google Scholar 

  • Eloff JN (1998) A sensitive and quick microplate method to determine the minimal inhibitory concentration of plant extracts for bacteria. Planta Med 64(08):711–713

    Article  CAS  Google Scholar 

  • El-Sharkaway S, Samaha IA, El-Galil HIA (2016) Prevalence of pathogenic microorganisms in raw meat products from retail outlets in Alexandria province. Alex J Vet Sci 51(2):374–380

    Google Scholar 

  • El Sheikha AF, Xu J (2017) Traceability as a key of seafood safety: reassessment and possible applications. Rev Fish Sci Aquac 25(2):158–170

    Article  Google Scholar 

  • El Sheikha AF, Xu J (2018) Molecular techniques and foodstuffs: innovative fingerprints, then what? Mol Tech Food Biol Saf Biotechnol Authent Traceab 19:S423-434

    Google Scholar 

  • EOS (2004) Frozen meat, Egyptian organization for standarization and quality control. Arab Republic of Egypt ES: 4334/2004

  • EOS (2005a) Frozen minced meat, Egyptian organization for standardization and quality control. Arab Republic of Egypt ES:1694/2005

  • EOS (2005b) Beef burger, Egyptian organization for standarization and quality control. Arab Republic of Egypt ES:1688/2005

  • EOS (2005c) Chicken and turkey meat products, Egyptian organization for standarization and quality control. Arab Republic of Egypt ES: 2910/2005

  • FAO (2019) The state of food and agriculture 2019. Moving forward on food loss and waste reduction. FAO, Rome

  • Fialova S, Rendekova K, Mucaji P, Slobodnikova L (2017) Plant natural agents: polyphenols, alkaloids andessential oils as perspective solution of microbial resistance. Curr Org Chem 21:1875–1884

    Article  CAS  Google Scholar 

  • Frye JG, Jackson CR (2013) Genetic mechanisms of antimicrobial resistance identified in Salmonella enterica, Escherichia coli, and Enteroccocus spp. isolated from US food animals. Front Microbiol 4:135

    Article  Google Scholar 

  • Gagaoua M, Boudechicha HR (2018) Ethnic meat products of the North African and Mediterranean countries: an overview. J Ethn Foods 5(2):83–98

    Article  Google Scholar 

  • Ghasemi K, Ghasemi Y, Ebrahimzadeh MA (2009) Antioxidant activity, phenol and flavonoid contents of 13 citrus species peels and tissues. Pak J Pharm Sci 22(3):277–281

    CAS  Google Scholar 

  • Gutiérrez-del-Río I, Fernández J, Lombó F (2018) Plant nutraceuticals as antimicrobial agents in food preservation: terpenoids, polyphenols and thiols. Int J Antimicrob Agents 52(3):309–315

    Article  CAS  Google Scholar 

  • Gwida M, Hotzel H, Geue L, Tomaso H (2014) Occurrence of Enterobacteriaceae in raw meat and in human samples from Egyptian retail sellers. In: International scholarly research notices

  • Hemeg HA (2018) Molecular characterization of antibiotic resistant Escherichia coli isolates recovered from food samples and outpatient Clinics. KSA Saudi J Biol Sci 25(5):928–931

    Article  CAS  Google Scholar 

  • Hęś M, Gramza-Michałowska A (2017) Effect of plant extracts on lipid oxidation and changes in nutritive value of protein infrozen-stored meat products. J Food Process Preserv 41:e12989

    Article  CAS  Google Scholar 

  • Hussein HS (2007) Prevalence and pathogenicity of Shiga toxin-producing Escherichia coli in beef cattle and their products. J Anim Sci 85:63–72

    Article  Google Scholar 

  • Hussein MA, Eldaly EA, Seadawy HG, El-Nagar EF (2018) Virulence and antimicrobial resistance genes of Escherichia coli in ready to eat sandwiches in sharkia governorate. Slov Vet Res 55(20):383–392

    Google Scholar 

  • Ichikawa M, Ide N, Yoshida J, Yamaguchi H, Ono K (2006) Determination of seven organosulfur compounds in garlic by high-performance liquid chromatography. J Agric Food Chem 54(5):1535–1540

    Article  CAS  Google Scholar 

  • Ifesan BOT, Fadipe EA, Ifesan BT (2014) Investigation of antioxidant and antimicrobial properties of garlic peel extract (Allium sativum) and its use as natural food additive in cooked beef. J Sci Res Rep 3:711–721

    Google Scholar 

  • Jabar MA, Al-Mossawi A (2007) Susceptibility of some multiple resistant bacteria to garlic extract. Afr J Biotechnol 6(6):771–776

    Google Scholar 

  • Kahali S, Sarkar B, Rajendran K, Khanam J, Yamasaki S, Nandy RK, Bhattacharya SK, Ramamurthy T (2004) Virulence characteristics and molecular epidemiology of enteroaggregative Escherichia coli isolates from hospitalized diarrheal patients in Kolkata, India. J Clin Microbiol 42(9):4111–4120

    Article  CAS  Google Scholar 

  • Karadeniz F (2004) Main organic acid distribution of authentic citrus juices in Turkey. Turk J Agric for 28(4):267–271

    CAS  Google Scholar 

  • Karimi E, Oskoueian E, Hendra R, Oskoueian A, Jaafar HZ (2012) Phenolic compounds characterization and biological activities of Citrus aurantium bloom. Molecules 17(2):1203–1218

    Article  CAS  Google Scholar 

  • Khameneh B, Iranshahy M, Soheili V, Bazzaz BSF (2019) Review on plant antimicrobials: a mechanisticviewpoint. Antimicrob Resist Infect Control 8:118

    Article  Google Scholar 

  • Kok T, Worswich D, Gowans E (1996) Some serological techniques for microbial and viral infections. In: Collee J, Fraser A, Marmion B, Simmons A (eds) Practical medical microbiology, 14th edn. Wiley, Edinburgh, Churchill Livingstone, UK, pp 179–204

    Google Scholar 

  • Koneman EW, Allen SD, Janda WM, Schreckenberger PC, Winn WC (1997) Diagnostic microbiology. The nonfermentative Gram-negative bacilli. Lippincott-Raven Publishers, Philedelphia, pp 253–320

    Google Scholar 

  • Krieg NR, Holt JG (1984) Bergey’s manual of systemic bacteriology, vol 1. The William & Wilkins Co., Baltimore

    Google Scholar 

  • Kumar M, Berwal JS (1998) Sensitivity of food pathogens to garlic (Allium sativum). J Appl Microbiol 84(2):213–215

    Article  CAS  Google Scholar 

  • Kumar KA, Narayani M, Subanthini A, Jayakumar M (2011) Antimicrobial activity and phytochemical analysis of citrus fruit peels-utilization of fruit waste. Int J Eng Sci Technol 3(6):5414–5421

    Google Scholar 

  • Ladaniya MS (2008) Citrus fruit: biology, technology and evaluation. Academic Press, London

    Google Scholar 

  • Lall N, Henley-Smith CJ, De Canha MN, Oosthuizen CB, Berrington D (2013) Viability reagent, PrestoBlue, in comparison with other available reagents, utilized in cytotoxicity and antimicrobial assays. Int J Microbiol 2013

  • Latasa C, Roux A, Toledo-Arana A, Ghigo JM, Gamazo C, Penadés JR, Lasa I (2005) BapA, a large secreted protein required for biofilm formation and host colonization of Salmonella enterica serovar Enteritidis. Mol Microbiol 58(5):1322–1339

    Article  CAS  Google Scholar 

  • Li LY, Long WF, Wan DR, Zhang F, Ding Q, Mei ZN (2014) Quantitative determination of total alkaloids and berberine in five medicinal berberis plants. Chin J Exp Tradit Med Formulae 17:28

    Google Scholar 

  • Magiorakos AP, Srinivasan A, Carey RT, Carmeli Y, Falagas MT, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, Olsson-Liljequist B, Paterson DL, Rice LB, Stelling J, Struelens MJ, Vatopoulos A, Weber JT, Monnet DT (2012) Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 18(3):268–281

    Article  CAS  Google Scholar 

  • Makkar HP (2003) Quantification of tannins in tree and shrub foliage: a laboratory manual. Springer, Berlin

    Book  Google Scholar 

  • Manessis G, Kalogianni AI, Lazou T, Moschovas M, Bossis I, Gelasakis AI (2020) Plant-derived natural antioxidants in meat and meat products. Antioxidants 9(12):1215

    Article  CAS  Google Scholar 

  • Meng J, Schroeder CM (2007) Escherichia coli in foodborne diseases. In: Simjee S (ed) 1–17

  • Messele YE, Abdi RD, Yalew ST, Tegegne DT, Emeru BA, Werid GM (2017) Molecular determination of antimicrobial resistance in Escherichia coli isolated from raw meat in Addis Ababa and Bishoftu, Ethiopia. Ann Clin Microbiol Antimicrob 16(1):55

    Article  CAS  Google Scholar 

  • Mu H, Tang J, Liu Q, Sun C, Wang T, Duan J (2016) Potent antibacterial nanoparticles against biofilm and intracellular bacteria. Sci Rep 6(1):1–9

    Article  CAS  Google Scholar 

  • Mukumbo FE, Descalzo AM, Collignan A, Hoffman LC, Servent A, Muchenje V, Arnaud E (2019) Effect of Moringa oleiferaleaf powder on drying kinetics, physico-chemical properties, ferric reducing antioxidant power, α-tocopherol, β-carotene, and lipidoxidation of dry pork sausages during processing and storage. J Food Process Preserv 44:44

    Google Scholar 

  • Najjaa H, Chekki R, Elfalleh W, Tlili H, Jaballah S, Bouzouita N (2020) Freeze-dried, oven-dried, and microencapsulation of essential oil from Allium sativum as potential preservative agents of minced meat. Food Sci Nutr 8(4):1995–2003

    Article  CAS  Google Scholar 

  • National Committee for Clinical Laboratory Standards (2002) Performance standards for antimicrobial susceptibility testing. 12th informational supplement. Approved standard M100-S12

  • Naves P, del Prado G, Huelves L, Gracia M, Ruiz V, Blanco J, Dahbi G, Blanco M, del Carmen PM, Soriano F (2008) Correlation between virulence factors and in vitro biofilm formation by Escherichia coli strains. Microb Pathog 45(2):86–91

    Article  CAS  Google Scholar 

  • Njue L, Kanja LW, Ombui JN, Nduhiu JG, Obiero D (2014) Efficacy of antimicrobial activity of garlic extracts on bacterial pathogens commonly found to contaminate meat. East Afr Med J 91(12):442–448

    CAS  Google Scholar 

  • Noor R (2016) Microbiological quality of commonly consumed street foods in Bangladesh. Nutr Food Sci 46(1):130–141

    Article  Google Scholar 

  • Nour V, Trandafir I, Ionica M (2010) HPLC organic acid analysis in different citrus juices under reversed phase conditions. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 38(1):44–48

    CAS  Google Scholar 

  • Nychas GE, Skandamis PN, Tassou CC, Koutsoumanis KP (2008) Meat spoilage during distribution. Meat Sci 78:77–89

    Article  Google Scholar 

  • Obrig TG (2010) Escherichia coli Shiga toxin mechanisms of action in renal disease. Toxins 2(12):2769–2794

    Article  CAS  Google Scholar 

  • Olaoye OA, Ntuen IG (2011) Spoilage and preservation of meat: a general appraisal and potential of lactic acid bacteria as biological preservatives. Int Res J Biotechnol 2(1):033–046

    Google Scholar 

  • Osés SM, Pascual-Mate A, de la Fuente D, de Pablo A, Fernandez-Muino MA, Sancho MT (2016) Comparison of methods to determine antibacterial activity of honeys against Staphylococcus aureus. NJAS Wagening J Life Sci 78:29–33

    Article  Google Scholar 

  • Özçelik B, Kartal M, Orhan I (2011) Cytotoxicity, antiviral and antimicrobial activities of alkaloids, flavonoids, and phenolic acids. Pharm Biol 49:396–402

    Article  CAS  Google Scholar 

  • Ozen BO, Soyer A (2018) Effect of plant extracts on lipid and protein oxidation of mackerel (Scomber scombrus) mince during frozenstorage. J Food Sci Technol 55:120–127

    Article  CAS  Google Scholar 

  • Papu S, Singh S, Singh BR (2014) Effect of drying methods, pretreatments and loading density on garlic leaves. Int J Food Nutr Sci 3(4):184

    Google Scholar 

  • Paton JC, Paton AW (1998) Pathogenesis and diagnosis of Shiga toxin-producing Escherichia coli infections. Clin Microbiol Rev 11(3):450–479

    Article  CAS  Google Scholar 

  • Pejin B, Savic A, Sokovic M, Glamoclija J, Ciric A, Nikolic M, Radotic K, Mojovic M (2014) Further in vitro evaluation of antiradical and antimicrobial activities of phytol. Nat Prod Res 28(6):372–376

    Article  CAS  Google Scholar 

  • Pejin B, Ciric A, Glamoclija J, Nikolic M, Sokovic M (2015a) In vitro anti-quorum sensing activity of phytol. Nat Prod Res 29(4):374–377

    Article  CAS  Google Scholar 

  • Pejin B, Ciric A, Glamoclija J, Nikolic M, Stanimirovic B, Sokovic M (2015b) Quercetin potently reduces biofilm formation of the strain Pseudomonas aeruginosa PAO1 in vitro. Curr Pharm Biotechnol 16(8):733–737

    Article  CAS  Google Scholar 

  • Piva IC, Pereira AL, Ferraz LR, Silva RS, Vieira AC, Blanco JE, Blanco M, Blanco J, Giugliano LG (2003) Virulence markers of enteroaggregative Escherichia coli isolated from children and adults with diarrhea in Brasilia. Brazil J Clin Microbiol 41(5):1827–1832

    Article  CAS  Google Scholar 

  • Rahman U, Sahar A, Ishaq A, Aadil RM, Zahoor T, Ahmad MH (2018) Advanced meat preservationmethods: a mini review. J Food Saf 38:e12467

    Article  Google Scholar 

  • Ratthawongjirakul P, Thongkerd V (2016) Fresh garlic extract inhibits Staphylococcus aureus biofilm formation under chemopreventive and chemotherapeutic conditions. Songklanakarin J Sci Technol 38(4):381–389

    CAS  Google Scholar 

  • Rekha C, Poornima G, Manasa M, Abhipsa V, Devi JP, Kumar HTV, Kekuda TRP (2012) Ascorbic acid, total phenol content and antioxidant activity of fresh juices of four ripe and unripe citrus fruits. Chem Sci Trans 1(2):303–310

    Article  CAS  Google Scholar 

  • Rocha RP, Melo EC (2011) Influence of drying process on the quality of medicinal plants: a review. J Med Plants Res 5(33):7076–7084

    Article  Google Scholar 

  • Salem W, Leitner DR, Zingl FG, Schratter G, Prassl R, Goessler W, Reidl J, Schild S (2015) Antibacterial activity of silver and zinc nanoparticles against Vibrio cholerae and enterotoxic Escherichia coli. Int J Med Microbiol 305(1):85–95

    Article  CAS  Google Scholar 

  • Salem WM, El-Hamed DS, Sayed W, Elamary R (2017) Alterations in virulence and antibiotic resistant genes of multidrug-resistant Salmonella serovars isolated from poultry: the bactericidal efficacy of Allium sativum. Microb Pathog 108:91–100

    Article  CAS  Google Scholar 

  • Sallam KI, Ishioroshi M, Samejima K (2004) Antioxidant and antimicrobial effects of garlic in chicken sausage. LWT Food Sci Technol 37(8):849–855

    Article  CAS  Google Scholar 

  • Sarma N (2004) Can garlic (Allium sativum) be used as a meat preservative? Trans Kans Acad Sci 107(3):148–154

    Article  Google Scholar 

  • Seper A, Fengler VH, Roier S, Wolinski H, Kohlwein SD, Bishop AL, Camilli A, Reidl J, Schild S (2011) Extracellular nucleases and extracellular DNA play important roles in Vibrio cholerae biofilm formation. Mol Microbiol 82(4):1015–1037

    Article  CAS  Google Scholar 

  • Shilenge LB, Shale K, Matodzi T, Machete F, Tshelane C (2017) A review of microbial hazards associated with meat processing in butcheries. Afr J Sci Technol Innov Dev 9(1):1–6

    Article  Google Scholar 

  • Singleton VL, Orthofer R, Lamuela-Raventós RM (1999) [14] Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent. Methods Enzymol 299:152–178

    Article  CAS  Google Scholar 

  • Sirelkhatim A, Mahmud S, Seeni A, Kaus NHM, Ann LC, Bakhori SKM, Hasan H, Mohamad D (2015) Review on zinc oxide nanoparticles: antibacterial activity and toxicity mechanism. Nano Micro Lett 7(3):219–242

    Article  CAS  Google Scholar 

  • Street RA, Prinsloo G (2013) Commercially important medicinal plants of South Africa: a review. J Chem 2013:1–16.

  • Tadesse HA, Gidey NB, Workelule K, Hailu H, Gidey S, Bsrat A, Taddele H (2018) Antimicrobial resistance profile of E. coli isolated from raw cow milk and fresh fruit juice in Mekelle, Tigray, Ethiopia. Veterinary Medicine International

  • Tamminen LM, Fransson H, Tråvén M, Aspán A, Alenius S, Emanuelson U, Dreimanis I, Törnquist M, Eriksson E (2018) Effect of on-farm interventions in the aftermath of an outbreak of hypervirulent verocytotoxin-producing Escherichia coli O157:H7 in Sweden. Veterinary Record

  • Wilson D, Dolan G, Aird H, Sorrell S, Dallman TJ, Jenkins C, Robertson L, Gorton R (2018) Farm-to-fork investigation of an outbreak of Shiga toxin-producing Escherichia coli O157. Microb Genom 4(3)

  • Wong CS, Jelacic S, Habeeb RL, Watkins SL, Tarr PI (2000) The risk of the hemolytic–uremic syndrome after antibiotic treatment of Escherichia coli O157:H7 infections. N Engl J Med 342(26):1930–1936

    Article  CAS  Google Scholar 

  • Yoo M, Lee S, Lee S, Seog H, Shin D (2010) Validation of high performance liquid chromatography methods for determination of bioactive sulfur compounds in garlic bulbs. Food Sci Biotechnol 19(6):1619–1626

    Article  CAS  Google Scholar 

  • Younis RI, Nasef SA, Salem WM (2019) Detection of multi-drug resistant food-borne bacteria in ready-to-eat meat products in Luxor City, Egypt. SVU Int J Vet Sci 2(1):20–35

    Google Scholar 

  • Zahid MA, Choi JY, Seo JK, Parvin R, Ko J, Yang HS (2020) Effects of clove extract on oxidative stability and sensory attributesin cooked beef patties at refrigerated storage. Meat Sci 161:107972

    Article  CAS  Google Scholar 

  • Zhang Y, Henning SM, Lee RP, Huang J, Zerlin A, Li Z, Heber D (2015) Turmeric and black pepper spices decrease lipidperoxidation in meat patties during cooking. Int J Food Sci Nutr 66:260–265

    Article  CAS  Google Scholar 

  • Zhishen J, Mengcheng T, Jianming W (1999) The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 64(4):555–559

    Article  CAS  Google Scholar 

  • Zhou GH, Xu XL, Liu Y (2010) Preservation technologies for fresh meat—a review. Meat Sci 86:119–128

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful to M. Abou El-Dahab, assitant lecturer of Microbiology, Department of Botany and Microbiology, Faculty of Science, South Valley University, for performing and presented the various statistical analysis.

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The authors did not receive support from any organization for the submitted work.

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  1. Department of Botany and Microbiology, Faculty of Science, South Valley University, Qena, 83523, Egypt

    R. B. Elamary, M. Wahba, W. F. Sayed & W. M. Salem

Authors
  1. R. B. Elamary
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  2. M. Wahba
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  3. W. F. Sayed
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  4. W. M. Salem
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Contributions

WFS, WMS, and RE supervised the whole research. RE draw the figures and make statistical analysis. MW performed practical work, analyzed the data and wrote the draft manuscript. RE was a major contributor in writing the manuscript and supervision of practile part. All authors read and approved the final manuscript.

Corresponding author

Correspondence to R. B. Elamary.

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All authors declare that they have no conflicts of interest.

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Editorial responsibility: Xu Han.

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Elamary, R.B., Wahba, M., Sayed, W.F. et al. Efficiency of certain vegetables under various storage conditions against the meat-borne Escherichia coli isolates. Int. J. Environ. Sci. Technol. 19, 7869–7884 (2022). https://doi.org/10.1007/s13762-021-03692-6

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  • DOI: https://doi.org/10.1007/s13762-021-03692-6

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