Detection of hemolytic Shiga toxin-producing Escherichia coli in fresh vegetables and efficiency of phytogenically synthesized silver nanoparticles by Syzygium aromaticum extract and gamma radiation against isolated pathogens.
Biogenic silver nanoparticles
Foodborne E. coli
Gamma irradiation
Journal
BMC microbiology
ISSN: 1471-2180
Titre abrégé: BMC Microbiol
Pays: England
ID NLM: 100966981
Informations de publication
Date de publication:
18 09 2023
18 09 2023
Historique:
received:
10
05
2023
accepted:
25
08
2023
medline:
20
9
2023
pubmed:
19
9
2023
entrez:
18
9
2023
Statut:
epublish
Résumé
Shiga toxin-producing E. coli (STEC) is a major cause of foodborne diseases accompanied by several clinical illnesses in humans. This research aimed to isolate, identify, and combat STEC using novel alternative treatments, researchers have lately investigated using plant extract to produce nanoparticles in an environmentally acceptable way. At various gamma-ray doses, gamma irradiation is used to optimize the conditions for the biogenically synthesized silver nanoparticles (Ag NPs) using an aqueous extract of clove as a reducing and stabilizing agent. On a specific medium, 120 vegetable samples were screened to isolate STEC and molecularly identified using real-time PCR. Moreover, the antibacterial and antibiofilm activities of biogenically synthesized Ag NPs against the isolated STEC were examined. Twenty-five out of 120 samples of eight types of fresh vegetables tested positive for E. coli, as confirmed by 16S rRNA, of which three were positive for the presence of Stx-coding genes, and six were partially hemolytic. Seven antibiotic disks were used to determine antibiotic susceptibility; the results indicated that isolate STX These findings suggest that the biogenic Ag NPs can be utilized as a new promising antibacterial agent to combat biofouling on surfaces.
Sections du résumé
BACKGROUND
Shiga toxin-producing E. coli (STEC) is a major cause of foodborne diseases accompanied by several clinical illnesses in humans. This research aimed to isolate, identify, and combat STEC using novel alternative treatments, researchers have lately investigated using plant extract to produce nanoparticles in an environmentally acceptable way. At various gamma-ray doses, gamma irradiation is used to optimize the conditions for the biogenically synthesized silver nanoparticles (Ag NPs) using an aqueous extract of clove as a reducing and stabilizing agent.
METHODS
On a specific medium, 120 vegetable samples were screened to isolate STEC and molecularly identified using real-time PCR. Moreover, the antibacterial and antibiofilm activities of biogenically synthesized Ag NPs against the isolated STEC were examined.
RESULTS
Twenty-five out of 120 samples of eight types of fresh vegetables tested positive for E. coli, as confirmed by 16S rRNA, of which three were positive for the presence of Stx-coding genes, and six were partially hemolytic. Seven antibiotic disks were used to determine antibiotic susceptibility; the results indicated that isolate STX
CONCLUSION
These findings suggest that the biogenic Ag NPs can be utilized as a new promising antibacterial agent to combat biofouling on surfaces.
Identifiants
pubmed: 37723460
doi: 10.1186/s12866-023-02994-8
pii: 10.1186/s12866-023-02994-8
pmc: PMC10508014
doi:
Substances chimiques
Silver
3M4G523W1G
RNA, Ribosomal, 16S
0
Anti-Bacterial Agents
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
262Informations de copyright
© 2023. BioMed Central Ltd., part of Springer Nature.
Références
Shen J, Zhi S, Guo D, Jiang Y, Xu X, Zhao L, et al. Prevalence, Antimicrobial Resistance, and Whole Genome Sequencing Analysis of Shiga Toxin-Producing Escherichia coli (STEC) and Enteropathogenic Escherichia coli (EPEC) from Imported Foods in China during 2015–2021. Toxins (Basel). 2022;14:68.
pubmed: 35202096
Organization WH. Shiga Toxin-producing Escherichia Coli (STEC) and Food: Attribution. Characterization and Monitoring: World Health Organization; 2019.
Solomon EB, Yaron S, Matthews KR. Transmission of Escherichia coli O157: H7 from contaminated manure and irrigation water to lettuce plant tissue and its subsequent internalization. Appl Environ Microbiol. 2002;68:397–400.
pubmed: 11772650
pmcid: 126537
De LC, De T. Nutrient rich foods in human diet as immunity boosters. J Pharmacogn Phytochem. 2021;10:197–206.
Micheal AO, Adenike AK, Oluwaseun AB, Ademola AD, Olutope OS, Joy OO, et al. Microbial contamination of some ready-to-eat vended fruits in Sango open-market, Saki, Oyo State. Nigeria Microbes and Infectious Diseases. 2022;3:160–5.
Rai PK, Tripathi BD. Microbial contamination in vegetables due to irrigation with partially treated municipal wastewater in a tropical city. Int J Environ Health Res. 2007;17:389–95.
pubmed: 17924267
Alegbeleye OO, Sant’Ana AS. Manure-borne pathogens as an important source of water contamination: An update on the dynamics of pathogen survival/transport as well as practical risk mitigation strategies. Int J Hyg Environ Health. 2020;227:113524.
Balali GI, Yar DD, Afua Dela VG, Adjei-Kusi P. Microbial contamination, an increasing threat to the consumption of fresh fruits and vegetables in today’s world. Int J Microbiol. 2020;2020.
Nile SH, Baskar V, Selvaraj D, Nile A, Xiao J, Kai G. Nanotechnologies in food science: applications, recent trends, and future perspectives. Nanomicro Lett. 2020;12:1–34.
Llorens A, Lloret E, Picouet PA, Trbojevich R, Fernandez A. Metallic-based micro and nanocomposites in food contact materials and active food packaging. Trends Food Sci Technol. 2012;24:19–29.
Ghobashy M, El-Wahab HA, … MI-MS and, undefined. Characterization of Starch-based three components of gamma-ray cross-linked hydrogels to be used as a soil conditioner. Elsevier. 2020.
Ghobashy MM, Alshangiti DM, Alkhursani SA, Al-Gahtany SA, Shokr FS, Madani M. Improvement of in vitro dissolution of the poor water-soluble amlodipine drug by solid dispersion with irradiated polyvinylpyrrolidone. ACS Omega. 2020;5:21476–87.
pubmed: 32905418
pmcid: 7469126
El-Behery RR, El-Sayed ESR, El-Sayyad GS. Gamma rays-assisted bacterial synthesis of bimetallic silver-selenium nanoparticles: powerful antimicrobial, antibiofilm, antioxidant, and photocatalytic activities. BMC Microbiol. 2023;23:224. https://0-doi-org.brum.beds.ac.uk/10.1186/s12866-023-02971-1 .
Mossa S, Shameli K. Gamma Irradiation-Assisted Synthesis of Silver Nanoparticle and Their Antimicrobial Applications: A Review. Journal of Research in Nanoscience and Nanotechnology. 2021;3:53–75.
Alavi M, Hamblin MR, Kennedy JF. Antimicrobial applications of lichens: Secondary metabolites and green synthesis of silver nanoparticles: A review. Nano Micro Biosystems. 2022;1:15–21.
Hashem AH, El-Sayyad GS. Antimicrobial and anticancer activities of biosynthesized bimetallic silver-zinc oxide nanoparticles (Ag-ZnO NPs) using pomegranate peel extract. Biomass Convers Biorefin. 2023;:1–13.
Ajitha B, Reddy YAK, Lee Y, Kim MJ, Ahn CW. Biomimetic synthesis of silver nanoparticles using Syzygium aromaticum (clove) extract: catalytic and antimicrobial effects. Appl Organomet Chem. 2019;33: e4867.
Vijayakumar S, Malaikozhundan B, Saravanakumar K, Durán-Lara EF, Wang M-H, Vaseeharan B. Garlic clove extract assisted silver nanoparticle–Antibacterial, antibiofilm, antihelminthic, anti-inflammatory, anticancer and ecotoxicity assessment. J Photochem Photobiol B. 2019;198: 111558.
pubmed: 31357173
Lakhan MN, Chen R, Shar AH, Chand K, Shah AH, Ahmed M, et al. Eco-friendly green synthesis of clove buds extract functionalized silver nanoparticles and evaluation of antibacterial and antidiatom activity. J Microbiol Methods. 2020;173: 105934.
pubmed: 32325159
Tekin V, Kozgus Guldu O, Dervis E, Yurt Kilcar A, Uygur E, Biber Muftuler FZ. Green synthesis of silver nanoparticles by using eugenol and evaluation of antimicrobial potential. Appl Organomet Chem. 2019;33: e4969.
Tango CN, Choi N-J, Chung M-S, Oh DH. Bacteriological quality of vegetables from organic and conventional production in different areas of Korea. J Food Prot. 2014;77:1411–7.
pubmed: 25198606
Jalil K, Vadood R, Abolfazl B. Isolation of Escherichia coli O157: H7 from manure fertilized farms and raw vegetables grown on it, in Tabriz city in Iran. Afr J Microbiol Res. 2010;4:891–5.
Mritunjay SK, Kumar V. A study on prevalence of microbial contamination on the surface of raw salad vegetables. 3 Biotech. 2017;7:1–9.
March SB, Ratnam S. Sorbitol-MacConkey medium for detection of Escherichia coli O157: H7 associated with hemorrhagic colitis. J Clin Microbiol. 1986;23:869–72.
pubmed: 3519658
pmcid: 268739
Possé B, de Zutter L, Heyndrickx M, Herman L. Novel differential and confirmation plating media for Shiga toxin-producing Escherichia coli serotypes O26, O103, O111, O145 and sorbitol-positive and-negative O157. FEMS Microbiol Lett. 2008;282:124–31.
pubmed: 18355285
England PH. Preparation of samples and dilutions, plating and sub‐culture. Microbiology Services Food Water and Environmental Microbiology Standard Method FNES26 (F2). 2014;:12–3.
Hu Q, Tu J, Han X, Zhu Y, Ding C, Yu S. Development of multiplex PCR assay for rapid detection of Riemerella anatipestifer, Escherichia coli, and Salmonella enterica simultaneously from ducks. J Microbiol Methods. 2011;87:64–9.
pubmed: 21791228
Santaniello A, Dipineto L, Cuomo A, Fontanella M, Calabria M, Sensale M, et al. Detection of Shiga toxin-producing Escherichia coli O157 in living layer hens. In: EPC 2006–12th European Poultry Conference, Verona, Italy, 10–14 September, 2006. World’s Poultry Science Association (WPSA); 2006.
Bauer AW. Antibiotic susceptibility testing by a standardized single disc method. Am J clin pathol. 1966;45:149–58.
Wayne PA. Clinical and laboratory standards institute; 2007. Performance standards for antimicrobial susceptibility testing CLSI document M100-S17. 2005.
Maksoud MIAA, El-Sayyad GS, El-Bastawisy HS, Fathy RM. Antibacterial and antibiofilm activities of silver-decorated zinc ferrite nanoparticles synthesized by a gamma irradiation-coupled sol–gel method against some pathogenic bacteria from medical operating room surfaces. RSC Adv. 2021;11:28361–74.
pubmed: 35480774
pmcid: 9038124
Meroni G, Soares Filipe JF, Martino PA. In vitro antibacterial activity of biological-derived silver nanoparticles: Preliminary data. Vet Sci. 2020;7:12.
pubmed: 31979282
pmcid: 7157719
Bhatwalkar SB, Gound SS, Mondal R, Srivastava RK, Anupam R. Anti-biofilm and antibacterial activity of Allium sativum against drug resistant shiga-toxin producing Escherichia coli (STEC) isolates from patient samples and food Sources. Indian J Microbiol. 2019;59:171–9.
pubmed: 31031431
pmcid: 6458215
El-Sayyad GS, El-Bastawisy HS, Gobara M, El-Batal AI. Gentamicin-assisted mycogenic selenium nanoparticles synthesized under gamma irradiation for robust reluctance of resistant urinary tract infection-causing pathogens. Biol Trace Elem Res. 2020;195:323–42.
pubmed: 31396853
Oliveira M, Viñas I, Usall J, Anguera M, Abadias M. Presence and survival of Escherichia coli O157: H7 on lettuce leaves and in soil treated with contaminated compost and irrigation water. Int J Food Microbiol. 2012;156:133–40.
pubmed: 22483400
Özpınar H, Turan B, Tekiner İH, Tezmen G, Gökçe İ, Akıneden Ö. Evaluation of pathogenic E scherichia coli occurrence in vegetable samples from district bazaars in Istanbul using real-time PCR. Lett Appl Microbiol. 2013;57:362–7.
pubmed: 23789811
Shakerian A, Rahimi E, Emad P. Vegetables and restaurant salads as a reservoir for Shiga toxigenic Escherichia coli: distribution of virulence factors, O-serogroups, and antibiotic resistance properties. J Food Prot. 2016;79:1154–60.
pubmed: 27357034
Nousiainen L-L, Joutsen S, Lunden J, Hänninen M-L, Fredriksson-Ahomaa M. Bacterial quality and safety of packaged fresh leafy vegetables at the retail level in Finland. Int J Food Microbiol. 2016;232:73–9.
pubmed: 27257744
Wood J, Chen J, … EF, 2015 undefined. Microbiological survey of locally grown lettuce sold at farmers’ markets in Vancouver, British Columbia. Journal of food protection . 2015;78:203–8.
Althaus D, Hofer E, Corti S, Julmi A, Stephan R. Bacteriological survey of ready-to-eat lettuce, fresh-cut fruit, and sprouts collected from the Swiss market. J Food Prot. 2012;75:1338–41.
pubmed: 22980021
WHO. The world health report 2000: health systems: improving performance. World Health Organization; 2000.
Lamikanra O. Fresh-cut fruits and vegetables: science, technology, and market. CRC press; 2002.
El-Tawab A, Ashraf A, Agag MA. Bacteriological and molecular studies on Shiga-Toxin producing Escherichia coli causing cattle clinical mastitis. Benha Vet Med J. 2017;33:17–26.
Iwu CD, du Plessis E, Korsten L, Okoh AI. Prevalence of E. coli O157: H7 strains in irrigation water and agricultural soil in two district municipalities in South Africa. International Journal of Environmental Studies. 2021;78:474–83.
Maciel MV de OB, da Rosa Almeida A, Machado MH, de Melo APZ, da Rosa CG, de Freitas DZ, et al. Syzygium aromaticum L.(clove) essential oil as a reducing agent for the green synthesis of silver nanoparticles. Open Journal of Applied Sciences. 2019;9:45.
Sayed WAA, El-Helaly A. Impact of silver nanoparticles synthesized by irradiated polyvinylpyrrolidone on spodoptera littoralis nucleopolyhedrosis virus activity. J Polym Environ. 2021;29:3364–74.
El-Batal AI, El-Sayyad GS, Al-Hazmi NE, Gobara M. Antibiofilm and antimicrobial activities of silver boron nanoparticles synthesized by PVP polymer and gamma rays against urinary tract pathogens. J Clust Sci. 2019;30:947–64.
Slistan-Grijalva A, Herrera-Urbina R, Rivas-Silva JF, Ávalos-Borja M, Castillón-Barraza FF, Posada-Amarillas A. Classical theoretical characterization of the surface plasmon absorption band for silver spherical nanoparticles suspended in water and ethylene glycol. Physica E Low Dimens Syst Nanostruct. 2005;27:104–12.
Jana F, Pareeka S, Srivastavab RP, Zahoora I, Sharmaa A, Shrivastavaa D. Anti-cancerous and anti-bacterial potential of silver nanoparticles synthesized using leaf extract of fern-Dryopteris barbigera. Dig J Nanomater Biostruct. 2022;17:285–99.
Saware K, Sawle B, Salimath B, Jayanthi K, Abbaraju V. Biosynthesis and characterization of silver nanoparticles using Ficus benghalensis leaf extract. Int J Res Eng Technol. 2014;3:867–74.
Dutta T, Ghosh NN, Das M, Adhikary R, Mandal V, Chattopadhyay AP. Green synthesis of antibacterial and antifungal silver nanoparticles using Citrus limetta peel extract: Experimental and theoretical studies. J Environ Chem Eng. 2020;8: 104019.
Suhas DP, Jeong HM, Aminabhavi TM, Raghu A v. Preparation and characterization of novel polyurethanes containing 4, 4′‐{oxy‐1, 4‐diphenyl bis (nitromethylidine)} diphenol schiff base diol. Polym Eng Sci. 2014;54:24–32.
Mir RA, Kudva IT. Antibiotic-resistant Shiga toxin-producing Escherichia coli: An overview of prevalence and intervention strategies. Zoonoses Public Health. 2019;66:1–13.
pubmed: 30375197
Howard-Varona C, Vik DR, Solonenko NE, Li Y-F, Gazitua MC, Chittick L, et al. Fighting fire with fire: phage potential for the treatment of E. coli O157 infection. Antibiotics. 2018;7:101.
Singh P, Mijakovic I. Strong antimicrobial activity of silver nanoparticles obtained by the green synthesis in Viridibacillus sp. extracts. Front Microbiol. 2022;13.
Anand R, Bhagat M. Silver nanoparticles (AgNPs): As nanopesticides and nanofertilizers. MOJ Biol Med. 2019;4:19–20.
Cannilla C, Bonura G, Frusteri F, Spadaro D, Trocino S, Neri G. Development of an ammonia sensor based on silver nanoparticles in a poly-methacrylic acid matrix. J Mater Chem C Mater. 2014;2:5778–86.
Jiang Z-J, Liu C-Y, Sun L-W. Catalytic properties of silver nanoparticles supported on silica spheres. J Phys Chem B. 2005;109:1730–5.
pubmed: 16851151
Singh J, Kaur G, Kaur P, Bajaj R, Rawat M. A review on green synthesis and characterization of silver nanoparticles and their applications: a green nanoworld. World J Pharm Pharm Sci. 2016;7:730–62.
Mohanta YK, Biswas K, Jena SK, Hashem A, Abd_Allah EF, Mohanta TK. Anti-biofilm and antibacterial activities of silver nanoparticles synthesized by the reducing activity of phytoconstituents present in the Indian medicinal plants. Front Microbiol. 2020;:1143.
Matthysse AG, Deora R, Mishra M, Torres AG. Polysaccharides cellulose, poly-β-1, 6-N-acetyl-d-glucosamine, and colanic acid are required for optimal binding of Escherichia coli O157: H7 strains to alfalfa sprouts and K-12 strains to plastic but not for binding to epithelial cells. Appl Environ Microbiol. 2008;74:2384–90.
pubmed: 18310435
pmcid: 2293172
Bokranz W, Wang X, Tschäpe H, Römling U. Expression of cellulose and curli fimbriae by Escherichia coli isolated from the gastrointestinal tract. J Med Microbiol. 2005;54:1171–82.
pubmed: 16278431
Dakal TC, Kumar A, Majumdar RS, Yadav V. Mechanistic basis of antimicrobial actions of silver nanoparticles. Front Microbiol. 2016;7:1831.
pubmed: 27899918
pmcid: 5110546
Mikhailova EO. Silver nanoparticles: mechanism of action and probable bio-application. J Funct Biomater. 2020;11:84.
pubmed: 33255874
pmcid: 7711612
Parvekar P, Palaskar J, Metgud S, Maria R, Dutta S. The minimum inhibitory concentration (MIC) and minimum bactericidal concentration (MBC) of silver nanoparticles against Staphylococcus aureus. Biomater Investig Dent. 2020;7:105–9.
pubmed: 32939454
pmcid: 7470068
Loo YY, Rukayadi Y, Nor-Khaizura M-A-R, Kuan CH, Chieng BW, Nishibuchi M, et al. In vitro antimicrobial activity of green synthesized silver nanoparticles against selected gram-negative foodborne pathogens. Front Microbiol. 2018;9:1555.
Buszewski B, Railean-Plugaru V, Pomastowski P, Rafińska K, Szultka-Mlynska M, Golinska P, et al. Antimicrobial activity of biosilver nanoparticles produced by a novel Streptacidiphilus durhamensis strain. J Microbiol Immunol Infect. 2018;51:45–54.
pubmed: 27103501