Application of Quercus infectoria extract as a natural antimicrobial agent for chicken egg decontamination

array:24 ["pii" => "S0325754118300257" "issn" => "03257541" "doi" => "10.1016/j.ram.2017.12.003" "estado" => "S300" "fechaPublicacion" => "2018-10-01" "aid" => "268" "copyright" => "Asociación Argentina de Microbiología" "copyrightAnyo" => "2018" "documento" => "article" "crossmark" => 1 "licencia" => "http://creativecommons.org/licenses/by-nc-nd/4.0/" "subdocumento" => "fla" "cita" => "Rev Argent Microbiol. 2018;50:391-7" "abierto" => array:3 [ "ES" => true "ES2" => true "LATM" => true ] "gratuito" => true "lecturas" => array:2 [ "total" => 1337 "formatos" => array:3 [ "EPUB" => 39 "HTML" => 403 "PDF" => 895 ] ] "itemSiguiente" => array:19 [ "pii" => "S0325754117301803" "issn" => "03257541" "doi" => "10.1016/j.ram.2017.11.001" "estado" => "S300" "fechaPublicacion" => "2018-10-01" "aid" => "253" "copyright" => "Asociación Argentina de Microbiología" "documento" => "article" "crossmark" => 1 "licencia" => "http://creativecommons.org/licenses/by-nc-nd/4.0/" "subdocumento" => "fla" "cita" => "Rev Argent Microbiol. 2018;50:398-407" "abierto" => array:3 [ "ES" => true "ES2" => true "LATM" => true ] "gratuito" => true "lecturas" => array:2 [ "total" => 763 "formatos" => array:3 [ "EPUB" => 39 "HTML" => 465 "PDF" => 259 ] ] "en" => array:13 [ "idiomaDefecto" => true "cabecera" => "Original article" "titulo" => "Development and storage studies of high density macrocapsules containing Lactobacillus spp. strains as nutritional supplement in young calves" "tienePdf" => "en" "tieneTextoCompleto" => "en" "tieneResumen" => array:2 [ 0 => "en" 1 => "es" ] "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "398" "paginaFinal" => "407" ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Desarrollo de macrocápsulas con cepas de Lactobacillus spp. en alta densidad como suplemento nutricional de terneros jóvenes y análisis de su viabilidad durante el almacenamiento" ] ] "contieneResumen" => array:2 [ "en" => true "es" => true ] "contieneTextoCompleto" => array:1 [ "en" => true ] "contienePdf" => array:1 [ "en" => true ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0015" "etiqueta" => "Figure 3" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr3.jpeg" "Alto" => 1169 "Ancho" => 1383 "Tamanyo" => 70572 ] ] "descripcion" => array:1 [ "en" => "Effect of cryoprotectants during the freeze-drying process. Lowercase letters represent the difference in microbial counts between capsules within each stage of the process. Capital letters represent difference counting in the capsules between the different stages of the process. Data represented as mean±standard deviation." ] ] ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "Diego M. Astesana, Jorge A. Zimmermann, Laureano S. Frizzo, María V. Zbrun, Jesica E. Blajman, Ayelén P. Berisvil, Analía Romero-Scharpen, Marcelo L. Signorini, Marcelo R. Rosmini, Lorena P. Soto" "autores" => array:10 [ 0 => array:2 [ "nombre" => "Diego M." "apellidos" => "Astesana" ] 1 => array:2 [ "nombre" => "Jorge A." "apellidos" => "Zimmermann" ] 2 => array:2 [ "nombre" => "Laureano S." "apellidos" => "Frizzo" ] 3 => array:2 [ "nombre" => "María V." "apellidos" => "Zbrun" ] 4 => array:2 [ "nombre" => "Jesica E." "apellidos" => "Blajman" ] 5 => array:2 [ "nombre" => "Ayelén P." 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Columns with different superscript letters differ significantly (two-way ANOVA; Tukey test; p<0.05)." ] ] ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "María A. Vissani, Osvaldo Zabal, María S. Tordoya, Viviana Parreño, Etienne Thiry, María Barrandeguy" "autores" => array:6 [ 0 => array:2 [ "nombre" => "María A." "apellidos" => "Vissani" ] 1 => array:2 [ "nombre" => "Osvaldo" "apellidos" => "Zabal" ] 2 => array:2 [ "nombre" => "María S." "apellidos" => "Tordoya" ] 3 => array:2 [ "nombre" => "Viviana" "apellidos" => "Parreño" ] 4 => array:2 [ "nombre" => "Etienne" "apellidos" => "Thiry" ] 5 => array:2 [ "nombre" => "María" "apellidos" => "Barrandeguy" ] ] ] ] ] "idiomaDefecto" => "en" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S0325754118300051?idApp=UINPBA00004N" "url" => "/03257541/0000005000000004/v1_201811250605/S0325754118300051/v1_201811250605/en/main.assets" ] "en" => array:19 [ "idiomaDefecto" => true "cabecera" => "Original article" "titulo" => "Application of Quercus infectoria extract as a natural antimicrobial agent for chicken egg decontamination" "tieneTextoCompleto" => true "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "391" "paginaFinal" => "397" ] ] "autores" => array:1 [ 0 => array:4 [ "autoresLista" => "Ahmed A. Tayel, Mahmoud A. El-Sedfy, Ahmed I. Ibrahim, Shaaban H. Moussa" "autores" => array:4 [ 0 => array:4 [ "nombre" => "Ahmed A." "apellidos" => "Tayel" "email" => array:1 [ 0 => "tayel_ahmad@yahoo.com" ] "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "*" "identificador" => "cor0005" ] ] ] 1 => array:3 [ "nombre" => "Mahmoud A." "apellidos" => "El-Sedfy" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "b" "identificador" => "aff0010" ] ] ] 2 => array:3 [ "nombre" => "Ahmed I." "apellidos" => "Ibrahim" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "b" "identificador" => "aff0010" ] ] ] 3 => array:3 [ "nombre" => "Shaaban H." "apellidos" => "Moussa" "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "b" "identificador" => "aff0010" ] 1 => array:2 [ "etiqueta" => "c" "identificador" => "aff0015" ] ] ] ] "afiliaciones" => array:3 [ 0 => array:3 [ "entidad" => "Faculty of Aquatic and Fisheries Sciences, Kafrelsheikh University, Kafr-Elsheikh, Egypt" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Genetic Engineering and Biotechnology Research Institute, University of Sadat City, El-Sadat City, Egypt" "etiqueta" => "b" "identificador" => "aff0010" ] 2 => array:3 [ "entidad" => "College of Science and Humanitarian Studies, Shaqra University, Qwaieah, Saudi Arabia" "etiqueta" => "c" "identificador" => "aff0015" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Aplicación de un extracto de Quercus infectoria como agente antimicrobiano natural para la desinfección de huevos de gallina" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1750 "Ancho" => 2333 "Tamanyo" => 438211 ] ] "descripcion" => array:1 [ "en" => "Reduction in eggshell-contaminating microorganisms after different exposure times to Quercus infectoria extract. *Mean of 5 replicates. *QIE concentration of 1%." ] ] ] "textoCompleto" => "IntroductionFood preservation is a challenging issue faced by scientists, industry overseers, health observers and regular customers. Food could be decontaminated and preserved using specific compounds, e.g. preservatives or antimicrobials, which are defined as the added compounds that have the ability to kill or hinder microbial growth in foods<a class="elsevierStyleCrossRef" href="#bib0205">6</a>.Microbial contamination of eggs with pathogenic microorganisms is a serious health concern worldwide. Eggshells may be contaminated with microorganisms at different industrial stages, e.g. production, processing, preparation and packaging. Contamination and microbial transmission may be “vertical”, during egg formation in the ovaries, or “horizontal”, through egg exposure to the surrounded contaminated environment<a class="elsevierStyleCrossRef" href="#bib0215">8</a>. The correlation between the average of eggshell contamination and penetrating microbial pathogens into the egg contents was reported in many previous investigations<a class="elsevierStyleCrossRefs" href="#bib0220">9,23</a>.Although there are many approved chemical food disinfectants and preservatives from international regulatory agencies, to be applied as food antimicrobials, there is a strong need for finding more effective agents originated from natural sources<a class="elsevierStyleCrossRefs" href="#bib0325">30,31,35</a>. The principal advantages of the application of natural disinfectants and antimicrobials are their biodegradability, high biosafety level, wide spectrum and non-accumulating properties<a class="elsevierStyleCrossRefs" href="#bib0205">6,7,33</a>.Many reports provided strong indications that the extracts of medicinal plant could be ideal sources for producing new antimicrobial compounds, especially against antibiotic-resistant strains<a class="elsevierStyleCrossRefs" href="#bib0200">5,11,29</a>.Oak galls (Quercus infectoria) are abnormal round-shaped growths, which may appear on young oak tree branches<a class="elsevierStyleCrossRef" href="#bib0310">27</a>. Gall powder and its extracts were traditionally used to treat many disorders, diseases and symptoms, including menorrhagia, dysentery, diarrhea, internal hemorrhages, gonorrhea, tonsillitis, and impetigo<a class="elsevierStyleCrossRef" href="#bib0190">3</a>. Pharmacologically, it was suggested that galls have potent bioactivities, e.g. antioxidant, antibacterial, antifungal, antiviral, larvicidal, antiamoebic, antidiabetic, anti-inflammatory, antivenin, and wound healing<a class="elsevierStyleCrossRefs" href="#bib0355">18,25,32</a>. Gall applications, in food-related sectors, were also reported after being washed with running water to exclude bitter tannins before cooking. After that, galls could be powdered and applied as thickening agents in stews, or used as cereal supplements for making bread; nutgall powder and extract can be also used as a coffee substitute, e.g. as tea or herbal drink for health promotion<a class="elsevierStyleCrossRef" href="#bib0355">18</a>.Therefore, the current study was designed to evaluate Q. infectoria extract as a potential antimicrobial agent for decontaminating eggshells and to analyze its possible antimicrobial mode of action.Materials and methodsOak gall extract preparationOak galls, Q. infectoria Olivier (Fagaceae), were obtained from the Medicinal and Aromatic Plants Research Department, Agricultural Research Center, Giza, Egypt. Galls were dried with hot air at 45°C for 24h, then dried materials were powdered using an electrical grinder and the powder was sieved to get ∼60mesh particle size. Two hundred grams of gall powder were immersed in 1l of 70% ethanol and agitated at 230×g for 6h, using a rotary shaker. QIE was filtered in a Buchner funnel through filter papers, Whatman No. 41, to eliminate the plant particles, which were re-extracted with 500ml of the solvent and filtered and the total extracts were combined and subjected to flash evaporation at reduced pressure (Büchi, Flavil, Switzerland) at 40°C to discard about 90% of solvent till constant weight was attained. The final dry extract was further dried under vacuum in a desiccator, weighed and powdered. QIE powder was then suspended in distilled water, by vigorous agitation at 45°C, to reach a final concentration of 10% (w/v). Finally, extract solution was sterilized using a syringe filter (0.22μm pore size, sterilized) and kept at 4°C, in sterile dark bottles.Microbial strainsDifferent microbial strains were used for examining the antimicrobial activity of QIE: Staphylococcus aureus ATCC 25923, Escherichia coli ATCC 25922, Pseudomonas aeruginosa ATCC 25006, Salmonella Typhimurium ATCC 23852, and Candida albicans ATCC 10231. The bacterial strains were propagated at 37°C in nutrient broth (NB) or nutrient agar (NA) under aerobic conditions, whereas C. albicans was grown in yeast malt broth (YMB) and maintained on yeast malt agar (YMA). All microbial media were purchased from Difco Lab., Detroit, MI.Determination of extract antimicrobial activityThe antimicrobial activity of QIE was qualitatively and quantitatively assessed, by two different determinations: zone of growth inhibition (ZOI), using the disc diffusion assay, and the determination of minimal inhibitory concentrations (MIC) (according to Tayel et al.<a class="elsevierStyleCrossRef" href="#bib0345">34</a>), using the suitable growth media for each microbial strain. The reduction in microbial counts was evaluated after their treatment with each relevant MIC, after 1h and 5h of the exposure, using the standard plate count method for comparing.Experimental infection of eggsOne hundred and twenty five chicken eggs (grade A, 3–24h old) were obtained from the poultry farm – Kafrelsheikh University. Eggs were firstly washed then sterilized through immersion in 1% sodium hypochlorite solution for 30min, rewashed with sterilized water and allowed to dry in aseptic bags. Chicken fecal samples (80 samples weighed ∼1000g) were collected from farm litter, aseptically transported to the laboratory and suspended in 4l of buffered peptone water (BPW), well homogenized and filtered through cheesecloth. The filtrate was used to simulate natural egg contamination with fecal microorganisms.For the experimental contamination, eggs were immersed in fecal suspension for 60min, in plastic bags, and then allowed to dry in a laminar flow chamber for 2h<a class="elsevierStyleCrossRef" href="#bib0245">14</a>.QIE application for egg disinfectionA stock solution of 1% QIE in sterilized water was prepared. Contaminated eggs (previously immersed in the fecal suspension) were dipped in the disinfection solution for 15, 30 and 60min, then subjected to microbiological analysis. Decontaminated and control eggs (uncontaminated) were individually immersed in sterile BPW (50ml/each egg), well shaken, serially diluted and 0.1ml from the BPW dilutions were spread on appropriate agar media (See below) to count the viable colonies after incubation for each examined microbial group.Each group for microbial examination contained five eggs and their mean results were calculated.Microbiological examinationsDifferent microbial analyses were conducted according to the reference test methods of the British Standards Institution (BSI) to evaluate the effectiveness of QIE as a natural antimicrobial and disinfection agent for chicken eggs, as follows:<ul class="elsevierStyleList" id="lis0005"><li class="elsevierStyleListItem" id="lsti0005">-Enumeration of total aerobic microorganisms, according to ISO 4833:2003.</li><li class="elsevierStyleListItem" id="lsti0010">-Enumeration of molds and yeasts, according to ISO 21527-1:2008.</li><li class="elsevierStyleListItem" id="lsti0015">-Enumeration of E. coli, according to ISO 16649-2:2001.</li><li class="elsevierStyleListItem" id="lsti0020">-Detection and enumeration of Enterobacteriaceae, according to ISO 21528-2:2004.</li><li class="elsevierStyleListItem" id="lsti0025">-Enumeration of coagulase positive staphylococci and S. aureus, according to ISO 6888-1:1999.</li></ul>Quantitative determination of QIE phytochemicalsThe phytochemical analysis of QIE was conducted in the Food Chemistry Lab., Food Technology Research Institute, National Research Center, Giza, Egypt. The quantification of phenolic contents in QIE was carried out according to the method illustrated by Spigno et al.<a class="elsevierStyleCrossRef" href="#bib0315">28</a>, whereas flavonoid contents were determined according to Mattila et al.<a class="elsevierStyleCrossRef" href="#bib0280">21</a>, using an HPLC system coupled with diode array detection (HPLC-DAD) (Hewlett-Packard, Series-1050, Palo Alto, CA).Scanning electron microscopy imagingThe micrographs illustrating morphological alterations in S. aureus bacterial cells were captured using scanning electron microscopy imaging (SEM; Hitachi S-500, Tokyo, Japan) after treatment with QIE<a class="elsevierStyleCrossRef" href="#bib0275">20</a>. The bacterial cells were firstly fixed using a primary fixative solution containing 2% paraformaldehyde in 0.1M Na-Cacodylate buffer and 2.5% glutaraldehyde at pH 7.3 for 30min. The fixed samples were repeatedly rinsed with ultrapure water, and were then dehydrated using a series of ethanol concentrations (10, 30, 50, 70, 90 and 100%). The critical point dryer (Tousimis, Rockville, MD, USA) was then used for immediate drying of the dehydrated samples, then they were sputter-coated with gold/palladium after mounting onto SEM stubs. The electron micrographs were captured, at 50kV and 8000×, for the control samples and after 3 and 6h from the exposure to QIE; the captured sections were chosen depending on the morphological alteration in treated bacterial cells.ResultsThe antimicrobial activity of QIE against the examined microbial strains is shown in <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a> and was evidenced against the entire species, using both the quantitative (MIC) and qualitative (ZOI) assays. It could be claimed that the most sensitive strain to QIE activity was S. aureus, whereas the most resistant one was S. Typhimurium. With regard to microbial count reduction, after exposure to the corresponding MICs from QIE, it was recorded that the microbial viability decreased to 57.4–69.8%, after 1h from exposure, and to less than 4.1%, after QIE exposure for 5h. Only 1.2% from exposed S. aureus cells could survive after 5h of treatment with QIE.<elsevierMultimedia ident="tbl0005"></elsevierMultimedia>The consequence of eggshell decontamination through immersion in 1% QIE solution on the count of contaminating microorganisms is shown in <a class="elsevierStyleCrossRef" href="#fig0005">Figure 1</a>. The number of all examined microbial groups severely decreased after immersion in QIE and the count decrement continued with the prolongation of the immersion period. S. aureus was the most sensitive group to the sterilization action of QIE. Both E. coli and S. aureus were entirely inhibited after 60min of immersion in QIE solution, whereas the remaining percentage of viable cells were 1.2, 2.5 and 0.3% for the total aerobic colony count, yeast & molds and Enterobacteriaceae groups, respectively, after the same immersion time.<elsevierMultimedia ident="fig0005"></elsevierMultimedia>The biochemical analysis of QIE content from phytochemical constituents (<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>) revealed that the extract was very rich in its contents of phenolic compounds. The main phenolic compound in the QIE was p-hydroxybenzoic acid (PHBA), with a concentration of 7.45% followed by pyrogallol, catechol, caffeine, catechein, e-vanillic acid and 3-hydroxytyrosol with percentages of 7.17, 6.70, 2.17, 1.56, 1.50 and 1.04%, respectively. On the other hand, the lowest concentrations of QIE phenolic constituents were recorded for cinnamic, p-Coumaric, gallic acids and resveratrol, respectively. The main flavonoid compounds in QIE were naringin and rutin with a concentration of 123.2 and 103.3ppm, whereas the lowest concentrations of flavonoid compounds were for 7-hydrohyflavone and hispertin, with 3.5 and 4.7ppm, respectively.<elsevierMultimedia ident="tbl0010"></elsevierMultimedia>The consequence of QIE exposure on the morphology and viability of S. aureus cells is shown in <a class="elsevierStyleCrossRef" href="#fig0010">Figure 2</a>. The captured micrographs of untreated (control) bacterial cells showed that they had a normal, unified and smooth structure (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>A). After 3h of exposure to QIE, the effect was remarkably strong on cell morphology (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>B); most cells were lysed and their interior contents released, the remaining intact cells had enlarged and buffy walls with notable initiation of lysis. Upon completion of the QIE exposure period (after 6h), all S. aureus cells became completely lysed and ruptured; the only observable materials were cell wall residues and the interior cell components released (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>C).<elsevierMultimedia ident="fig0010"></elsevierMultimedia>DiscussionPlants ordinarily protect themselves from invaders and microorganisms via the production of secondary metabolites, which generally represent miscellaneous arrays derived from alkaloid, phenylpropanoid, isoprenoid, and fatty acid/polyketide pathways<a class="elsevierStyleCrossRef" href="#bib0250">15</a>; therefore, these are the main reasons for screening plants as potential sources for antimicrobial agents<a class="elsevierStyleCrossRef" href="#bib0225">10</a>. The antibacterial power of QIE was strong against Gram positive bacteria such as S. aureus compared to its action against treated Gram negative bacterial strains; a fact that was confirmed by ZOI diameters and the required MIC values. Accordant results were previously reported from other studies, which indicated that Gram positive bacteria are generally more susceptible to be inhibited by plant extracts than Gram negative strains<a class="elsevierStyleCrossRef" href="#bib0200">5</a>. The alteration in bacterial cell wall composition could explain the variation in microbial sensitivity to QIE or other plant extracts<a class="elsevierStyleCrossRef" href="#bib0230">11</a>.The applied solvent in this study for the extraction of bioactive compounds in Q. infectoria, contained 70% ethanol and 30% water. It was reported that the usage of alcoholic solvents is commonly recommended for the extraction of phenolics from natural origins because they can yield higher amounts of total extract compared with other types of solvents<a class="elsevierStyleCrossRef" href="#bib0315">28</a>.As tannins are the major compounds in QIE, which is soluble in water, the used solvent had a portion of water to dissolve the high amounts of total tannin contents<a class="elsevierStyleCrossRef" href="#bib0180">1</a>.Medicinal plants have been recurrently applied in many nutritional, pharmaceutical, medicinal and health promoting fields; this ethnopharmacological usage confidently warrants their compatibility and biosafety for man<a class="elsevierStyleCrossRef" href="#bib0200">5</a>. Many traditional and modern food applications were reported for Q. infectoria powders and extracts<a class="elsevierStyleCrossRef" href="#bib0355">18</a>, which could indicate the potential biosafety of nutgalls for human uses.The application of QIE for disinfection of eggshells exhibited powerful antimicrobial activity against contaminating microbial groups; which could be correlated with the high content of QIE from bioactive compounds<a class="elsevierStyleCrossRef" href="#bib0235">12</a>. It was affirmed that many flavonoids and phenolics, which are contained with high percentages in QIE, have a potent antimicrobial and antioxidant activities<a class="elsevierStyleCrossRefs" href="#bib0240">13,26</a>; the combination of these functional compounds is supposed to strengthen their action.Oak galls arise because of tree attacks by insects, thus they contain many defence phytochemicals. This characteristic could explain the wide variety of bioactive compounds found in Q. infectoria extract. It was reported that intact plants might include many bioactive compounds, e.g. glycosides, flavonols, alkaloids, flavones, lactones, organic acids, phenolic compounds and protein-like compounds, whereas other antimicrobial compounds, e.g. isothiocyanates phytoalexins, phenolic compounds and sulfoxides may be found in post-infection plants<a class="elsevierStyleCrossRef" href="#bib0270">19</a>.The highest concentration of phenolic compounds in QIE was reported for p-hydroxybenzoic acid (74474ppm), which was reported to have a powerful antimicrobial activity against many microbial strains, and this was also reported for vanillic, caffeic and ferulic acids<a class="elsevierStyleCrossRef" href="#bib0285">22</a>.From the detected phenolic compounds with high concentration in QIE, pyrogallol and catechol (the allelochemicals that belong to plant-synthesized phenolic compounds) exhibited concentrations of 71666 and 66966ppm, respectively. The antimicrobial activities of both pyrogallol and catechol were confirmed against many bacterial and fungal strains<a class="elsevierStyleCrossRef" href="#bib0260">17</a>.Phenolic allelochemicals are assumed to serve as defensive agents against microbial phytopathogens and to act as signal molecules in the interactions between plants with pathogens<a class="elsevierStyleCrossRef" href="#bib0255">16</a>.With regard to flavonoid content in QIE, it was reported that many flavonoid compounds, e.g. rosmarinic acid, could have antimicrobial potential against a wide variety of microorganisms<a class="elsevierStyleCrossRef" href="#bib0195">4</a>.Tannin content in QIE is typically high and contains both the hydrolysable and condensed types<a class="elsevierStyleCrossRef" href="#bib0340">33</a>. Both tannin types were used for the treatment of many diseases, especially the hydrolysable tannins, which were more medicinally applied as antifungal and antibacterial agents<a class="elsevierStyleCrossRef" href="#bib0250">15</a>; this could be a further explanation for the antimicrobial activity of QIE<a class="elsevierStyleCrossRef" href="#bib0295">24</a>.S. aureus was selected as a model organism to elucidate the antimicrobial action of QIE using scanning electron microscopy, because it was recorded in the study as the most sensitive strain to the extract, using the different antibacterial assays. Thus, it could be expected to exhibit various explanations for QIE modes of action, through SEM imaging.With regard to the captured micrographs of S. aureus cells treated with QIE (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>), it could be assumed that some potential bioactive compound(s) in QIE may have a metabolic interference in bacterial growth, development or function.From the alteration in bacterial morphology after treatment with QIE for an extended duration, it could be suggested that the extract has a time-dependent killing action. The QIE mechanism of action could also be thought to depend on the degradation of bacterial cell walls, destruction of cytoplasmic membrane proteins, leakage of cell contents, coagulation of cytoplasm, reduction in the proton motive force or binding with some synthesis proteins<a class="elsevierStyleCrossRefs" href="#bib0180">1,12</a>.It was suggested that extracts of medicinal plants with high tannin content, e.g. QIE, target the enzymes involved in cell wall synthesis of resistant S. aureus strains<a class="elsevierStyleCrossRef" href="#bib0185">2</a>.The current study could serve as a starting point for further investigations concerning the antimicrobial action, application and biosafety of individual/combined purified compounds in QIE.From the results achieved in this study, it can be concluded that oak gall (Q. infectoria) extract has antimicrobial activity, which can be applied as a natural disinfectant to protect chicken eggs from microbial contamination.FundingThere are no funding sources to declare.Conflict of interestThere are not any conflicts of interest." "textoCompletoSecciones" => array:1 [ "secciones" => array:11 [ 0 => array:3 [ "identificador" => "xres1113360" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec1051152" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres1113359" "titulo" => "Resumen" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0010" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec1051153" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 5 => array:3 [ "identificador" => "sec0010" "titulo" => "Materials and methods" "secciones" => array:8 [ 0 => array:2 [ "identificador" => "sec0015" "titulo" => "Oak gall extract preparation" ] 1 => array:2 [ "identificador" => "sec0020" "titulo" => "Microbial strains" ] 2 => array:2 [ "identificador" => "sec0025" "titulo" => "Determination of extract antimicrobial activity" ] 3 => array:2 [ "identificador" => "sec0030" "titulo" => "Experimental infection of eggs" ] 4 => array:2 [ "identificador" => "sec0035" "titulo" => "QIE application for egg disinfection" ] 5 => array:2 [ "identificador" => "sec0040" "titulo" => "Microbiological examinations" ] 6 => array:2 [ "identificador" => "sec0045" "titulo" => "Quantitative determination of QIE phytochemicals" ] 7 => array:2 [ "identificador" => "sec0050" "titulo" => "Scanning electron microscopy imaging" ] ] ] 6 => array:2 [ "identificador" => "sec0055" "titulo" => "Results" ] 7 => array:2 [ "identificador" => "sec0060" "titulo" => "Discussion" ] 8 => array:2 [ "identificador" => "sec0065" "titulo" => "Funding" ] 9 => array:2 [ "identificador" => "sec0070" "titulo" => "Conflict of interest" ] 10 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2017-05-02" "fechaAceptado" => "2017-12-09" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec1051152" "palabras" => array:5 [ 0 => "Antibacterial" 1 => "Disinfection" 2 => "Mode of action" 3 => "Natural" 4 => "Quercus infectoria" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec1051153" "palabras" => array:5 [ 0 => "Antibacteriano" 1 => "Desinfección" 2 => "Modo de acción" 3 => "Natural" 4 => "Quercus infectoria" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "Egg contamination with microbial pathogens is an enduring worldwide concern. Natural products are frequently recommended as ideal alternatives to substitute synthetic and chemical antimicrobials. Oak galls (Quercus infectoria) are aberrant growths on oak trees that have many medicinal and pharmaceutical applications. Q. infectoria extract (QIE) antimicrobial action was assessed against many microbial species, and used for eggshell decontamination. QIE antimicrobial activity was evidenced against Staphylococcus aureus, Escherichia coli, Pseudomonas aeruginosa, Salmonella Typhimurium and Candida albicans, using different assay methods. Disinfection of eggshell microbial contamination, by immersion in 1% QIE solution, sharply reduced total colony count, yeasts and molds, Enterobacteriaceae. E. coli and S. aureus were completely inhibited after 60min of immersion in QIE. QIE biochemical analysis revealed elevated contents of phenolic and flavonoid compounds. The captured micrographs of S. aureus cells treated with QIE showed strong alterations in cell morphology; cells were entirely lysed and ruptured after 6h of treatment. QIE can be recommended as an effective and natural disinfectant for decontaminating eggshells from pathogenic microorganisms." ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "La contaminación de huevos con patógenos microbianos es un problema constante en todo el mundo. Con frecuencia se recomiendan diversos productos naturales como alternativas ideales para sustituir a los antimicrobianos sintéticos. Las agallas de roble (Quercus infectoria) son de crecimiento aberrante en los robles y tienen muchas aplicaciones medicinales y farmacéuticas. Se evaluó la acción antimicrobiana del extracto de Quercus infectoria (QIE) contra varias especies microbianas y también este se aplicó para la descontaminación de cáscaras de huevo. La actividad antimicrobiana del extracto de QIE se evidenció en relación con Staphylococcus aureus, Escherichia coli, Pseudomonas aeruginosa, Salmonella typhimurium y Candida albicans, utilizando diferentes métodos de ensayo. La inmersión de las cáscaras de huevo en extracto de QIE al 1% logró una fuerte reducción del recuento total de colonias, de levaduras y de mohos, y de miembros de Enterobacteriaceae. La inmersión durante 60min inhibió completamente el desarrollo de E. coli y S. aureus. El análisis bioquímico del extracto de QIE reveló que este tiene un contenido elevado de compuestos fenólicos y de flavonoides. Se documentó mediante micrografías la presencia de grandes alteraciones en la morfología celular de S. aureus tras la exposición al extracto de QIE: las células se lisaron completamente y se rompieron después de 6h de tratamiento. El extracto de QIE se puede recomendar como un desinfectante eficaz y natural para descontaminar cáscaras de huevos de microorganismos patógenos." ] ] "multimedia" => array:4 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1750 "Ancho" => 2333 "Tamanyo" => 438211 ] ] "descripcion" => array:1 [ "en" => "Reduction in eggshell-contaminating microorganisms after different exposure times to Quercus infectoria extract. *Mean of 5 replicates. *QIE concentration of 1%." ] ] 1 => array:7 [ "identificador" => "fig0010" "etiqueta" => "Figure 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 2295 "Ancho" => 1000 "Tamanyo" => 294238 ] ] "descripcion" => array:1 [ "en" => "Scanning electron micrographs of treated Staphylococcus aureus cells with Quercus infectoria extract after different exposure times. (A) Control, (B) after 3h and (C) after 6h." ] ] 2 => array:8 [ "identificador" => "tbl0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at1" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:2 [ "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Examined microorganisms \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">ZOI \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">MIC \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Count reduction 1 (%)<a class="elsevierStyleCrossRef" href="#tblfn0005">a</a> \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Count reduction 2 (%)<a class="elsevierStyleCrossRef" href="#tblfn0005">a</a> \t\t\t\t\t\t\n \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Escherichia coli ATCC 25922 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">21.4 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.625 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">30.2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">95.9 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Salmonella Typhimurium ATCC-23852 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">19.3 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.250 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">41.5 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">96.2 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Pseudomonas aeruginosa ATCC-25006 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">24.1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.625 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">36.4 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">97.0 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Staphylococcus aureus ATCC-25923 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">24.3 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.313 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">40.2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">98.8 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Candida albicans ATCC-10231 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">25.8 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.250 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">42.6 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">97.6 \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1903390.png" ] ] ] "notaPie" => array:1 [ 0 => array:3 [ "identificador" => "tblfn0005" "etiqueta" => "a" "nota" => "Count reduction was calculated as a mean of triplicates after 1h (1) and 5h (2) from exposure to Q. infectoria extract at each corresponding MICs." ] ] ] "descripcion" => array:1 [ "en" => "Antimicrobial activity of Quercus infectoria extract measured qualitatively as zone of inhibition diameter (ZOI, mm) and quantitatively as minimal inhibitory concentrations (MIC, mg/ml)." ] ] 3 => array:8 [ "identificador" => "tbl0010" "etiqueta" => "Table 2" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at2" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:1 [ "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head " colspan="4" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Phytochemical constituents</th></tr><tr title="table-row"><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Phenolic compounds \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Concentration (ppm) \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Flavonoid compounds \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Concentration (ppm) \t\t\t\t\t\t\n \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">p-Hydroxybenzoic \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">74473.96 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Naringin \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">123.22 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Pyrogallol \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">71666.14 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Rutin \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">103.25 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Catechol \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">66966.37 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Rosmarinic \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">16.33 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Caffeine \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">21676.51 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Quercetrin \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">89.82 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Catechein \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">15622.42 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Quercetin \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">14.27 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">e-Vanillic \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">15012.16 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Hispertin \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">4.66 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">3-Hydroxytyrosol \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">10384.97 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">7-Hydrohyflavone \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3.50 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Vanillic \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">9518.89 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Chlorogenic \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">8887.12 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Caffeic \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">7667.85 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Protocatchuic \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3768.09 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Iso-ferulic \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1928.71 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Benzoic \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1414.21 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Ellagic \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1146.86 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Alpha-Coumaric \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">803.21 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Ferulic \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">751.61 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Coumarin \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">557.30 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">4-Amino-Benzoic \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">495.97 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Resveratrol \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">469.84 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Gallic \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">364.76 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">p-Coumaric \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">171.26 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Cinnamic \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">49.18 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1903389.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Biochemical analysis of phytochemical constituents in Quercus infectoria extract." ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0015" "bibliografiaReferencia" => array:35 [ 0 => array:3 [ "identificador" => "bib0180" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "The potential of aqueous and acetone extracts of galls of Quercus infectoria as antibacterial agents" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:2 [ 0 => "D.F. 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Aplicación de un extracto de Quercus infectoria como agente antimicrobiano natural para la desinfección de huevos de gallina

Ahmed A. Tayela,

Corresponding author

tayel_ahmad@yahoo.com

Corresponding author.

, Mahmoud A. El-Sedfyb, Ahmed I. Ibrahimb, Shaaban H. Moussab,c

a Faculty of Aquatic and Fisheries Sciences, Kafrelsheikh University, Kafr-Elsheikh, Egypt

b Genetic Engineering and Biotechnology Research Institute, University of Sadat City, El-Sadat City, Egypt

c College of Science and Humanitarian Studies, Shaqra University, Qwaieah, Saudi Arabia

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    "cabecera" => "<span class="elsevierStyleTextfn">Original article</span>"
    "titulo" => "Application of <span class="elsevierStyleItalic">Quercus infectoria</span> extract as a natural antimicrobial agent for chicken egg decontamination"
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        "titulo" => "Aplicaci&#243;n de un extracto de <span class="elsevierStyleItalic">Quercus infectoria</span> como agente antimicrobiano natural para la desinfecci&#243;n de huevos de gallina"
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          "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Reduction in eggshell-contaminating microorganisms after different exposure times to <span class="elsevierStyleItalic">Quercus infectoria</span> extract&#46; &#42;Mean of 5 replicates&#46; &#42;QIE concentration of 1&#37;&#46;</p>"
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Food preservation is a challenging issue faced by scientists&#44; industry overseers&#44; health observers and regular customers&#46; Food could be decontaminated and preserved using specific compounds&#44; <span class="elsevierStyleItalic">e&#46;g&#46;</span> preservatives or antimicrobials&#44; which are defined as the added compounds that have the ability to kill or hinder microbial growth in foods<a class="elsevierStyleCrossRef" href="#bib0205"><span class="elsevierStyleSup">6</span></a>&#46;</p><p id="par0010" class="elsevierStylePara elsevierViewall">Microbial contamination of eggs with pathogenic microorganisms is a serious health concern worldwide&#46; Eggshells may be contaminated with microorganisms at different industrial stages&#44; <span class="elsevierStyleItalic">e&#46;g&#46;</span> production&#44; processing&#44; preparation and packaging&#46; Contamination and microbial transmission may be &#8220;vertical&#8221;&#44; during egg formation in the ovaries&#44; or &#8220;horizontal&#8221;&#44; through egg exposure to the surrounded contaminated environment<a class="elsevierStyleCrossRef" href="#bib0215"><span class="elsevierStyleSup">8</span></a>&#46; The correlation between the average of eggshell contamination and penetrating microbial pathogens into the egg contents was reported in many previous investigations<a class="elsevierStyleCrossRefs" href="#bib0220"><span class="elsevierStyleSup">9&#44;23</span></a>&#46;</p><p id="par0015" class="elsevierStylePara elsevierViewall">Although there are many approved chemical food disinfectants and preservatives from international regulatory agencies&#44; to be applied as food antimicrobials&#44; there is a strong need for finding more effective agents originated from natural sources<a class="elsevierStyleCrossRefs" href="#bib0325"><span class="elsevierStyleSup">30&#44;31&#44;35</span></a>&#46; The principal advantages of the application of natural disinfectants and antimicrobials are their biodegradability&#44; high biosafety level&#44; wide spectrum and non-accumulating properties<a class="elsevierStyleCrossRefs" href="#bib0205"><span class="elsevierStyleSup">6&#44;7&#44;33</span></a>&#46;</p><p id="par0020" class="elsevierStylePara elsevierViewall">Many reports provided strong indications that the extracts of medicinal plant could be ideal sources for producing new antimicrobial compounds&#44; especially against antibiotic-resistant strains<a class="elsevierStyleCrossRefs" href="#bib0200"><span class="elsevierStyleSup">5&#44;11&#44;29</span></a>&#46;</p><p id="par0025" class="elsevierStylePara elsevierViewall">Oak galls &#40;<span class="elsevierStyleItalic">Quercus infectoria</span>&#41; are abnormal round-shaped growths&#44; which may appear on young oak tree branches<a class="elsevierStyleCrossRef" href="#bib0310"><span class="elsevierStyleSup">27</span></a>&#46; Gall powder and its extracts were traditionally used to treat many disorders&#44; diseases and symptoms&#44; including menorrhagia&#44; dysentery&#44; diarrhea&#44; internal hemorrhages&#44; gonorrhea&#44; tonsillitis&#44; and impetigo<a class="elsevierStyleCrossRef" href="#bib0190"><span class="elsevierStyleSup">3</span></a>&#46; Pharmacologically&#44; it was suggested that galls have potent bioactivities&#44; <span class="elsevierStyleItalic">e&#46;g&#46;</span> antioxidant&#44; antibacterial&#44; antifungal&#44; antiviral&#44; larvicidal&#44; antiamoebic&#44; antidiabetic&#44; anti-inflammatory&#44; antivenin&#44; and wound healing<a class="elsevierStyleCrossRefs" href="#bib0355"><span class="elsevierStyleSup">18&#44;25&#44;32</span></a>&#46; Gall applications&#44; in food-related sectors&#44; were also reported after being washed with running water to exclude bitter tannins before cooking&#46; After that&#44; galls could be powdered and applied as thickening agents in stews&#44; or used as cereal supplements for making bread&#59; nutgall powder and extract can be also used as a coffee substitute&#44; <span class="elsevierStyleItalic">e&#46;g&#46;</span> as tea or herbal drink for health promotion<a class="elsevierStyleCrossRef" href="#bib0355"><span class="elsevierStyleSup">18</span></a>&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">Therefore&#44; the current study was designed to evaluate <span class="elsevierStyleItalic">Q&#46; infectoria</span> extract as a potential antimicrobial agent for decontaminating eggshells and to analyze its possible antimicrobial mode of action&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Materials and methods</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Oak gall extract preparation</span><p id="par0035" class="elsevierStylePara elsevierViewall">Oak galls&#44; <span class="elsevierStyleItalic">Q&#46; infectoria</span> Olivier &#40;Fagaceae&#41;&#44; were obtained from the Medicinal and Aromatic Plants Research Department&#44; Agricultural Research Center&#44; Giza&#44; Egypt&#46; Galls were dried with hot air at 45<span class="elsevierStyleHsp" style=""></span>&#176;C for 24<span class="elsevierStyleHsp" style=""></span>h&#44; then dried materials were powdered using an electrical grinder and the powder was sieved to get &#8764;60<span class="elsevierStyleHsp" style=""></span>mesh particle size&#46; Two hundred grams of gall powder were immersed in 1<span class="elsevierStyleHsp" style=""></span>l of 70&#37; ethanol and agitated at 230<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">g</span> for 6<span class="elsevierStyleHsp" style=""></span>h&#44; using a rotary shaker&#46; QIE was filtered in a Buchner funnel through filter papers&#44; Whatman No&#46; 41&#44; to eliminate the plant particles&#44; which were re-extracted with 500<span class="elsevierStyleHsp" style=""></span>ml of the solvent and filtered and the total extracts were combined and subjected to flash evaporation at reduced pressure &#40;B&#252;chi&#44; Flavil&#44; Switzerland&#41; at 40<span class="elsevierStyleHsp" style=""></span>&#176;C to discard about 90&#37; of solvent till constant weight was attained&#46; The final dry extract was further dried under vacuum in a desiccator&#44; weighed and powdered&#46; QIE powder was then suspended in distilled water&#44; by vigorous agitation at 45<span class="elsevierStyleHsp" style=""></span>&#176;C&#44; to reach a final concentration of 10&#37; &#40;w&#47;v&#41;&#46; Finally&#44; extract solution was sterilized using a syringe filter &#40;0&#46;22<span class="elsevierStyleHsp" style=""></span>&#956;m pore size&#44; sterilized&#41; and kept at 4<span class="elsevierStyleHsp" style=""></span>&#176;C&#44; in sterile dark bottles&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Microbial strains</span><p id="par0040" class="elsevierStylePara elsevierViewall">Different microbial strains were used for examining the antimicrobial activity of QIE&#58; <span class="elsevierStyleItalic">Staphylococcus aureus</span> ATCC 25923&#44; <span class="elsevierStyleItalic">Escherichia coli</span> ATCC 25922&#44; <span class="elsevierStyleItalic">Pseudomonas aeruginosa</span> ATCC 25006&#44; <span class="elsevierStyleItalic">Salmonella</span> Typhimurium ATCC 23852&#44; and <span class="elsevierStyleItalic">Candida albicans</span> ATCC 10231&#46; The bacterial strains were propagated at 37<span class="elsevierStyleHsp" style=""></span>&#176;C in nutrient broth &#40;NB&#41; or nutrient agar &#40;NA&#41; under aerobic conditions&#44; whereas <span class="elsevierStyleItalic">C&#46; albicans</span> was grown in yeast malt broth &#40;YMB&#41; and maintained on yeast malt agar &#40;YMA&#41;&#46; All microbial media were purchased from Difco Lab&#46;&#44; Detroit&#44; MI&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Determination of extract antimicrobial activity</span><p id="par0045" class="elsevierStylePara elsevierViewall">The antimicrobial activity of QIE was qualitatively and quantitatively assessed&#44; by two different determinations&#58; zone of growth inhibition &#40;ZOI&#41;&#44; using the disc diffusion assay&#44; and the determination of minimal inhibitory concentrations &#40;MIC&#41; &#40;according to Tayel et al&#46;<a class="elsevierStyleCrossRef" href="#bib0345"><span class="elsevierStyleSup">34</span></a>&#41;&#44; using the suitable growth media for each microbial strain&#46; The reduction in microbial counts was evaluated after their treatment with each relevant MIC&#44; after 1<span class="elsevierStyleHsp" style=""></span>h and 5<span class="elsevierStyleHsp" style=""></span>h of the exposure&#44; using the standard plate count method for comparing&#46;</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Experimental infection of eggs</span><p id="par0050" class="elsevierStylePara elsevierViewall">One hundred and twenty five chicken eggs &#40;grade A&#44; 3&#8211;24<span class="elsevierStyleHsp" style=""></span>h old&#41; were obtained from the poultry farm &#8211; Kafrelsheikh University&#46; Eggs were firstly washed then sterilized through immersion in 1&#37; sodium hypochlorite solution for 30<span class="elsevierStyleHsp" style=""></span>min&#44; rewashed with sterilized water and allowed to dry in aseptic bags&#46; Chicken fecal samples &#40;80 samples weighed &#8764;1000<span class="elsevierStyleHsp" style=""></span>g&#41; were collected from farm litter&#44; aseptically transported to the laboratory and suspended in 4<span class="elsevierStyleHsp" style=""></span>l of buffered peptone water &#40;BPW&#41;&#44; well homogenized and filtered through cheesecloth&#46; The filtrate was used to simulate natural egg contamination with fecal microorganisms&#46;</p><p id="par0055" class="elsevierStylePara elsevierViewall">For the experimental contamination&#44; eggs were immersed in fecal suspension for 60<span class="elsevierStyleHsp" style=""></span>min&#44; in plastic bags&#44; and then allowed to dry in a laminar flow chamber for 2<span class="elsevierStyleHsp" style=""></span>h<a class="elsevierStyleCrossRef" href="#bib0245"><span class="elsevierStyleSup">14</span></a>&#46;</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">QIE application for egg disinfection</span><p id="par0060" class="elsevierStylePara elsevierViewall">A stock solution of 1&#37; QIE in sterilized water was prepared&#46; Contaminated eggs &#40;previously immersed in the fecal suspension&#41; were dipped in the disinfection solution for 15&#44; 30 and 60<span class="elsevierStyleHsp" style=""></span>min&#44; then subjected to microbiological analysis&#46; Decontaminated and control eggs &#40;uncontaminated&#41; were individually immersed in sterile BPW &#40;50<span class="elsevierStyleHsp" style=""></span>ml&#47;each egg&#41;&#44; well shaken&#44; serially diluted and 0&#46;1<span class="elsevierStyleHsp" style=""></span>ml from the BPW dilutions were spread on appropriate agar media &#40;See below&#41; to count the viable colonies after incubation for each examined microbial group&#46;</p><p id="par0065" class="elsevierStylePara elsevierViewall">Each group for microbial examination contained five eggs and their mean results were calculated&#46;</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Microbiological examinations</span><p id="par0070" class="elsevierStylePara elsevierViewall">Different microbial analyses were conducted according to the reference test methods of the British Standards Institution &#40;BSI&#41; to evaluate the effectiveness of QIE as a natural antimicrobial and disinfection agent for chicken eggs&#44; as follows&#58;<ul class="elsevierStyleList" id="lis0005"><li class="elsevierStyleListItem" id="lsti0005"><span class="elsevierStyleLabel">-</span><p id="par0075" class="elsevierStylePara elsevierViewall">Enumeration of total aerobic microorganisms&#44; according to ISO 4833&#58;2003&#46;</p></li><li class="elsevierStyleListItem" id="lsti0010"><span class="elsevierStyleLabel">-</span><p id="par0080" class="elsevierStylePara elsevierViewall">Enumeration of molds and yeasts&#44; according to ISO 21527-1&#58;2008&#46;</p></li><li class="elsevierStyleListItem" id="lsti0015"><span class="elsevierStyleLabel">-</span><p id="par0085" class="elsevierStylePara elsevierViewall">Enumeration of <span class="elsevierStyleItalic">E&#46; coli</span>&#44; according to ISO 16649-2&#58;2001&#46;</p></li><li class="elsevierStyleListItem" id="lsti0020"><span class="elsevierStyleLabel">-</span><p id="par0090" class="elsevierStylePara elsevierViewall">Detection and enumeration of <span class="elsevierStyleItalic">Enterobacteriaceae</span>&#44; according to ISO 21528-2&#58;2004&#46;</p></li><li class="elsevierStyleListItem" id="lsti0025"><span class="elsevierStyleLabel">-</span><p id="par0095" class="elsevierStylePara elsevierViewall">Enumeration of coagulase positive staphylococci and <span class="elsevierStyleItalic">S&#46; aureus</span>&#44; according to ISO 6888-1&#58;1999&#46;</p></li></ul></p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Quantitative determination of QIE phytochemicals</span><p id="par0100" class="elsevierStylePara elsevierViewall">The phytochemical analysis of QIE was conducted in the Food Chemistry Lab&#46;&#44; Food Technology Research Institute&#44; National Research Center&#44; Giza&#44; Egypt&#46; The quantification of phenolic contents in QIE was carried out according to the method illustrated by Spigno et al&#46;<a class="elsevierStyleCrossRef" href="#bib0315"><span class="elsevierStyleSup">28</span></a>&#44; whereas flavonoid contents were determined according to Mattila et al&#46;<a class="elsevierStyleCrossRef" href="#bib0280"><span class="elsevierStyleSup">21</span></a>&#44; using an HPLC system coupled with diode array detection &#40;HPLC-DAD&#41; &#40;Hewlett-Packard&#44; Series-1050&#44; Palo Alto&#44; CA&#41;&#46;</p></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Scanning electron microscopy imaging</span><p id="par0105" class="elsevierStylePara elsevierViewall">The micrographs illustrating morphological alterations in <span class="elsevierStyleItalic">S&#46; aureus</span> bacterial cells were captured using scanning electron microscopy imaging &#40;SEM&#59; Hitachi S-500&#44; Tokyo&#44; Japan&#41; after treatment with QIE<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">20</span></a>&#46; The bacterial cells were firstly fixed using a primary fixative solution containing 2&#37; paraformaldehyde in 0&#46;1<span class="elsevierStyleHsp" style=""></span>M Na-Cacodylate buffer and 2&#46;5&#37; glutaraldehyde at pH 7&#46;3 for 30<span class="elsevierStyleHsp" style=""></span>min&#46; The fixed samples were repeatedly rinsed with ultrapure water&#44; and were then dehydrated using a series of ethanol concentrations &#40;10&#44; 30&#44; 50&#44; 70&#44; 90 and 100&#37;&#41;&#46; The critical point dryer &#40;Tousimis&#44; Rockville&#44; MD&#44; USA&#41; was then used for immediate drying of the dehydrated samples&#44; then they were sputter-coated with gold&#47;palladium after mounting onto SEM stubs&#46; The electron micrographs were captured&#44; at 50<span class="elsevierStyleHsp" style=""></span>kV and 8000&#215;&#44; for the control samples and after 3 and 6<span class="elsevierStyleHsp" style=""></span>h from the exposure to QIE&#59; the captured sections were chosen depending on the morphological alteration in treated bacterial cells&#46;</p></span></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Results</span><p id="par0110" class="elsevierStylePara elsevierViewall">The antimicrobial activity of QIE against the examined microbial strains is shown in <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a> and was evidenced against the entire species&#44; using both the quantitative &#40;MIC&#41; and qualitative &#40;ZOI&#41; assays&#46; It could be claimed that the most sensitive strain to QIE activity was <span class="elsevierStyleItalic">S&#46; aureus</span>&#44; whereas the most resistant one was <span class="elsevierStyleItalic">S&#46;</span> Typhimurium&#46; With regard to microbial count reduction&#44; after exposure to the corresponding MICs from QIE&#44; it was recorded that the microbial viability decreased to 57&#46;4&#8211;69&#46;8&#37;&#44; after 1<span class="elsevierStyleHsp" style=""></span>h from exposure&#44; and to less than 4&#46;1&#37;&#44; after QIE exposure for 5<span class="elsevierStyleHsp" style=""></span>h&#46; Only 1&#46;2&#37; from exposed <span class="elsevierStyleItalic">S&#46; aureus</span> cells could survive after 5<span class="elsevierStyleHsp" style=""></span>h of treatment with QIE&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0115" class="elsevierStylePara elsevierViewall">The consequence of eggshell decontamination through immersion in 1&#37; QIE solution on the count of contaminating microorganisms is shown in <a class="elsevierStyleCrossRef" href="#fig0005">Figure 1</a>&#46; The number of all examined microbial groups severely decreased after immersion in QIE and the count decrement continued with the prolongation of the immersion period&#46; <span class="elsevierStyleItalic">S&#46; aureus</span> was the most sensitive group to the sterilization action of QIE&#46; Both <span class="elsevierStyleItalic">E&#46; coli</span> and <span class="elsevierStyleItalic">S&#46; aureus</span> were entirely inhibited after 60<span class="elsevierStyleHsp" style=""></span>min of immersion in QIE solution&#44; whereas the remaining percentage of viable cells were 1&#46;2&#44; 2&#46;5 and 0&#46;3&#37; for the total aerobic colony count&#44; yeast &#38; molds and <span class="elsevierStyleItalic">Enterobacteriaceae</span> groups&#44; respectively&#44; after the same immersion time&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0120" class="elsevierStylePara elsevierViewall">The biochemical analysis of QIE content from phytochemical constituents &#40;<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>&#41; revealed that the extract was very rich in its contents of phenolic compounds&#46; The main phenolic compound in the QIE was <span class="elsevierStyleItalic">p</span>-hydroxybenzoic acid &#40;PHBA&#41;&#44; with a concentration of 7&#46;45&#37; followed by pyrogallol&#44; catechol&#44; caffeine&#44; catechein&#44; e-vanillic acid and 3-hydroxytyrosol with percentages of 7&#46;17&#44; 6&#46;70&#44; 2&#46;17&#44; 1&#46;56&#44; 1&#46;50 and 1&#46;04&#37;&#44; respectively&#46; On the other hand&#44; the lowest concentrations of QIE phenolic constituents were recorded for cinnamic&#44; <span class="elsevierStyleItalic">p</span>-Coumaric&#44; gallic acids and resveratrol&#44; respectively&#46; The main flavonoid compounds in QIE were naringin and rutin with a concentration of 123&#46;2 and 103&#46;3<span class="elsevierStyleHsp" style=""></span>ppm&#44; whereas the lowest concentrations of flavonoid compounds were for 7-hydrohyflavone and hispertin&#44; with 3&#46;5 and 4&#46;7<span class="elsevierStyleHsp" style=""></span>ppm&#44; respectively&#46;</p><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><p id="par0125" class="elsevierStylePara elsevierViewall">The consequence of QIE exposure on the morphology and viability of <span class="elsevierStyleItalic">S&#46; aureus</span> cells is shown in <a class="elsevierStyleCrossRef" href="#fig0010">Figure 2</a>&#46; The captured micrographs of untreated &#40;control&#41; bacterial cells showed that they had a normal&#44; unified and smooth structure &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>A&#41;&#46; After 3<span class="elsevierStyleHsp" style=""></span>h of exposure to QIE&#44; the effect was remarkably strong on cell morphology &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>B&#41;&#59; most cells were lysed and their interior contents released&#44; the remaining intact cells had enlarged and buffy walls with notable initiation of lysis&#46; Upon completion of the QIE exposure period &#40;after 6<span class="elsevierStyleHsp" style=""></span>h&#41;&#44; all <span class="elsevierStyleItalic">S&#46; aureus</span> cells became completely lysed and ruptured&#59; the only observable materials were cell wall residues and the interior cell components released &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>C&#41;&#46;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Discussion</span><p id="par0130" class="elsevierStylePara elsevierViewall">Plants ordinarily protect themselves from invaders and microorganisms via the production of secondary metabolites&#44; which generally represent miscellaneous arrays derived from alkaloid&#44; phenylpropanoid&#44; isoprenoid&#44; and fatty acid&#47;polyketide pathways<a class="elsevierStyleCrossRef" href="#bib0250"><span class="elsevierStyleSup">15</span></a>&#59; therefore&#44; these are the main reasons for screening plants as potential sources for antimicrobial agents<a class="elsevierStyleCrossRef" href="#bib0225"><span class="elsevierStyleSup">10</span></a>&#46; The antibacterial power of QIE was strong against Gram positive bacteria such as <span class="elsevierStyleItalic">S&#46; aureus</span> compared to its action against treated Gram negative bacterial strains&#59; a fact that was confirmed by ZOI diameters and the required MIC values&#46; Accordant results were previously reported from other studies&#44; which indicated that Gram positive bacteria are generally more susceptible to be inhibited by plant extracts than Gram negative strains<a class="elsevierStyleCrossRef" href="#bib0200"><span class="elsevierStyleSup">5</span></a>&#46; The alteration in bacterial cell wall composition could explain the variation in microbial sensitivity to QIE or other plant extracts<a class="elsevierStyleCrossRef" href="#bib0230"><span class="elsevierStyleSup">11</span></a>&#46;</p><p id="par0135" class="elsevierStylePara elsevierViewall">The applied solvent in this study for the extraction of bioactive compounds in <span class="elsevierStyleItalic">Q&#46; infectoria</span>&#44; contained 70&#37; ethanol and 30&#37; water&#46; It was reported that the usage of alcoholic solvents is commonly recommended for the extraction of phenolics from natural origins because they can yield higher amounts of total extract compared with other types of solvents<a class="elsevierStyleCrossRef" href="#bib0315"><span class="elsevierStyleSup">28</span></a>&#46;</p><p id="par0140" class="elsevierStylePara elsevierViewall">As tannins are the major compounds in QIE&#44; which is soluble in water&#44; the used solvent had a portion of water to dissolve the high amounts of total tannin contents<a class="elsevierStyleCrossRef" href="#bib0180"><span class="elsevierStyleSup">1</span></a>&#46;</p><p id="par0145" class="elsevierStylePara elsevierViewall">Medicinal plants have been recurrently applied in many nutritional&#44; pharmaceutical&#44; medicinal and health promoting fields&#59; this ethnopharmacological usage confidently warrants their compatibility and biosafety for man<a class="elsevierStyleCrossRef" href="#bib0200"><span class="elsevierStyleSup">5</span></a>&#46; Many traditional and modern food applications were reported for <span class="elsevierStyleItalic">Q&#46; infectoria</span> powders and extracts<a class="elsevierStyleCrossRef" href="#bib0355"><span class="elsevierStyleSup">18</span></a>&#44; which could indicate the potential biosafety of nutgalls for human uses&#46;</p><p id="par0150" class="elsevierStylePara elsevierViewall">The application of QIE for disinfection of eggshells exhibited powerful antimicrobial activity against contaminating microbial groups&#59; which could be correlated with the high content of QIE from bioactive compounds<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">12</span></a>&#46; It was affirmed that many flavonoids and phenolics&#44; which are contained with high percentages in QIE&#44; have a potent antimicrobial and antioxidant activities<a class="elsevierStyleCrossRefs" href="#bib0240"><span class="elsevierStyleSup">13&#44;26</span></a>&#59; the combination of these functional compounds is supposed to strengthen their action&#46;</p><p id="par0155" class="elsevierStylePara elsevierViewall">Oak galls arise because of tree attacks by insects&#44; thus they contain many defence phytochemicals&#46; This characteristic could explain the wide variety of bioactive compounds found in <span class="elsevierStyleItalic">Q&#46; infectoria</span> extract&#46; It was reported that intact plants might include many bioactive compounds&#44; <span class="elsevierStyleItalic">e&#46;g&#46;</span> glycosides&#44; flavonols&#44; alkaloids&#44; flavones&#44; lactones&#44; organic acids&#44; phenolic compounds and protein-like compounds&#44; whereas other antimicrobial compounds&#44; <span class="elsevierStyleItalic">e&#46;g&#46;</span> isothiocyanates phytoalexins&#44; phenolic compounds and sulfoxides may be found in post-infection plants<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">19</span></a>&#46;</p><p id="par0160" class="elsevierStylePara elsevierViewall">The highest concentration of phenolic compounds in QIE was reported for <span class="elsevierStyleItalic">p</span>-hydroxybenzoic acid &#40;74<span class="elsevierStyleHsp" style=""></span>474<span class="elsevierStyleHsp" style=""></span>ppm&#41;&#44; which was reported to have a powerful antimicrobial activity against many microbial strains&#44; and this was also reported for vanillic&#44; caffeic and ferulic acids<a class="elsevierStyleCrossRef" href="#bib0285"><span class="elsevierStyleSup">22</span></a>&#46;</p><p id="par0165" class="elsevierStylePara elsevierViewall">From the detected phenolic compounds with high concentration in QIE&#44; pyrogallol and catechol &#40;the allelochemicals that belong to plant-synthesized phenolic compounds&#41; exhibited concentrations of 71<span class="elsevierStyleHsp" style=""></span>666 and 66<span class="elsevierStyleHsp" style=""></span>966<span class="elsevierStyleHsp" style=""></span>ppm&#44; respectively&#46; The antimicrobial activities of both pyrogallol and catechol were confirmed against many bacterial and fungal strains<a class="elsevierStyleCrossRef" href="#bib0260"><span class="elsevierStyleSup">17</span></a>&#46;</p><p id="par0170" class="elsevierStylePara elsevierViewall">Phenolic allelochemicals are assumed to serve as defensive agents against microbial phytopathogens and to act as signal molecules in the interactions between plants with pathogens<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">16</span></a>&#46;</p><p id="par0175" class="elsevierStylePara elsevierViewall">With regard to flavonoid content in QIE&#44; it was reported that many flavonoid compounds&#44; <span class="elsevierStyleItalic">e&#46;g&#46;</span> rosmarinic acid&#44; could have antimicrobial potential against a wide variety of microorganisms<a class="elsevierStyleCrossRef" href="#bib0195"><span class="elsevierStyleSup">4</span></a>&#46;</p><p id="par0180" class="elsevierStylePara elsevierViewall">Tannin content in QIE is typically high and contains both the hydrolysable and condensed types<a class="elsevierStyleCrossRef" href="#bib0340"><span class="elsevierStyleSup">33</span></a>&#46; Both tannin types were used for the treatment of many diseases&#44; especially the hydrolysable tannins&#44; which were more medicinally applied as antifungal and antibacterial agents<a class="elsevierStyleCrossRef" href="#bib0250"><span class="elsevierStyleSup">15</span></a>&#59; this could be a further explanation for the antimicrobial activity of QIE<a class="elsevierStyleCrossRef" href="#bib0295"><span class="elsevierStyleSup">24</span></a>&#46;</p><p id="par0185" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">S&#46; aureus</span> was selected as a model organism to elucidate the antimicrobial action of QIE using scanning electron microscopy&#44; because it was recorded in the study as the most sensitive strain to the extract&#44; using the different antibacterial assays&#46; Thus&#44; it could be expected to exhibit various explanations for QIE modes of action&#44; through SEM imaging&#46;</p><p id="par0190" class="elsevierStylePara elsevierViewall">With regard to the captured micrographs of <span class="elsevierStyleItalic">S&#46; aureus</span> cells treated with QIE &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#44; it could be assumed that some potential bioactive compound&#40;s&#41; in QIE may have a metabolic interference in bacterial growth&#44; development or function&#46;</p><p id="par0195" class="elsevierStylePara elsevierViewall">From the alteration in bacterial morphology after treatment with QIE for an extended duration&#44; it could be suggested that the extract has a time-dependent killing action&#46; The QIE mechanism of action could also be thought to depend on the degradation of bacterial cell walls&#44; destruction of cytoplasmic membrane proteins&#44; leakage of cell contents&#44; coagulation of cytoplasm&#44; reduction in the proton motive force or binding with some synthesis proteins<a class="elsevierStyleCrossRefs" href="#bib0180"><span class="elsevierStyleSup">1&#44;12</span></a>&#46;</p><p id="par0200" class="elsevierStylePara elsevierViewall">It was suggested that extracts of medicinal plants with high tannin content&#44; <span class="elsevierStyleItalic">e&#46;g&#46;</span> QIE&#44; target the enzymes involved in cell wall synthesis of resistant <span class="elsevierStyleItalic">S&#46; aureus</span> strains<a class="elsevierStyleCrossRef" href="#bib0185"><span class="elsevierStyleSup">2</span></a>&#46;</p><p id="par0205" class="elsevierStylePara elsevierViewall">The current study could serve as a starting point for further investigations concerning the antimicrobial action&#44; application and biosafety of individual&#47;combined purified compounds in QIE&#46;</p><p id="par0210" class="elsevierStylePara elsevierViewall">From the results achieved in this study&#44; it can be concluded that oak gall &#40;<span class="elsevierStyleItalic">Q&#46; infectoria</span>&#41; extract has antimicrobial activity&#44; which can be applied as a natural disinfectant to protect chicken eggs from microbial contamination&#46;</p></span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Funding</span><p id="par0215" class="elsevierStylePara elsevierViewall">There are no funding sources to declare&#46;</p></span><span id="sec0070" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Conflict of interest</span><p id="par0220" class="elsevierStylePara elsevierViewall">There are not any conflicts of interest&#46;</p></span></span>"
    "textoCompletoSecciones" => array:1 [
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          "identificador" => "xres1113360"
          "titulo" => "Abstract"
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              "identificador" => "abst0005"
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        1 => array:2 [
          "identificador" => "xpalclavsec1051152"
          "titulo" => "Keywords"
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          "titulo" => "Resumen"
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          "titulo" => "Palabras clave"
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        4 => array:2 [
          "identificador" => "sec0005"
          "titulo" => "Introduction"
        ]
        5 => array:3 [
          "identificador" => "sec0010"
          "titulo" => "Materials and methods"
          "secciones" => array:8 [
            0 => array:2 [
              "identificador" => "sec0015"
              "titulo" => "Oak gall extract preparation"
            ]
            1 => array:2 [
              "identificador" => "sec0020"
              "titulo" => "Microbial strains"
            ]
            2 => array:2 [
              "identificador" => "sec0025"
              "titulo" => "Determination of extract antimicrobial activity"
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            3 => array:2 [
              "identificador" => "sec0030"
              "titulo" => "Experimental infection of eggs"
            ]
            4 => array:2 [
              "identificador" => "sec0035"
              "titulo" => "QIE application for egg disinfection"
            ]
            5 => array:2 [
              "identificador" => "sec0040"
              "titulo" => "Microbiological examinations"
            ]
            6 => array:2 [
              "identificador" => "sec0045"
              "titulo" => "Quantitative determination of QIE phytochemicals"
            ]
            7 => array:2 [
              "identificador" => "sec0050"
              "titulo" => "Scanning electron microscopy imaging"
            ]
          ]
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        6 => array:2 [
          "identificador" => "sec0055"
          "titulo" => "Results"
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        7 => array:2 [
          "identificador" => "sec0060"
          "titulo" => "Discussion"
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          "identificador" => "sec0065"
          "titulo" => "Funding"
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          "titulo" => "References"
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    "fechaRecibido" => "2017-05-02"
    "fechaAceptado" => "2017-12-09"
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          "clase" => "keyword"
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          "palabras" => array:5 [
            0 => "Antibacterial"
            1 => "Disinfection"
            2 => "Mode of action"
            3 => "Natural"
            4 => "<span class="elsevierStyleItalic">Quercus infectoria</span>"
          ]
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            0 => "Antibacteriano"
            1 => "Desinfecci&#243;n"
            2 => "Modo de acci&#243;n"
            3 => "Natural"
            4 => "<span class="elsevierStyleItalic">Quercus infectoria</span>"
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        "titulo" => "Abstract"
        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Egg contamination with microbial pathogens is an enduring worldwide concern&#46; Natural products are frequently recommended as ideal alternatives to substitute synthetic and chemical antimicrobials&#46; Oak galls &#40;<span class="elsevierStyleItalic">Quercus infectoria</span>&#41; are aberrant growths on oak trees that have many medicinal and pharmaceutical applications&#46; <span class="elsevierStyleItalic">Q&#46; infectoria</span> extract &#40;QIE&#41; antimicrobial action was assessed against many microbial species&#44; and used for eggshell decontamination&#46; QIE antimicrobial activity was evidenced against <span class="elsevierStyleItalic">Staphylococcus aureus</span>&#44; <span class="elsevierStyleItalic">Escherichia coli</span>&#44; <span class="elsevierStyleItalic">Pseudomonas aeruginosa</span>&#44; <span class="elsevierStyleItalic">Salmonella</span> Typhimurium and <span class="elsevierStyleItalic">Candida albicans</span>&#44; using different assay methods&#46; Disinfection of eggshell microbial contamination&#44; by immersion in 1&#37; QIE solution&#44; sharply reduced total colony count&#44; yeasts and molds&#44; <span class="elsevierStyleItalic">Enterobacteriaceae</span>&#46; <span class="elsevierStyleItalic">E&#46; coli</span> and <span class="elsevierStyleItalic">S&#46; aureus</span> were completely inhibited after 60<span class="elsevierStyleHsp" style=""></span>min of immersion in QIE&#46; QIE biochemical analysis revealed elevated contents of phenolic and flavonoid compounds&#46; The captured micrographs of <span class="elsevierStyleItalic">S&#46; aureus</span> cells treated with QIE showed strong alterations in cell morphology&#59; cells were entirely lysed and ruptured after 6<span class="elsevierStyleHsp" style=""></span>h of treatment&#46; QIE can be recommended as an effective and natural disinfectant for decontaminating eggshells from pathogenic microorganisms&#46;</p></span>"
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        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">La contaminaci&#243;n de huevos con pat&#243;genos microbianos es un problema constante en todo el mundo&#46; Con frecuencia se recomiendan diversos productos naturales como alternativas ideales para sustituir a los antimicrobianos sint&#233;ticos&#46; Las agallas de roble &#40;<span class="elsevierStyleItalic">Quercus infectoria</span>&#41; son de crecimiento aberrante en los robles y tienen muchas aplicaciones medicinales y farmac&#233;uticas&#46; Se evalu&#243; la acci&#243;n antimicrobiana del extracto de <span class="elsevierStyleItalic">Quercus infectoria</span> &#40;QIE&#41; contra varias especies microbianas y tambi&#233;n este se aplic&#243; para la descontaminaci&#243;n de c&#225;scaras de huevo&#46; La actividad antimicrobiana del extracto de QIE se evidenci&#243; en relaci&#243;n con <span class="elsevierStyleItalic">Staphylococcus aureus</span>&#44; <span class="elsevierStyleItalic">Escherichia coli</span>&#44; <span class="elsevierStyleItalic">Pseudomonas aeruginosa</span>&#44; <span class="elsevierStyleItalic">Salmonella typhimurium</span> y <span class="elsevierStyleItalic">Candida albicans</span>&#44; utilizando diferentes m&#233;todos de ensayo&#46; La inmersi&#243;n de las c&#225;scaras de huevo en extracto de QIE al 1&#37; logr&#243; una fuerte reducci&#243;n del recuento total de colonias&#44; de levaduras y de mohos&#44; y de miembros de <span class="elsevierStyleItalic">Enterobacteriaceae</span>&#46; La inmersi&#243;n durante 60<span class="elsevierStyleHsp" style=""></span>min inhibi&#243; completamente el desarrollo de <span class="elsevierStyleItalic">E&#46; coli</span> y <span class="elsevierStyleItalic">S&#46; aureus</span>&#46; El an&#225;lisis bioqu&#237;mico del extracto de QIE revel&#243; que este tiene un contenido elevado de compuestos fen&#243;licos y de flavonoides&#46; Se document&#243; mediante micrograf&#237;as la presencia de grandes alteraciones en la morfolog&#237;a celular de <span class="elsevierStyleItalic">S&#46; aureus</span> tras la exposici&#243;n al extracto de QIE&#58; las c&#233;lulas se lisaron completamente y se rompieron despu&#233;s de 6<span class="elsevierStyleHsp" style=""></span>h de tratamiento&#46; El extracto de QIE se puede recomendar como un desinfectante eficaz y natural para descontaminar c&#225;scaras de huevos de microorganismos pat&#243;genos&#46;</p></span>"
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          "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Reduction in eggshell-contaminating microorganisms after different exposure times to <span class="elsevierStyleItalic">Quercus infectoria</span> extract&#46; &#42;Mean of 5 replicates&#46; &#42;QIE concentration of 1&#37;&#46;</p>"
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          "en" => "<p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Scanning electron micrographs of treated <span class="elsevierStyleItalic">Staphylococcus aureus</span> cells with <span class="elsevierStyleItalic">Quercus infectoria</span> extract after different exposure times&#46; &#40;A&#41; Control&#44; &#40;B&#41; after 3<span class="elsevierStyleHsp" style=""></span>h and &#40;C&#41; after 6<span class="elsevierStyleHsp" style=""></span>h&#46;</p>"
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                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Examined microorganisms&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">ZOI&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">MIC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Count reduction 1 &#40;&#37;&#41;<a class="elsevierStyleCrossRef" href="#tblfn0005"><span class="elsevierStyleSup">a</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Count reduction 2 &#40;&#37;&#41;<a class="elsevierStyleCrossRef" href="#tblfn0005"><span class="elsevierStyleSup">a</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Escherichia coli</span><br>ATCC 25922&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">21&#46;4&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;625&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">30&#46;2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">95&#46;9&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Salmonella</span> Typhimurium<br>ATCC-23852&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">19&#46;3&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;250&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">41&#46;5&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">96&#46;2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Pseudomonas aeruginosa</span><br>ATCC-25006&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">24&#46;1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;625&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">36&#46;4&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">97&#46;0&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Staphylococcus aureus</span><br>ATCC-25923&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">24&#46;3&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;313&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">40&#46;2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">98&#46;8&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Candida albicans</span><br>ATCC-10231&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">25&#46;8&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;250&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">42&#46;6&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">97&#46;6&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
              ]
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            0 => array:3 [
              "identificador" => "tblfn0005"
              "etiqueta" => "a"
              "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Count reduction was calculated as a mean of triplicates after 1<span class="elsevierStyleHsp" style=""></span>h &#40;1&#41; and 5<span class="elsevierStyleHsp" style=""></span>h &#40;2&#41; from exposure to <span class="elsevierStyleItalic">Q&#46; infectoria</span> extract at each corresponding MICs&#46;</p>"
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          ]
        ]
        "descripcion" => array:1 [
          "en" => "<p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">Antimicrobial activity of <span class="elsevierStyleItalic">Quercus infectoria</span> extract measured qualitatively as zone of inhibition diameter &#40;ZOI&#44; mm&#41; and quantitatively as minimal inhibitory concentrations &#40;MIC&#44; mg&#47;ml&#41;&#46;</p>"
        ]
      ]
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            "identificador" => "at2"
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              "tabla" => array:1 [
                0 => """
                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head  " colspan="4" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Phytochemical constituents</th></tr><tr title="table-row"><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Phenolic compounds&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Concentration &#40;ppm&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Flavonoid compounds&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Concentration &#40;ppm&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">p</span>-Hydroxybenzoic&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">74<span class="elsevierStyleHsp" style=""></span>473&#46;96&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Naringin&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">123&#46;22&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Pyrogallol&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">71<span class="elsevierStyleHsp" style=""></span>666&#46;14&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Rutin&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">103&#46;25&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Catechol&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">66<span class="elsevierStyleHsp" style=""></span>966&#46;37&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Rosmarinic&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">16&#46;33&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Caffeine&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">21<span class="elsevierStyleHsp" style=""></span>676&#46;51&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Quercetrin&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">89&#46;82&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Catechein&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">15<span class="elsevierStyleHsp" style=""></span>622&#46;42&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Quercetin&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">14&#46;27&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">e-Vanillic&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">15<span class="elsevierStyleHsp" style=""></span>012&#46;16&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Hispertin&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">4&#46;66&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">3-Hydroxytyrosol&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">10<span class="elsevierStyleHsp" style=""></span>384&#46;97&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">7-Hydrohyflavone&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">3&#46;50&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Vanillic&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">9518&#46;89&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Chlorogenic&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">8887&#46;12&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Caffeic&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">7667&#46;85&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Protocatchuic&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">3768&#46;09&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Iso-ferulic&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1928&#46;71&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Benzoic&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1414&#46;21&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Ellagic&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1146&#46;86&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Alpha-Coumaric&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">803&#46;21&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Ferulic&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">751&#46;61&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Coumarin&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">557&#46;30&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">4-Amino-Benzoic&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">495&#46;97&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Resveratrol&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">469&#46;84&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Gallic&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">364&#46;76&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">p</span>-Coumaric&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">171&#46;26&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Cinnamic&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">49&#46;18&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
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        "descripcion" => array:1 [
          "en" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">Biochemical analysis of phytochemical constituents in <span class="elsevierStyleItalic">Quercus infectoria</span> extract&#46;</p>"
        ]
      ]
    ]
    "bibliografia" => array:2 [
      "titulo" => "References"
      "seccion" => array:1 [
        0 => array:2 [
          "identificador" => "bibs0015"
          "bibliografiaReferencia" => array:35 [
            0 => array:3 [
              "identificador" => "bib0180"
              "etiqueta" => "1"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "The potential of aqueous and acetone extracts of galls of <span class="elsevierStyleItalic">Quercus infectoria</span> as antibacterial agents"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:2 [
                            0 => "D&#46;F&#46; Basri"
                            1 => "S&#46;H&#46; Fan"
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                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Revista" => array:5 [
                        "tituloSerie" => "Indian J Pharmacol"
                        "fecha" => "2005"
                        "volumen" => "37"
                        "paginaInicial" => "26"
                        "paginaFinal" => "29"
                      ]
                    ]
                  ]
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            1 => array:3 [
              "identificador" => "bib0185"
              "etiqueta" => "2"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Electron microscope study of gall extract from <span class="elsevierStyleItalic">Quercus infectoria</span> in combination with vancomycin against MRSA using post-antibiotic effect determination"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:4 [
                            0 => "D&#46;F&#46; Basri"
                            1 => "N&#46; Jaffar"
                            2 => "N&#46;M&#46; Zin"
                            3 => "S&#46;L&#46; Raj"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Revista" => array:5 [
                        "tituloSerie" => "Int J Pharmacol"
                        "fecha" => "2013"
                        "volumen" => "9"
                        "paginaInicial" => "150"
                        "paginaFinal" => "156"
                      ]
                    ]
                  ]
                ]
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            2 => array:3 [
              "identificador" => "bib0190"
              "etiqueta" => "3"
              "referencia" => array:1 [
                0 => array:1 [
                  "host" => array:1 [
                    0 => array:1 [
                      "LibroEditado" => array:3 [
                        "titulo" => "Pharmacognosy&#44; phytochemistry&#44; medicinal plants"
                        "edicion" => "2nd ed&#46;"
                        "serieFecha" => "1999"
                      ]
                    ]
                  ]
                ]
              ]
            ]
            3 => array:3 [
              "identificador" => "bib0195"
              "etiqueta" => "4"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Rosmarinic acid and its derivatives&#58; biotechnology and application"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:3 [
                            0 => "V&#46;P&#46; Bulgakov"
                            1 => "Y&#46;V&#46; Inyushkina"
                            2 => "S&#46;A&#46; Fedoreyev"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.3109/07388551.2011.596804"
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Article information

ISSN: 03257541
Original language: English

DOI:10.1016/j.ram.2017.12.003

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Year/Month	Html	Pdf	Total

2024 October	49	5	54
2024 September	101	26	127
2024 August	96	19	115
2024 July	92	4	96
2024 June	67	7	74
2024 May	57	5	62
2024 April	88	14	102
2024 March	101	15	116
2024 February	80	7	87
2024 January	70	6	76
2023 December	67	10	77
2023 November	98	6	104
2023 October	81	10	91
2023 September	73	1	74
2023 August	59	6	65
2023 July	79	3	82
2023 June	74	12	86
2023 May	141	43	184
2023 April	87	11	98
2023 March	58	5	63
2023 February	26	18	44
2023 January	19	7	26
2022 December	25	18	43
2022 November	31	10	41
2022 October	30	10	40
2022 September	38	12	50
2022 August	20	17	37
2022 July	21	14	35
2022 June	19	26	45
2022 May	27	9	36
2022 April	34	17	51
2022 March	32	19	51
2022 February	28	6	34
2022 January	58	10	68
2021 December	30	18	48
2021 November	42	8	50
2021 October	32	15	47
2021 September	29	15	44
2021 August	35	12	47
2021 July	23	12	35
2021 June	28	15	43
2021 May	20	10	30
2021 April	29	36	65
2021 March	25	42	67
2021 February	22	36	58
2021 January	38	43	81
2020 December	21	35	56
2020 November	21	27	48
2020 October	16	32	48
2020 September	10	29	39
2020 August	15	32	47
2020 July	8	22	30
2020 June	22	24	46
2020 May	18	31	49
2020 April	14	22	36
2020 March	20	34	54
2020 February	19	35	54
2020 January	18	68	86
2019 December	15	41	56
2019 November	14	21	35
2019 October	8	41	49
2019 September	20	24	44
2019 August	3	13	16
2019 July	20	25	45
2019 June	32	35	67
2019 May	103	51	154
2019 April	67	45	112
2019 March	13	50	63
2019 February	20	40	60
2019 January	22	27	49
2018 December	12	7	19
2018 November	4	12	16
2018 October	5	23	28
2018 September	15	8	23
2018 August	0	5	5
2018 July	0	10	10
2018 June	2	9	11
2018 May	1	322	323
2018 April	0	1	1

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