
==== Front
Microb Cell Fact
Microb Cell Fact
Microbial Cell Factories
1475-2859
BioMed Central London

39238019
2508
10.1186/s12934-024-02508-9
Research
Impeding microbial biofilm formation and Pseudomonas aeruginosa virulence genes using biologically synthesized silver Carthamus nanoparticles
Abdel-Fatah Sobhy S. 1
Mohammad Nasser H. 2
Elshimy Rana. 34
http://orcid.org/0000-0003-1784-101X
Mosallam Farag M. farag3m2012@gmail.com
farag.abomosalam@eaea.org.eg

1
1 https://ror.org/04hd0yz67 grid.429648.5 0000 0000 9052 0245 Drug Radiation Research Department, Drug Microbiology Lab, Biotechnology Division, National Center for Radiation Research and Technology (NCRRT), Egyptian Atomic Energy Authority, Cairo, Egypt
2 https://ror.org/04hd0yz67 grid.429648.5 0000 0000 9052 0245 Radiation Microbiology Department, National Center for Radiation Research and Technology (NCRRT), Egyptian Atomic Energy Authority (EAEA), Cairo, Egypt
3 Microbiology and Immunology, Egyptian Drug Authority, Cairo, Egypt
4 Microbiology and immunology, Faculty of Pharmacy, AL-Aharm Canadian University (ACU), Giza, Egypt
5 9 2024
5 9 2024
2024
23 2402 6 2024
9 8 2024
© The Author(s) 2024
2024
https://creativecommons.org/licenses/by/4.0/ Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
Long-term antibiotic treatment results in the increasing resistance of bacteria to antimicrobials drugs, so it is necessary to search for effective alternatives to prevent and treat pathogens that cause diseases. This study is aimed for biological synthesis of silver Carthamus nanoparticles (Ag-Carth-NPs) to combat microbial biofilm formation and Pseudomonas aeruginosa virulence genes. Ag-Carth-NPs are synthesized using Carthamus tenuis aqueous extract as environmentally friendly method has no harmful effect on environment. General factorial design is used to optimize Ag-Carth-NPs synthesis using three variables in three levels are Carthamus extract concentration, silver nitrate concentration and gamma radiation doses. Analysis of response data indicates gamma radiation has a significant effect on Ag-Carth-NPs production. Ag-Carth-NPs have sharp peak at λ max 425 nm, small and spherical particles with size 20.0 ± 1.22 nm, high stability up to 240 day with zeta potential around − 43 ± 0.12 mV, face centered cubic crystalline structure and FT-IR spectroscopy shows peak around 620 cm−1 that corresponding to AgNPs that stabilized by C. tenuis extract functional moiety. The antibacterial activity of Ag-Carth-NPs against pathogenic bacteria and fungi was determined using well diffusion method. The MIC values of Ag-Carth-NPs were (6.25, 6.25, 3.126, 25, 12.5, 12.5, 25 and 12.5 µg/ml), MBC values were (12.5, 12.5, 6.25, 50, 25, 25, 50 and 25 µg/ml) and biofilm inhibition% were (62.12, 68.25, 90.12, 69.51, 70.61, 71.12, 75.51 and 77.71%) against Escherichia coli, Klebsiella pneumoniae, Pseudomonas aeruginosa, Bacillus subtilis, Staphylococcus aureus, Staphylococcus epidermidis, Candida tropicalis and Candida albicans respectively. Ag-Carth-NPs has bactericidal efficacy and significantly reduced the swarming, swimming motility, pyocyanin and protease production of P. aeruginosa. Furthermore, P. aeruginosa ToxA gene expression was significantly down regulated by 81.5%, while exoU reduced by 78.1%, where lasR gene expression reduction was 68%, while the reduction in exoU was 66% and 60.1% decrease in lasB gene expression after treatment with Ag-Carth-NPs. This activity is attributed to effect of Ag-Carth-NPs on cell membrane integrity, down regulation of virulence gene expression, and induction of general and oxidative stress in P. aeruginosa. Ag-Carth-NPs have no significant cytotoxic effects on normal human cell (Hfb4) but have IC50 at 5.6µg/mL against of HepG-2 cells. Limitations of the study include studies with low risks of silver nanoparticles for in vitro antimicrobial effects and its toxicity.

Supplementary Information

The online version contains supplementary material available at 10.1186/s12934-024-02508-9.

Keywords

Ag-Carth-NPs
Radiation
Anti-biofilm
Kinetic growth
P. aeruginosa and anti-virulence genes
Egyptian Atomic Energy AuthorityOpen access funding provided by The Science, Technology & Innovation Funding Authority (STDF) in cooperation with The Egyptian Knowledge Bank (EKB).

issue-copyright-statement© BioMed Central Ltd., part of Springer Nature 2024
==== Body
pmcIntroduction

Nanotechnology has emerged as one of the most promising technologies to overcome the crisis of drug resistance microbes [1–4]. Chemical vapor deposition, microwave, laser ablation, ultrasonic radiation, and electrochemical methods are a few frequently used for metallic nanoparticles synthesis, because these methods are characterized by high production costs and the use of hazardous and toxic compounds, which may have detrimental impacts on human health and the environment [5]. Green synthesis in which mostly uses plant extracts, is an environmentally acceptable method to produce metallic nanoparticles without having to deal with hazardous chemicals, because compounds derived from plant extracts (flavonoids, polyphenols, proteins, sugars, and saponins) act as stabilizing and reducing agents metals instead hazardous chemicals [6].The biological synthesis of nanoparticles using plants and plant extracts appears to be an attractive alternative to conventional chemical synthesis [7–9]. Recently, synthesizing metal nanoparticles using plants has been extensively studied and has been recognized as a green and efficient method [10, 11]. The biological synthesis of metal nanoparticles has low toxicity when compared with other methods [12]. They are used natural extracts for example, as tomato, paprika, or marigold extracts, fenugreek, lupin, and other plants for biological synthesis of metals nanoparticles [13–15]. Use of Gymnanthemum amygdalinum extracts for Se-NPs biosynthesis [16]. Synthesis of copper nanoparticles Using Krameria sp. Root extract [17]. Leaf extracts of Clerodendrum Inerme were used for the generation of silver nanoparticles [18].

There are about 47 species in the genus Carthamus (family Asteraceae), 15 of which are found in Western Asia and the Middle East region, Carthamus tenuis is one of them [19]. While several of these species were explored for their potential medical uses, it’s odd that not much research was done on C. tenuis, despite the fact that it’s widely distributed throughout the Middle East [20]. C. tenuisleaves and stems aqueous extract it has not been used before in the formation of nanoparticles and is neglected in use in the Middle East. Most previous researches are focused on Carthamus tinctorius no Carthamus tenuis. Additionally, they show that the plant is traditionally used in Egypt as an aphrodisiac, to promote fertility, to prevent abortions and as antimicrobial herbal medicine[21]. The crop holds significant industrial value as a result of its ability to extract commercial oil. Moreover, the substances found in its petals serve as natural food coloring [22]. Nevertheless, after the seed is extracted, over 80% of this product (leaf or stem) is regarded as an agricultural waste [23]. Flavonoids, quinochalcones, polyacetylenes, alkaloids, fatty acids, steroids, lignans, proteins, and polysaccharides are among the chemical families that have been identified from safflower; quinochalcones and flavonoids are the primary active chemicals [24, 25], that play important role in reduction and stabilization of nanoparticles. Plant extracts have been shown to possess antibacterial properties due to the presence of phenolic chemicals [3, 26]. Safflower’s antibacterial activity is probably caused by polyphenols rupturing membranes and allowing biological components to escape. Thus, substances that disrupt membranes cause cellular contents to leak out and obstruct metabolic enzymes, which inactivates bacteria[27].

Recently, as an alternative to antibiotics, the use of different nanoparticles (NPs) to treat bacterial infections [28, 29] and fungal infection has been increasing in popularity [30]. A significant advancement in nanotechnology is the use of silver nanoparticles compared to other metals, because of their great stability, low chemical reactivity and have special physicochemical features, they have drawn a lot of interest in biological applications [31]. The high surface area and distinct chemical and physical properties of silver nanoparticles have made them effective antimicrobial agents against multidrug resistant microbes [9]. Silver nanoparticles remarkable antibacterial properties make it an essential tool for tissue regeneration, cancer treatment, wound healing, and infection prevention[32]. Furthermore, AgNPs exhibit significant potential as adaptable drug carriers for targeted treatments and as contrast agents for cutting-edge medical imaging methods [33]. Silver nanoparticles can kill organisms by causing breakdown of the cytoplasmic membrane and cell wall, then liberating silver ions (Ag +) to adhere to or go through the membrane, causing ribosome denaturation and stopping protein production [34].According to their earlier research, biofilm formation in Escherichia coli, Pseudomonas aeruginosa, and Klebsiella pneumoniae was inhibited within 24 h by increasing the concentration of silver nanoparticles from 12.5 to 100 μg/ml [35]. Silver Nano that applied to textile materials for wound dressing can prevent bacterial adhesion and biofilm formation [36].

Bacterial biofilms are bacterial communities embedded in a selfproduced polymeric matrix (extracellular polymeric substance) that adheres to surfaces and their interface, this biofilm shields the bacterium from antimicrobial agents and host immune responses [37].Biofilm forming organisms have a natural resistance to antibiotics, disinfectants, and germicides [38, 39]. The biofilm bacteria can withstand higher antibiotic concentrations than bacteria in suspension makes it more difficult to eradicate a persistent illness linked to biofilm formation [40]. The production of several virulence factors further aids pathogenicity and infection by biofilm-forming bacterial pathogens [41]. The bacterial infections that produce biofilms are responsible for causing mutant cells to become more resistant to antibiotics [42]. It is now widely known that biofilms are extremely difficult to remove and frequently resistant to systemic antibiotic therapy [43]. P. aeruginosa is a gram negative bacterium widely distributed in the environment, usually inhabiting soil, water, plants, and humans [44]. P. aeruginosa infects individuals suffering from immunodeficiency, cystic fibrosis, burn wounds, cancer, chronic obstructive pulmonary disease (COPD), and severe infections that need to be ventilated, such COVID-19 [45]. In all biological domains, P. aeruginosa is also a widely used model bacteria[46]. P. aeruginosa virulence factors that are related to disease development in healthy organisms and resistance to antibiotics [47]. The use of nanoparticles to inhibit P. aeruginosa virulence factors is a promising strategy [48]. Biologically synthesized silver nanoparticles are reported as anti-QS and antibiofilm drugs against P. aeruginosa infections[49]. Previous study show a significantly decreased the expression of quorum sensing regulatory genes of P. aeruginosa; lasR, lasI, pqsA, fliC, exoS and pslA with Ag-MET-NEs [50]. Ag-nanoparticles can inhibit virulence factors of microbes, this action mechanism is related to their effect on the integrity of cell membranes, the down regulation of the expression of virulence genes, and the creation of oxidative and general stress in microorganisms[51]. Novelty of the study is Ag-Carth-NPs using C. tenuis aqueous extract, where C. tenuis it has not been used before in the formation of nanoparticles and is neglected in use in the Middle East.

The current study aimed to biological synthesis of silver Carthamus nanoparticles (Ag-Carth-NPs) to combat pathogenic microbe’s biofilm formation and P. aeruginosa virulence genes.

Materials and methods

Chemicals

The ingredients of the media utilized in the microbiological examination were obtained from Oxoid, and silver nitrate, Clindamycin, Nystatin, Crystal Violet, ethanol was obtained from Sigma-Aldrich.

Preparation of safflower (Carthamus tenuis) aqueous extract

Plant sample

Fresh samples of Carthamus tenuis were collected locally from Abu El Matamir, Al Buhayrah, Egypt, 2023. The C. tenuis waste used in the present investigation consisted of a mixture of stem and leaf obtained after the seed collection process. The sample was collected 150 days after sowing. The plant samples leafs and stems were cleaned using sterile distilled water and then dried at room temperature (25 ℃ for 1 weeks), after drying the leaf and stem samples was ground into powder using a blender. The dried plant materials were stored in a dark area until needed.

Extraction of bioactive compounds

Extraction of Carthamus tenuis was performed according to the modified method described by [52]. Briefly, 5.0 g of fine safflower powder was immersed in 100 ml of sterile distilled water for 3 h on magnetic stirrer at 80 ℃. Finally, it was centrifuging the macerate at 4000 rpm and 5 ℃ using a cooling centrifuge, the supernatants were was recovered and filtered on Whatman #4 paper, and then dried at room temperature (25 ℃) and stored at 5 ℃ until used for nanoparticles synthesis.

Preparation of Silver- Carthamus nanoparticles

Optimization of silver- Carthamus nanoparticles (Ag-Carth-NPs) synthesis

A general factorial design was used to compare the influence of different parameters on the synthesis of silver nanoparticles [15]. The statistical software package used was Design-Expert 7.0 (Stat Ease Inc., Minneapolis, U.S.A) to determine the factors that have positive and significant effects on the process. Certain factors were chosen as they have the most meaningful impact on AgNPs synthesis. The influences of the three variables in three levels are Carthamus extract (1, 2, and 3 × 102 µg/ml disolved in DMSO), silver nitrate concentration (0.5, 1and 1.5 × 102 µg/ml disolved in sterile deionized water), and gamma radiation doses (0, 1, and 5 kGy). All samples was mixed by v/v using magnetic stirrer at 25 ℃. and then exposed to gamma radiation according to Table 1. Responses as optical density (OD) was meaured after radiation using UV-visible spectroscopy at wavlentgh 425 nm to estimated how the main parameter affects the synthesis of Ag-Carth-NPs after 24 h of reaction time. Table 1 Experimental factors that have an effect on Ag-Carth-NPs production

Run no	Factors	Response	
Ag-nitrate (µg/ml)  × 102	Radiation dose	Carthamus dry extract (µg/ml)  × 102	Optical density (OD) of Ag-Carth-NPs at 425nm	
1	0.5	1	2	1.3 ± 0.01	
2	1.5	1	1	1.03 ± 0.05	
3	1	5	1	2 ± .012	
4	1.5	5	2	2.4 ± 0.031	
5	1	5	3	2.1 ± 0.041	
6	1.5	1	3	1 ± 0.41	
7	1	5	2	4.42 ± 0.21	
8	1.5	5	1	2.6 ± 071	
9	1	1	2	3.12 ± 0.031	
10	1.5	0	3	1.23 ± 0.041	
11	1	1	1	2.3 ± 0.071	
12	0.5	1	3	1.9 ± 0.081	
13	0.5	0	3	1.032 ± .057	
14	1.5	0	1	1.16 ± 0.019	
15	1.5	0	2	1.6 ± 0.018	
16	0.5	0	1	1.32 ± 0.061	
17	1	0	2	1.7 ± 0.026	
18	0.5	5	1	1.84 ± 0.061	
19	0.5	5	3	2.3 ± 0.01	
20	1	0	1	1.02 ± 0.038	
21	0.5	1	1	2.15 ± 0.031	
22	0.5	0	2	1.3 ± 0.003	
23	1.5	5	3	1.95 ± 0.019	
24	1	1	3	2.054 ± 0.019	
25	1.5	1	2	2.15 ± 0.017	
26	1	0	3	1.2 ± 0.019	
27	0.5	5	2	1.94 ± 0.12	
Analysis of variance tablea	
Source	Sum of squares	df	Mean square	F Value	p-value Prob > F	
Model	9.03	6	1.50	5.20	0.0023	
A-Ag	1.72	2	0.86	2.96	0.0746	
B Radiation	5.56	2	2.78	9.60	0.0012	
C-Extract	1.76	2	0.88	3.03	0.0707	
Residual	5.79	20	0.29		
Cor Total	14.82	26		
The statistical software package used was Design-Expert 7.0 (Stat Ease Inc., Minneapolis, U.S.A). Where the comparison tests were performed for values of similar responses (p < 0.05)

Bold values are refer to P values

aSignificant: The Model F-value of 5.20 implies the model is significant. There is only a 0.23% chance that a “Model F-Value” this large could occur due to noise. Values of “Prob > F” less than 0.0500 indicate model terms are significant. In this case B is significant model terms

Validation of Ag-Carth-NPs and stability

The size and morphology of the synthesized Ag-Carth-NPs were characterized using the following techniques. Transmission electron microscope (TEM) (TEM-JEOL electron microscope JEM-100 CX) operating at 80 kV accelerating energy is great for characterizing the size and shape of nanoparticles [53]. Particle size, particle size distribution and Zeta potential was determined by Dynamic light scattering (DLS) Zetasizer Technique (PSS-NICOMP 380-ZLS, USA) where 250 μl of suspension transferred to a disposable small volume cuvette. While the Fourier transforms infrared spectroscopy (FT-IR) was employed to assess the function moiety [54], where the samples were recorded in KBr pellets using an FT-IR (JASCO FT-IR -3600). Using X-ray diffraction analysis, the crystalline structure of the produced metallic nanoparticles [55], was established. Cu-Ka target and nickel filter were used in the study of extended X-ray diffraction models (Shimadzu apparatus -Shimadzu Scientific Instruments; SSI, Japan). Operating at 50.0 mA and 40.0 kV, with a flow rate of 2/min, and a 2 h value between 20 and 100, a Cu anode is used. The intensity of the diffracted X-rays is determined based on the diffracted angle 2 h.

The stability of Ag-Carth-NPs was estimated at different storage time ranged from 1 to 240 day at room temperature (25 ℃ and neutral pH (7.0) using by UV-vis spectroscopy [56, 57]. Further, the zeta potential was measured to assess the stability and solubility of Ag-Carth-NPs in aqueous solution.

Antimicrobial assays

Microorganism

Microbial strains: In this study standard strain were kindly provided from culture collection of Drug Microbiology Lab, Drug Radiation Research Department, Biotechnology Division, National Center for Radiation Research and Technology (NCRRT), Egyptian Atomic Energy Authority. In addition to clinical isolates of P. aeruginosa were used and selected after screening of more than 50 P. aeruginosa clinical isolate. The selection of P. aeruginosa clinical isolates based on higher resistant to free silver nitrate and Carthamus extract solution. Preparation and sterilizing the agar plates was done according to previous described study [58], with slightly significant modification (Supplementary data).

A colony of the required strain was picked from the stock plates and transferred to 10mL of LB medium to prepare the overnight bacterial cultures (37 ℃, 200 rpm, using an orbital shaker incubator). The overnight cultures were refreshed by adding fresh LB medium and incubated at 37 ℃ for approximately 1 h. We aimed to reach the appropriate OD 600 corresponding to the known concentration of bacteria expressed as CFU per ml. Each bacterial culture was diluted in sterile 0.9% NaCl to an initial concentration of about 1 × 106 cells per mL.

Inhibition zone diameter

The antimicrobial activity of Ag-Carth-NPs was determined by using the agar diffusion method [59, 60] against gram positive bacteria Staphylococcus aureus ATCC 25923, Staphylococcus epidermidis ATTC 12228 and Bacillus subtilis ATCC 6633 and gram negative bacteria like Escherichia coli RCMB 0020B01, Klebsiella pneumoniae ATTC 13883, P. aeruginosa clinical isolate; additionally, antifungal towards Candida tropicalis RCMB001Y004 and Candida albicans ATCC 10231.

The agar plate surface is inoculated by spreading a volume of the microbial inoculum (1 × 106 cells per ml) over the entire agar surface. Then, a well (with a diameter of 6 mm) is made aseptically using a sterile corkborer. The well was diffused with 50 µl of each tested sample: Ag-Carth-NPs at 100 µg/ml. Carthamus extract (2 × 102 µg/ml) and silver nitrate (1 × 102 µg/ml) was used as negative control and Clindamycin 2 μg/ml and Nystatin 100 μg/ml as positive control, then incubated at 37 ℃ for 24 h [61, 62]. The measurement of inhibition was carried out by observing the emergence of a clear zone.

Minimum inhibitory concentration (MIC) determination and minimum bactericidal concentration (MBC)

The MIC was determined by well diffusion method based on the guidelines of the Clinical Laboratory Standard Institute (CLSI) [63]. The MIC of Ag-Carth-NPs was identified to determine the lowest concentration that inhibits the visible growth of the test organisms. Different concentrations of Ag-Carth-NPs (100, 50, 25, 12.5, 6.25, 3.125, and 1.625 µg/ml) were used. The procedure was repeated three times and the mean value was taken into consideration. In these experiments, a positive control (nutrient plus microorganism), and negative control one (the nutrient only) had been used. The data within the samples are analyzed using one way analysis of variance (ANOVA).

After the MIC determination of the Ag-Carth-NPs, aliquots of 10 µl samples from all the tubes which showed no visible bacterial growth were seeded on Brain Heart Infusion Agar (BHI agar) plates and incubated for 24 h at 37 ℃. When 99.9% of the bacterial population is killed at the lowest concentration of an antimicrobial agent, it is termed as the minimum bactericidal concentration (MBC) endpoint [64]. This was done by observing pre and post-incubated agar plates for the presence or absence of bacterial colonies. The procedure was repeated three times and the mean value was taken into consideration. The data within the samples are analyzed using one way analysis of variance (ANOVA).

Anti-biofilm activity

The biofilm qualitative and quantitative formation analysis was performed in the absence and presence of Ag-Carth-NPs against all tested organisms. A semi-qualitative detection of biofilm formation was determined according to Elbasuney, [65]. Fifty microliters of the chosen microbes overnight culture in LB, the broth turbidity was adjusted at 0.5McFarland Standards (5 × 105 CFU/ml). The microbial suspension was put to the tubes contain two milliliters of sterilized LB broth, and these tubes were kept at 37 ℃ for 1 day after addition of Ag-Carth-NPs at sub-MIC (0.25MIC, 0.5MIC and 0.75MIC) to each separate tubes. The experiment also included tubes containing media alone represented negative controls and tube contain media plus tested organisms in absence of Ag-Carth-NPs represented as positive control. Following incubation, the broth culture was poured out and washed with three PBS (PBS; pH 7.0). Next, the bacterial and yeast cells biofilms that adhered to the tube walls were fixed using sodium acetate (3.5%) for approximately 20 min. For thirty minutes, the insides of the tubes were stained with 10 mL 0.1% crystal violet dye. While the excess dye was decanted and washed off with deionized water gently, the tubes were dried and the biofilm formation ability was determined by observing a thin layer of blue film on the walls of tubes.

The microtiter plate technique was utilized for quantitative estimation of biofilm formation [66]. Using 96-well microtiter plates, the assay involved inoculating each well with 100 μl of LB broth, 10 μl of culture cultured overnight and diluted further to a final concentration of 5 × 105 CFU/ml, and 10 μl of Ag-Carth-NPs at sub-MIC (0.25MIC, 0.5MIC and 0.75MIC) was measured against the chosen microbes. After being incubated at 37 ℃ for 24 h, the contents of the wells was carefully removed and three times cleaned with PBS (PBS; pH 7.0) to get rid of any bacteria. After that, biofilms were fixed with sodium acetate sodium acetate (3.5%) and stained for ten minutes with 50 μl of 0.1% crystal violet dye. After being dyed and affixed to wells, the cells were dried and cleaned with distilled water. 200 μl of 95% ethanol was added in each well to elute the attached cells, and absorbance was measured at 600 nm on ELISA reader in order to quantify cells capable of forming biofilms. Negative and positive controls were also used in the assay.

The inhibition percentage was calculated using equation (1)1 Percentageofbiofilminhibition(%)=1-ODoftreatedwithAg-Carth-NPs/ODofuntreatedcontrolx100

Time-Kill curve assay

Time-kill assay was done in MHB medium as described by Loo et al. [9]. The inoculums were adjusted to 106 CFU/millimeter. The Ag-Carth-NPs solution was diluted with MHB media containing microbial inoculums to obtain the final concentration of 0 MIC, 0.5 MIC, 1 MIC, 2MIC and 4MIC, for each type of microbes in the total final volume of 1 ml. The cultures were then incubated at 37 ℃ with 140 rpm agitation. The cultures (100 µl) were spread on MHA plates at time 0, 1, 2, 4 and 8 h. The experiment was carried out in triplicate. The number of colonies on the MHA plates was quantified in CFU/mL after incubation at 37 ℃ for 24 h and then, their growth rate was identified through reading OD600 using fixed UV- spectroscopy.

Statistical Analysis- One way ANOVA: The results represent the mean±SD from at least three independent experiments. One-way ANOVA with Tuckey post-hox test, using Graph 10 software (*P<0.05; **P<0.01 and ***P<0.001) was performed (*P<0.05; **P<0.01 and ***P<0.001) compare to the control group.

Motility of P. aeruginosa assay

Swarming motility assay In order to test the capacity of the Ag-Carth-NPs to block the swarming motility of P. aeruginosa clinical isolate was performed as discussed earlier [67]. A clinical isolate of P. aeruginosa was grown in Luria Bertani broth (LB) for 24 h then bacterial suspension was adjusted to reach an OD600=1. The swarming medium composed of LB along with 0.5% (w/v) casamino acids and 0.4% (w/v) Bacto agar. Before agar solidification, 0.5MIC concentration of Ag-Carth-NPs was added, and then 2.5 µl fresh bacterial culture was placed on the surface of the medium, followed by incubation at 35 ℃ for 24 h. and bacterial swarming zone was then measured [68]. All motility experiments were performed in triplicate. All motility experiments were performed in triplicate. Tubes contain media plus P. aeruginosa in absence of Ag-Carth-NPs represented as positive control.

Swimming assay Ag-Carth-NPs were tested for their impact on P. aeruginosa using a plate-based swimming assay. To put it briefly, the petri dishes were filled with Luria broth medium that included 0.3% agar and 0.5MICs Ag-Carth-NPs. Next, bacterial cells were added to the plate’s agar layer using sterile yellow pipette tips (not to the base of the Petri plate). After a 24-hour incubation period, the swimming phenotype's radial growth was measured on the plates [69]. Tubes contain media plus P. aeruginosa in absence of Ag-Carth-NPs represented as positive control.

Pyocyanin level

In order to determine how Ag-Carth-NPs affected P. aeruginosas capability to produce pyocyanin, bacterial cultures in an LB medium containing 0.5MIC Ag-Carth-NPs were created in tubes. The tubes were shaken at 80 rpm for 48 h at 37 ℃. Following centrifugation of the cultures, samples of the cell-free supernatant (CFS) were taken. After that, 4 ml of the CFS samples were mixed with 2 ml of chloroform, vortexed, and centrifuged for 15 mins. Then, the chloroform layer was transferred to a fresh tube and mixed with 1 ml of 0.2 M HCl. After centrifugation again, the top layer was removed and OD at 520 nm was measured [70]. Tubes contain media plus P. aeruginosa in absence of Ag-Carth-NPs represented as positive control.

Total proteases inhibition assay

Using the modified skimmed milk broth method, the effect of Ag-Carth-NPs on inhibition of total proteases by P. aeruginosa isolates was investigated. To acquire the supernatants, P. aeruginosa overnight cultures in MHB with and without 0.5MIC of the Ag-Carth-NPs were centrifuged. 500 μl aliquots of bacterial supernatants were cultured for 1 h at 37°C with 1 ml of 1.25 percent skim milk. Using a Biotek spectrofuorometer (USA), the drop in optical density of skimmed milk was measured at 600 nm and was thought to be estimate for proteolytic activity [50]. Tubes contain media plus P. aeruginosa in absence of Ag-Carth-NPs represented as positive control.

Gene expression

Effect of Ag-Carth-NPs on relative genes expression P. aeruginosa clinical isolate were tested for virulence genes using real-time reverse transcriptase-polymerase chain reaction (rt-PCR) according to the following steps

Bacterial DNA extraction DNA extraction from samples was performed using the QIAamp DNA Mini kit (Qiagen, Germany, GmbH) as previously described [71] with modifications from the manufacturer’s recommendations. Oligonucleotide Primer; Primers used were supplied from Metabion (Germany) are listed with specific references [72–75] in Table 1s. PCR reaction and Analysis of the PCR Products were performed in an applied biosystem 2720 thermal cycler as published before [76].

Bacterial RNA extraction and quantitative real-time PCR (qRT-PCR)

Total RNA was isolated from clinical isolate stain of P. aeruginosa cells cultured in the presence or absence of Ag-Carth-NPs (0.5MIC) in order to analyze the expression genes. The RNeasy Mini kit (Qiagen, Germany, GmbH) and the TRIzol reagent (Invitrogen, Waltham, MA, USA) were used for the extraction process. To eradicate DNA contamination, the RQ1-DNAse kit (Promega, USA) was utilized. The A260/A280 ratio calculation and agarose gel electrophoresis were used to confirm the quality of the extracted RNA. Primer-BLAST and BioEdit Sequence Alignment Editor were used to generate and analyze primers after gene sequences were taken from Gen Bank. The primers pair’s sequences for individual genes are presented with references [72, 75] in Table 2s. The QuantiNova SYBR Green RT-PCR kit (QIAGEN, Germantown, MA, EUA) was used to perform RT-qPCR in a final volume of 20 µl. The kit contained 10 µl of SYBR Green RT-PCR Master Mix, 0.2 µl of RT mix, 1 µl (20 µM) of each primer, 5 µl of bacterial RNA (50 ng/µl), and 2.8 µl of RNase-free water. Using the Rotor-Gene Q 2plex (QIAGEN, Germantown, MA, EUA) for the reaction, the following procedures were followed: 10 min of reverse transcription at 50 ℃, 2 min of initial denaturation at 95 ℃, 40 cycles of 95 ℃ for 5 s, and 10 s of hybridization and extension at 60 ℃. The changes in the expression level of target gene were analyzed by using the method adopted by Livak and Schmittgen [77].

Evaluation of cytotoxic effects

The cytotoxic action of Ag-Carth-NPs on the Hfb4 cells (normal skin cell lines) and HepG-2 cells (human Hepatocellular carcinoma) was determined as previously described by [54, 78];. A volume of 100 µl/well of Ag-Carth-NPs at concentrations 100, 50, 25, 12.5, 6.25, 3.125 and 1.56 µg/ml was injected into the 96-well microliter plate containing 1 × 106 HepG-2 cells or and Vero cells. The samples were incubated for 4 h at 37 ℃, 5% CO2. Controls are wells were left without Ag-Carth-NPs. The absorbance at λ=570 nm was measured using a plate reader. The relation between surviving cells and Ag-Carth-NPs concentration is plotted to get the survival curve of each tumor cell line after treatment with the specified compound The Cytotoxic concentration (CC50), the concentration required to cause toxic effects in 50% of intact cells, was estimated from graphic plots of the dose response curve for each conc. using Graphpad Prism software (San Diego, CA. USA).

Statistical analysis

The results represent the mean±SD from at least three independent experiments. One-way ANOVA with Tuckey post-hox test, using Graph 10 software (*P<0.05; **P<0.01 and ***P<0.001) was performed (*P<0.05; **P<0.01 and ***P<0.001) compare to the control group.

Results and discussion

Optimization of silver- Carthamus nanoparticles synthesis

The experimental factorial design was used in this study for screening factors that significantly effect on the final Ag-Carth-NPs production. Responses optical density (O.D) estimated how the main parameter effects on the Ag-Carth-NPs production (Table 1) where, OD values is was triplicate measured at fixed wavelength 425 nm using UV-visible spectroscopy. All parameters, such as concentration of Carthamus extract (1, 2, and 3 × 102 µg/ml), silver nitrate concentration (0.5, 1 and 1.5 × 102 µg/ml), and gamma radiation doses (0, 1, and 5kGy) were maintained constantly.

The results showed that, trial no (7) has high peak optical intensity (O.D a.u) about 4.42 ± 0.21 in competing with other trials that show optical density at range from 1.02±0.038 to 3.12±0.031 (Table 1); where high value of OD indicates higher yields of NPs [79]. The variation in the OD value coincides with nanoparticles production amount [80], trial with high OD indicate high yield of NPs than trial with low OD [81]. Factorial design indicates that, the maximum yield of Ag-Carth-NPs (OD = 4.42) was achieved with run corresponds to an actual 1 × 102 µg/ml Ag-nitrate, 5kGy and 2 × 102 µg/ml Carthamus dry extract. Analysis of response data show Values of “Prob > F” less than 0.0500 indicate radiation is significant model terms. The peak optical density increased proportionately, that is mainly due to the high production of nanoparticles [82, 83]. Optimization of lupin-Se-NPs production using general factorial design was previously discussed [14]. Gamma ray improve metallic nanoparticles synthesis in presence of plant extract [84], this attributed to potent reducing free electron generated from radiation that assist reduction of ions to metallic nanoparticles [85, 86].

The conditions 1 × 102 µg/ml Ag-nitrate, 5kGy and 2 × 102 µg/ml Carthamus dry extract, with change in gamma radiation dose by increase or decrease the dose show negative effect on Ag-Carth-NPs production (Figure 1a). This attributed to increase in random movement of particles in Ag-Carth-NPs suspension, that associate with increase of gamma doses leading to Ag-Carth-NPs aggregation and precipitation [86], or decrease in Ag-Carth-NPs production that associated with decrease in gamma radiation due to low level of free electron production that responsible for silver reduction [85].Fig. 1 a UV–visible scanning of Ag-Carth-NPs, b DLS diagram of Ag-Carth-NPs, c diagram of Ag-Carth-NPs Zeta potential, d TEM image of diagram of Ag-Carth-NPs, e FT-IR spectrum of Ag-Carth-NPs, f XRD pattern of Ag-Carth-NPs and g UV–visible scanning of Ag-Carth-NPs stability over time

Ag-Carth-NPs validation and stability

UV-Vis spectrophotometry: For the first validation of metallic nanoparticle production, UV Vis spectrophotometry is an essential tool [87]. The UV-Vis spectrum of Ag-Carth-NPs (Figure 1a) showed the highest absorption peaks at 425nm in solutions, which indicate the localized surface Plasmon resonance (LSPR) characteristics of silver nanoparticles [88]. Smaller nanoparticles absorb light primarily and have peaks that are near 400 nm, whereas larger particles show more scattering and have peaks that broaden and shift toward longer wavelengths (a process called red-shifting) [89]. Figure 1a show that, Ag-Carth-NPs UV-Vis spectrum at 0kGy, 10kGy at 1 × 102µg/ml Ag-nitrate and 2 × 102 µg/ml Carthamus dry extract has the same peak wavelength 425 nm with decrease in optical density (1.7±0.031 and 3.23±0.161 respectively) compering with 5kGy (4.42±0.21), this indicates low Ag-Carth-NPs production with decrease or increase of gamma radiation dose. Where increase in optical density corresponds with a dosage of gamma rise from 0 to 5kGy and then decreased with 10kGy. an increase in peak intensity, indicating a decrease in particle size and an increase in NPs production[85]. The results from UV-Vis spectrum of Ag-Carth-NPs and general factorial design optical density response confirm gamma radiation has significant effect on Ag-Carth-NPs production yield and the optimum dose is 5kGy.

The particle size distribution and zeta potential of Ag-Carth-NPs in water dispersion was measured by DLS technique [90]. Ag-Carth-NPs size distribution was found at range 32.00 nm (Figure 1b). Dynamic Light Scattering (DLS) estimates the hydrodynamic diameter of dissolved nanoparticles and gives insights on their aggregated state [91]. Size dispersed particle averages of DLS values are slightly greater than TEM values. Because, DLS you measure hydration sphere diameter where there will be solvent molecules associated with your particle [92].

Zeta potential is it an important tool for understanding the state of the nanoparticle surface and predicting the long term stability of a colloidal dispersion [93]. Figure 1c show Zeta potential of Ag-Carth-NPs at range about − 43±0.12 mV. The negative zeta potential indicated the stability of the nanoparticles and prevent them from agglomeration[94]. According to previously published research, nanoparticles that have a zeta potential less than – 30 mV are thought to be highly stable in the dispersion medium [95].

Transmission electron microscopy (TEM) it’s a quantitative technique to determine the particle size, shape and distribution [96]. The TEM images clearly demonstrated the Ag-Carth-NPs has spherical isotropic shape and anisotropic particles, with average particle sizes ranging 20 ± 1.22 nm (Figure 1d). TEM results are based on a number analysis of a dry particle and the values tend to be smaller than DLS results [97], this because TEM reveals the structure of molecule from interior and gives thought approximately molecule diameter and framework structure in solid case [98]. The presence of Carthamus extract act as capping and stabilizing agents that prevents the aggregation and agglomeration of generated Ag-Carth-NPs.

FTIR spectrum is used to identify the functional groups used in capping of NPs [99]. FT-IR spectrum (Figure 1e) evidences the presence of different functional groups of biomolecules participated in stabilization NPs [100]. Accordingly, the FTIR spectrum of the Carthamus extract exhibited several peaks around 3520, 3020, 2630, 1170 and 890 cm−1 that indicate presence of (O-H), (N-H), (C-O) and (RCOO) function moiety. These characteristic bands predict that in the extract there are structures as proteins, polysaccharides/sugars and phenolic compounds, mainly flavonoids[101]. Results of FT-IR Ag-Carth-NPs analysis shows absorption peak at 620 cm-1 corresponding to presence of AgNPs [102], that absent from Carthamus extract. The FTIR results we can conclude that some of the biological compounds from Carthamus extract formed a strong capping agent on the AgNPs for their stabilization.

Figure 1f illustrates the XRD pattern for Ag-Carth-NPs, which showed several peaks related to Ag-Carth-NPs. Within 2 h (degree), the diffraction characteristics are 37.04, 43.11, 65.31, and 76.51, respectively. These peaks correspond to the Bragg’s reflections (111), (200), (220), and (311) planes. This suggests that silver nanoparticles have a face-centered cubic (fcc) crystalline structure [59]. The XRD pattern shows amorphous regions before 30.0 degree of 2 theta, its due to presence of biological extract [103].

The stability of Ag-Carth-NPs over a range of time was estimate firstly using UV-vis spectroscopy (Figure 1g), the intensity and sharpness of peak and location has no changed after 30 day of storage this indicate highest stability and no changes in size or distribution of nanoparticles [104, 105]. Peak intensity of Ag-Carth-NPs are slightly decreased with time increased after 60 day up to 240 day with no changes in wavelength location or sharpness, this indicate slightly aggregation of NPs [106].The stability of Ag-Carth-NPs is also estimated by DLS and zeta potential (Table 2), that show Ag-Carth-NPs has DLS size distribution at range from 32.00 ± 1.55 nm to 37.51 ± 1.71 nm at time storage ranged from 1 to 240 day with zeta potential ranged from – 43 ± 0.12 to -47±0.81 mV and Polydispersity index value at range from 0.211 ± 0.05 to 0.321 ± 0.09. These results confirm high stability of Ag-Carth-NPs over longer time with no significant changes in size with time storage. Table 2 The stability of Ag-Carth-NPs at different time

Time (day)	Wavelength (nm)	Absorbance O.D	DLS (nm)	Zeta potential (mV)	Polydispersity index (PDI)	
1	425	4.42	32.00 ± 1.55	− 43 ± 0.12	0.211 ± 0.05	
15	425	4.41	32.01 ± 1.45	− 43 ± 0.12	0.212 ± 0.06	
30	425	4.41	32.02 ± 1.50	− 43 ± 0.12	0.215 ± 0.06	
60	425	4.22	33.31 ± 0.39	− 44 ± 0.58	0.241 ± 0.06	
120	425	4.03	36.92 ± 1.02	− 45 ± 0.64	0.301 ± 0.07	
240	425	3.91	37.51 ± 1.71	− 47 ± 0.81	0.321 ± 0.09	
Where the comparison tests were performed for values of similar responses (p < 0.05)

Antimicrobial activity of Ag-Carth-NPs

Inhibition zone, MIC, MBC and Mechanism of action

Natural compounds have distinct antibacterial activities against both gram-positive and gram-negative bacteria [107]. Using biogenic synthesis to create nanoparticles (NPs) through the redox balance of an natural active substance with metal is one method of enhancing antimicrobial action [108]. In this study, the inhibition zone values of AgNO3, Carthamus extract, and Ag-Carth-NPs were represent in (Figure 2a) in compere with positive control (Clindamycin for bacteria and Nystatin for fungi. The diameter of the inhibition zone demonstrated the antibacterial activity of Ag-Carth-NPs against the examined microorganisms, which was found to be more significant than AgNO3, Carthamus extract. P. aeruginosa is the most common gram-negative pathogen causing multidrug resistant infections [109]. The results showed that the P. aeruginosa strain is more resistant to clindamycin antibiotic disc and is also the most susceptible strain to the Ag-Carth-NPs. Inhibition zone values of Ag-Carth-NPs are 23 ± 0.17, 21.0 ± 0.14, 27.0 ± 0.30, 22.0 ± 0.13, 26.0 ± 0.19, 24.0 ± 0.12, 21.0 ± 0.15 and 23.0 ± 0.14 against E. coli, K. pneumonia, P. aeruginosa, B. subtilis, S. aureus, S. epidermidis, C. tropicalis and C. albicans respectively.Fig. 2 a refer to inhibition zone (mm) of AgNO3, Carthamus extract, and Ag-Carth-NPs against tested organisms; Where, Clindamycin 2 μg/ml, Nystatin 100 μg/ml as positive control for bacteria and fungi respectively; Experiments were performed in triplicates and b refer to Biofilm inhibition % of silver nitrate, Carthamus extract and Sub-MIC Ag-Carth-NPs. Mean values with standard deviation (error bars) with *, **, ***are statistically different from the respective control at P < 0.05, P < 0.01, and P < 0.001, respectively; (One way ANOVA, Tukey test)

A further investigation in estimating the antibacterial activity was performed by determining the MIC and MBC (Table 3). The MIC of Ag-Carth-NPs was defined as the lowest concentration at which significant inhibition of bacterial growth was achieved. P. aeruginosa revealed an MIC value of 3.126 µgml−1 for Ag-Carth-NPs, >100 µgml−1 for AgNO3 and 100 µgml−1 for Carthamus extract, in that more potent inhibition has been observed in the case of Ag-Carth-NPs against all tested organism. The results show Ag-Carth-NPs has MIC at 6.25 ± 1.05 µgml−1 for E. coli and K. pneumonia, 12.5 ± 1.051 µgml−1 for S. aureus, S. epidermidis and C. albicans and 25 ± 1.071 µgml−1 for B. subtilis and C. tropicalis. Previous study demonstrated MIC of myco-synthesized silver nanoparticles for different bacterial strains was 1.5625 µg/ml for Listeria and Shigella, 0.78125 for E. coli and 3.125 for S. typhi[110]. The MICof AgNPs against S. aureus was 2.5 µg/disc and less than 2.5 µg/disc for P. aeruginosa[111]. Other studies refer biogenic AgNPs showed antimicrobial activities against gram-positive and gram-negative bacteria at MIC ranged between 16 and 64 μg ml−1[112]. Table 3 MIC and MBC of AgNO3, Carthamus extract, and Ag-Carth-NPs

Isolates strains	MIC (µg/ml)	MBC (µg/ml)	
Ag-NO3	Carthamus extract	Ag-Carth-NPs	Ag-Carth-NPs	
E. coli RCMB 0020B01	 > 100	100	6.25ad ± 1.05	12.5c ± 1.061	
K. pneumonia ATTC 13883	 > 100	100	6.25be ± 0.92	12.5e ± 1.041	
P. aeruginosa clinical isolate	 > 100	100	3.126a ± 0.83	6.25ae ± 0.72	
B. subtilis ATCC 6633	 > 100	 > 100	25be ± 1.031	50a ± 1.021	
S. aureus ATCC 25923	 > 100	100	12.5c ± 1.051	25a ± 1.71	
S. epidermidis ATTC 12228	 > 100	 > 100	12.5cd ± 1.061	25ad ± 1.096	
C. C. tropicalis RCMB 001Y004	 > 100	 > 100	25ae ± 1.071	50d ± 1.017	
C. albicans ATCC 10231	 > 100	 > 100	12.5b ± 0.925	25ab ± 1.082	
LSD	–	–	1.002	1.061	
Values are mean ± SD (n = 1.00). Data within the groups are analyzed using one-way analysis of variance (ANOVA)

LSD least significant differences

a, b, c, d, eDuncan’s multiple range test at p < 0.05

The lowest concentration of NPs that was bactericidal, i.e. that showed no growth on agar plates, was selected as MBC. In this study, for P. aeruginosa in case of Ag-Carth-NPs the MBC was 6.25 µgml−1. In case of other tested organisms Ag-Carth-NPs showed bactericidal activity at 12.5 for both E. coli and K. pneumonia and 25 µgml−1 for S. aureus, S. epidermidis and C. albicans and 50 µgml−1 for B. subtilis and C. tropicalis. Previous study refer to biogenic silver nanoparticles has MBC values against P. aeruginosa 27853 and S. aureus 25923 at 12 μg ml−1 and 3 μg ml−1 for E. coli 35218 [113]. The biogenic silver nanoparticles were found to be more potent bactericidal agents at low concentration [114].

Previous study indicates that majority of the examined bacteria were not inhibited in growth by aqueous extracts of safflower, with the exception of Acinetobacter baumannii, for which the inhibition zone measured two millimeters [115]. The antibacterial properties of silver nanoparticles synthesized from plant extract may have different processes when applied to gram positive and gram negative cells, where production of reactive oxygen species (ROS), radicals OH and hydrogen peroxide, is one of those mechanisms [116]. Especially when it involves gram-negative bacteria, reactive oxygen species cause oxidative stress and target the lipids in the outer membrane, leading to lipid oxidation, damage to proteins, RNA, and DNA, and ultimately, cell death [117]. Fecal microbiota transplantation has been proposed as a potential therapeutic solution [118] Several authors have reported that the microbial activity of AgNPs measuring 20–80 nm was attributed to the release of silver ions [119].

Silver nanoparticles, are recognized as a superior antibacterial agent than other metallic nanoparticles or antimicrobial agents that can fight both in vivo and in vitro microbes that cause diseases [120]. AgNPs have the ability to combat both gram-positive and gram-negative bacteria and fungi, including those that are resistant to multiple drugs [121]. AgNPs have several simultaneous modes of action. They have also demonstrated a synergistic effect against pathogen microbes when combined with antimicrobial agents or antibiotics [122]. Due to their unique properties, silver nanoparticles can be effectively used to cure or prevent infections in a variety of medical and healthcare goods [123]. Advantages of using AgNPs as new antibacterial agents in combination with antibiotic, which will reduce the dosage needed and prevent secondary effects associated to both [124].

Proposal antimicrobial Mechanisms of Ag-Carth-NPs Ag-Carth-NPs It is very likely that it has the same mechanism as the AgNPs. Different hypotheses for antimicrobial mechanism of AgNPs are discussed, including (i) Penetrating bacterial membrane, causing the cell membrane to be destroyed and content to spill out [125]. (ii) disrupt DNA structure, or directly contact with DNA to cause DNA mutations and disrupt DNA replication [126], (iii) Generating ROS and disabling the respiratory chains and iv) Inactivating enzymes and denaturing proteins [127]. AgNPs exhibit good antifungal properties against Candida spp. and resistant fungus. For instance, AgNPs may influence drug sensitivities by targeting many cellular targets of Candida albicans, such as fatty acids like oleic acid, which are crucial for the hyphal morphogenesis responsible for the pathogenicity [128]. AgNPs may be able to bind to and saturate the fungal hypoha, ultimately rendering the fungus inactive [129]. AgNPs have been proven to effectively inhibit various pathogenic bacteria, fungi and viruses, including gram positive and negative bacteria and fungi and viruses [29, 130]. Some factors can effect on antimicrobial activity of AgNPs such as bacteria strains, size, shape and concentration of AgNPs, time contact, and surface charge of particles [131]. AgNPs with larger surface has larger reaction surface, show stronger antibacterial activity [132]. Microorganism surfaces typically exhibit negative charge [133]. Antimicrobial activity of AgNPs is also affected by the surface charge, so positive charge can facilitate the adherence of Ag-NPs on bacterial membranes through electrostatic attraction [134]. Therefore, adjusting the surface charges of AgNPs may contribute to the enhanced antibacterial effect [135].

Surface interactions between polyphenols and newly reduced metallic silver particles function as the capping factor preventing the agglomeration of AgNPs [136]. Combining silver nanoparticles and plant extracts against microbes has drawn attention within the past few years [137]. Synergistic effect of plant extracts and silver nanoparticles allowed for efficacy higher than that of antibiotics (ampicillin) when tested at the same concentrations and after a relatively short exposure time of 3 h [138]. Preparation of silver nanoparticles in combination with C. tenuis extract in form of Ag-Carth-NPs, it is a preferred method and has a strong effect on all tested microbes.

Nanomaterials are used in a variety of biomedical applications, including anticancer therapeutics, antiviral applications, antibacterial and antifungal applications, wound healing, and antitumor activity [139, 140]. Green synthesis methods for silver nanoparticles are currently being developed by researchers and are beneficial for biomedical applications [141, 142]. Because unique characteristics of Ag-NPs such as their higher surface to volume ratio, a wide surface area, strong surface Plasmon resonance, stability, ease of processing, and multi-functionalization are well suited for a variety of biological applications such as antibacterial, antifungal applications, wound healing, target therapy and antitumor activity [133]. Silver nanoparticles, however, have a lot of interesting potential for use in biomedical applications, such as coatings for medical devices, formulations, drug administration, detection and diagnosis platforms, and biomaterials [143].

Biofilm inhibition

Microbes producing biofilms are the cause of numerous diseases. According to one study by the Centers for Disease Control and the National Institutes of Health, between 65 and 80% of infections were caused by bacteria producing biofilms [144]. The biofilm inhibitory activities of the Ag-Carth-NPs were performed using crystal violet assay. The Ag-Carth-NPs showed significant reduction in the biofilm formation compared to silver nitrate and Carthamus extract (positive control) as shown in (Figure 3). It was observed that Ag-Carth-NPs were able to reduce the biofilm formed by E. col, K. pneumonia, P. aeruginosa, B. subtilis, S. aureus, S. epidermidis, C. tropicalis and C. albicans are 62.12, 68.25, 90.12, 69.51, 70.61, 71.12, 75.51 and 77.71 %, respectively at 0.75MIC and 40.21, 45.51, 62.12, 42.12, 47.3, 43.61, 48.21 and 49.6% at 0.5MIC and 30.31, 34.5, 38.32, 31.61, 33.21, 32.41, 35.41 and 31.61% at 0.25MIC respectively.Fig. 3 Time kill curve of Ag-Carth-NPs against tested organisms at different concentration and time length. Untreated bacteria/fungi refer to growth at 0MIC and Minimum inhibitory concentration (MIC) is different according to MIC of each microbe. Where; a E. coli, b K. pneumonia, c P. aeruginosa, d B. subtilis, e S. aureus, f S. epidermidis, g C. tropicalis and h C. albicans. Mean values with standard deviation (error bars) with *, **, *** are statistically different from the respective control at P < 0.05, P < 0.01, and P < 0.001, respectively; (One way ANOVA, Tukey test)

The negative controls is experiment tubes containing media alone represented no growth or biofilm formation in the other hand negative controls is experiment tube contain media plus tested organisms in absence of Ag-Carth-NPs represented microbial biofilm formation without any percent of biofilm formation inhibition. Ag-Carth-NPs have significant inhibition of biofilm formation in compere with AgNO3 and Carthamus extract. AgNPs (10 µg/ml) synthesized by plant extract of G. lanceolarium were used to treat P. aeruginosa for 24 hours, resulting in a >99% reduction in biofilm formation[145]. Ag-NPs significantly eradicated mature biofilms developed by A. baumannii, K. pneumoniae and P. aeruginosa standard strains and clinical isolates[146]. Ag-NPs exhibited reduction in biofilm formation at range 22–79, 29–87, 12–59, 22–63, and 17–81% against P. aeruginosa, E. coli, C. violaceum, K. pneumoniae, and S. aureus respectively at sub-MICs ranging from 1/16 × MIC-1/2 × MIC[147]. Previous study reported biogenic synthesized AgNPs resulted in an 89% inhibition of biofilm formation in S. aureus and 75% in E. coli [145].

Prior research regarding the anti-biofilm effects of biosynthesized AgNPs against P. aeruginosa and S. epidermidis has been done by S. Kalishwaralal et al. [66]. The synergistic activity of the AgNPs and plant extract to control the biofilm formation by the pathogenic organisms are discussed by previous study [145]. The antibiofilm activity of AgNPs against P. aeruginosa, S. aureus (MRSA), S. mutans, and C. albicans was studied extensively and reported the potentiality of AgNPs [148]. Rolim et al. [149] reported the biofilm eradication of AgNPs against P. aeruginosa which supports our current results. Three pathways in particular are significant for the antibiotic resistance of bacteria in biofilms are (i) Resistance at the Biofilm Surface, (ii) Resistance in Biofilm Microenvironments and (3) Persister bacterial cells resistance [150].

Biofilm formation inhibition by Ag-NPs is due to, structural alterations of the membrane, increasing permeability and damaging membrane integrity. Furthermore, Ag-NPs adhered to the cell surface can stop the production of biofilms since bacterial adherence to any surface is the first step in the process [151]. Since Ag ions which generated from Ag-NPs after transported into the cell may interfere with microbial proteins and enzymes which are required for microbial adherences or formation of quorum sensing that resulted in the reduction in biofilm formation [152]. Physical and chemical properties of AgNPs, such as size and shape influence the activity of the nanoparticles, because smaller sizes increase the surface contact area of AgNPs with microorganisms and then decrease biofilm formation [37].

Time kill curve activity of Ag-Carth-NPs

The time kill activity of tested pathogens is done at Ag-Carth-NPs final concentration of 0 MIC, 0.5 MIC, 1 MIC, 2MIC and 4MIC and different time interval 0, 1, 2, 4 and 8 h as shown in (Figure 3). Ag-Carth-NPs were effective in inhibiting and killing the microbes in a dose and time dependent manner as shown in the time kill assays. The bactericidal activity of Ag-Carth-NPs is effective against the selected bacteria and fungi; the reduction in the number of CFU/ml is significant in compered with growth of controls (untreated bacteria/fungi refer to growth at 0MIC) that has ascending growth curve over all tested time.

The bactericidal endpoint of Ag-Carth-NPs for E. coli was reached after 1 h of incubation at 4MIC (25 µg/ml); while for K. pneumoniae, the bacteria was killed after 2 h of incubation at 2MIC (12.5 µg/ml) and after 1 h at 4MIC (25µg/ml). P. aeruginosa was killed after 1 h of incubation at 2MIC (6.25 µg/ml) and 4MIC (12.5 µg/ml). The bactericidal endpoint of Ag-Carth-NPs for B. subtilis was reached after 2 h of incubation at 2MIC (50 µg/ml) and 4MIC (100 µg/ml); however, the end point reached after 2h of incubation at 2MIC (25 µg/ml) and (100 µg/ml) for S. aureus. The bactericidal endpoint of Ag-Carth-NPs for S. epidermidis was reached after 2 h of incubation at 2 MIC (25 µg/ml) and 4MIC (50 µg/ml). C. tropicalis was killed after 2 h of incubation at 2MIC (50 µg/ml) and 4MIC (100 µg/ml); however, the bactericidal endpoint of Ag-Carth-NPs for C. albicans after 2 h of incubation at 2 MIC (25 µg/ml) and 4MIC (50 µg/ml).

The results demonstrated that Ag-Carth-NPs could completely inhibit growth of the tested microorganisms in dose dependent manner. A Significant difference was found among the tested pathogens at the time killing depend on types of organisms and concentration of Ag-Carth-NPs. However, the end point reached faster after 1h of incubation with low concentration for P. aeruginosa in competing with other tested microbes. Ag-NP concentrations and the types of bacteria used in the research have an impact on the inhibition of bacterial growth [153]. Ag-Carth-NPs exhibit significant bactericidal effect against all tested organisms, this must be due to synergistic effect of AgNPs and bioactive agent of Carthamus extract present over its surface as reported earlier with AgNPs plant extract combination [154]. Furthermore, such surface loading biochemical agents over NPs enhance solubility of NPs in aqueous suspension, thereby providing the additional benefit of increased bioavailability and therapeutic potential [155].

The killing activity of AgNPs are fast acting against all the gram negative bacteria and the reduction in the number of CFU mL-1 was >3 Log10 units (99.9%) in 1–2 h [9]. The bactericidal ability of Ag-NPs synthesized by S. polyanthum leaves extract entirely killed most foodborne pathogens after 4 h of incubation at 4 × MIC concentration [156]. AgNPs reduced the number of the bacterial cells by more than 3 log10 when compared to the initial inoculum [157]. Based on the results, the tested gram negative bacteria were able to kill in a shorter time at low concentration of Ag-Carth-NPs compere with positive bacteria and fungi. This may be attributed to the composition of bacteria's cell walls. Compared to gram positive bacteria, gram negative bacteria have a distinct cell wall structure, an outer membrane made of lipopolysaccharide, a thin layer of peptidoglycan, and a cytoplasmic membrane [158]. Due to their potent biocidal impact against pathogens, silver nanoparticles are widely recognized as among the most common antimicrobial agents [159] and AgNPs have been used as anti-fungal [160]. The smaller NPs have a higher surface area than bigger ones; they may be more bactericidal to bacteria and exhibit superior bactericidal effects because they can more easily attach to the cell wall and penetrate the bacterial cell [161].

Motility of P. aeruginosa

The sub-MIC inhibitory effect of Ag-Carth-NPs on different types of virulence factors in P. aeruginosa was investigated (Selected because is more resistant strain to control antibiotic and high sensitive to Ag-Carth-NPs). The Ag-Carth-NPs had a significant influence on the swarming, motility of P. aeruginosa when they were present at concentrations of 1.56 μg/ml as compared to the untreated controls as shown in (Figure 4a). Ag-Carth-NPs show maximum inhibition of swarming motility about 84.23% in compere with control (untreated samples). Since P. aeruginosa motility, which includes properties like swarming, promotes more biofilm development and the surface attachment process [162]. In contrast Ag-Carth-NPs showed a remarkable reduction in bacterial swimming (by 86.59%) after treatment with Ag-Carth-NPs (Figure 4b).Fig. 4 a Swarming motility inhibition of P. aeruginosa by sub-MICs of Ag-Carth-NPs, b Swimming motility inhibition of P. aeruginosa by sub-MICs of Ag-Carth-NPs, c Pyocyanin production inhibition of P. aeruginosa by sub-MICs of Ag-Carth-NPs and d Proteases production inhibition of P. aeruginosa by sub-MICs of Ag-Carth-NPs. Mean values with standard deviation (error bars) with *, **, ***are statistically different from the respective control at P < 0.05, P < 0.01, and P < 0.001, respectively; (One way ANOVA, Tukey test)

One potential strategy for managing biofilm and infections is to use NPs to reduce microbial motility [163]. Ag-Carth-NPs effectively reduce swarming motility at sub-MIC levels, which is similar with the previous NPs inhibitory effects when made from other natural products [164]. The biosynthesized Ag-NPs have been observed to decrease the swarming motility and biofilm formation in P. aeruginosa [147]. Silver metformin nanostructure show swarming motility inhibition by about (88.87–94.16%) [50]. The previous study demonstrated that AgNPs show 42–81 % reduction in motility behavior of P. aeruginosa [145]. It has also been shown that the sub-MIC level of Ag-Carth-NPs inhibits the formation of biofilm in P. aeruginosa, as well as inhibits the swarming motility activity.

Pyocyanin level

Treating of P. aeruginosa with Ag-Carth-NPs reduced by 78.71% (Figure 4c); Based on results of ANOVA, it was found that, the of OD value of pyocyanin produced by P. aeruginosa was significantly reduced compared to the control (untreated sample). Treatment of Pseudomonas aeruginosa with the Ag-NPs (0.5–1 μg/mL) resulted in a significant a significant decrease of production of pyocyanin [165]. In a study, Khan et al, showed that the production of P. aeruginosa PAO1 KCTC 1637 pyocyanin at gold nanoparticles concentrations of 0.032, 0.128 and 0.256 mg/ml decreased 79.4, 81.9, and 87.7%, respectively compared to the control [164]. Comparable to the findings of this investigation, demonstrated the impact of nanoparticles on decreasing P. aeruginosa pyocyanin production [166]. Thus, without influencing bacterial growth or starting resistance selection, pyocyanin decrease can be thought of as an effective way to reduce the pathogenicity and colonization of P. aeruginosa [167].

Total protease production

The ability of the Ag-Carth-NPs to inhibit proteolytic activity was measured using the modified skimmed milk broth method. It was found that the inhibitory activity of Ag-Carth-NPs is 73.8% in compere with control (Figure 4d). Proteases destroy immune globulins and fibrin as well as they disrupts epithelial tight junctions [168]. Nanoparticles has significant capability to inhibit P. aerouginosa Proteases production [169]. Significantly reduced the levels of total protease by biologically Synthesized gold and selenium Nanoparticles [48].

Virulence attenuating properties of Ag-Carth-NPs against P.aeruginosa

Conventional PCR for virulence genes screening

Upon screening of the major P. aerugenosae virulence genes, the isolate was positive for exoU, phzM, toxA and lasB showing bands at 134, 875, 396, and 1220 bp, respectively. Therefore, this clinical isolate can be identified as a hypervirulent strain (Figure 5a). Previous study confirm virulence genes, of ExoU, ExoS, phzM, toxA, and lasB genes are present in P. aeruginosa isolate [170]. The presence of different virulence genes in P. aeruginosa isolates indicates that these strains have a relationship to various levels of intrinsic pathogenicity and virulence[171]. The phz, lasB, toxA, exoS and exoU genes were detected in P. aeruginosa strains exhibit high antimicrobial resistance [172].Fig. 5 a Screening of the major P. aerugenosae virulence genes and b RT-qPCR showed reduced expression of lasR, exoU, phzM, toxA and lasB with the Ag-Carth-NPs in sub-MICs compared to untreated controls. Mean values with standard deviation (error bars) with *, **, ***are statistically different from the respective control at P < 0.05, P < 0.01, and P < 0.001, respectively; (One way ANOVA, Tukey test)

Assessment of the effect of of Ag-Carth-NPs genes using qRT‑PCR

The DNA extract were tested for the presence of the five exotoxin genes (lasR, exoU, phzM, toxA and lasB) in P. aeruginosa using specific primers by multiplex PCR. A variety of virulence factors play a role in the pathogenesis of P. aeruginosa [45]. The inhibition of the expression of P. aeruginosa virulence genes (lasR, exoU, phzM, toxA and lasB) were assessed by qRT-PCR after 24 h of treatment with 1.562 µg/ml Ag-Carth-NPs. The expression levels of lasR, exoU, phzM, toxA and lasB were significantly decreased after treatment with sub-MICs of the Ag-Carth-NPs compared to controls (Figure 5b). The results show, ToxA gene expression was significantly downregulated by 81.5%, while exoU gene expression reduced by 78.1%. The percentage inhibition in lasR gene expression was 68%, while the reduction in exoU was 66%. Furthermore, there was a 60.1% decrease in lasB gene expression.

Biogenic synthesized Ag-NP show a significant reduction in LasB production by P. aeruginosa [173]. The expression of QS regulatory genes (lasI, lasR, rhlI, rhlR, and fabH2) in P. aeruginosa PAO1 was suppressed by AgNPs, according to Singh et al, [174]. The combination of AgNPs and 4-nitropyridine N-oxide can inhibit the expression genes (lasI, lasR, rhlI, rhlR, pqsA, and pqsR) [175]. A significant reduction in virulence gene expression was observed with chemical synthesized AgNPs [50, 176]. Previous study refer to Ag-CNTs, the expression levels of the rpoS, rsmZ, and oprD genes were significantly down regulated in P. aeruginosa compared to the untreated samples [51]. These results suggest that the mechanism of action may be attributed to their effect on cell-membrane integrity, down regulation of virulence-gene expression, and induction of general and oxidative stress in P. aeruginosa

Ag nanoparticles (NPs), exhibits superior ion release per unit mass, essentially owing to the augmented effective surface area. The dynamic correlation between nanoscale effects and Ag(I) ions contributes to the enhanced antimicrobial efficacy of Ag-NPs compared to their bulk counterparts [177]. It raises three probable antimicrobial mechanisms in Ag-NPs, including Ag-NPs as a reservoir for Ag(I) ions, particle only effects, and synergistic effects due to the combination of the first two mechanisms [178]. Synergistic antimicrobial mechanism, in which the NPs are absorbed intracellular and endure subsequent leaching of Ag+, raising local ion concentrations, resulting in physical interference or disruption of the phospholipid cell membrane and ROS generation at the surface of cell biomolecules [179]. This leads to damage the biomolecules such as enzymes, proteins and DNA, resulting in bacterial cell death [180].

Possible strategies for Ag-Carth-NPs from the environment

There is extensive research on the application of Nano based materials and the consequences of their release into the environment. However, there is little information about environmentally friendly approaches for removing nanomaterial’s from the environment [181]. Nanomaterial’s especially AgNPs affect soil properties, microorganisms, and plants and can therefore cause toxicity for living organisms including humans. However, there is little information about environmentally friendly approaches for removing nanomaterials from the environment. The possibility of remediation of Ag-Carth-NPs using phytotechnology approaches. Phytotechnology refers to a technology that uses plants to remove, uptake, absorb, transform, transfer, attenuate, accumulate, degrade, or metabolite organic, inorganic, metallic, or metalloid contaminants from soil, water, or air [182]. The term phytotechnology refers to a group of sub-disciplines of scientific study that include phytoextraction, phytosequestration, phytovolatilization, phytodegradation, and phytoremediation. The terms phytotechnology and phytoremediation are synonymous, however the latter term usually designates a phytotechnological process that eliminates contaminants from the surrounding environment. By storing contaminants in plant biomass to assure environmental safety, phytoremediation is a natural, easy, affordable, and widely used bioremediation approach that uses the principles of a plant’s metabolic system to clean, recover, and remediate contaminated environments [183].

Cytotoxicity of Ag-Carth-NPs

The potential application of Ag-Carth-NPs as antimicrobial agent must be taken into account that it is not harmful to the normal. The results in this, Ag-Carth-NPs have no significant cytotoxic effects on normal human cell (Hfb4) at different concentration ranged from 100 to 1.56 (Figure 6) this indicates Ag-Carth-NPs are safe against human normal cells. The anticancer efficacy of Ag-Carth-NPs has been investigated against HepG-2 cells (human Hepatocellular carcinoma). As the concentrations of Ag-Carth-NPs increased, cell viability decreased, meaning cytotoxicity increased (Figure 6). Data analysis confirms that the IC50 value of Ag-Carth-NPs against HepG-2 cells is 5.6 µg/ml.Fig. 6 Cytotoxicity of Ag-Carth-NPs against Hfb4 cells (normal skin cell lines) and HepG-2 cells (human Hepatocellular carcinoma). Ag-Carth-NPs have no cytotoxic effects on the normal tested cell lines. IC50 value of Ag-Carth-NPs against HepG-2 cell lines is 5.6 µg/mL. Mean values with standard deviation (error bars) with *, **, ***are statistically different from the respective control at P < 0.05, P < 0.01, and P < 0.001, respectively; (One way ANOVA, Tukey test)

Ag-NP exposure may cause morphological abnormalities in cells, decrease viability in cells, increase the release of lactate dehydrogenase (LDH), and ultimately cause necrosis and apoptosis in cells. The direct result of AgNP-induced oxidative stress and Ag ion release is cytotoxicity [184]. Biologically synthesized Ag-NP were also proved to exhibit excellent cytotoxic effect on MCF-7 and HT-29 [185]. Human body can tolerate 0.4 to 27 μg of AgNPs per day when consumed through the oral route [186]. Human cells were found to have a greater resistance to the toxic effects of silver nanoparticles in comparison with other cells [187]. Green synthesized AgNPs are biocompatible and do not harm normally functioning human or host cells [188].

Conclusion

In the present study, a facile biological technology is used for Ag-Carth-NPs synthesis in the presence of Silver nitrate and Carthamus tenuis extract. The synthesized Ag-Carth-NPs demonstrated spherical particles with 20  ±  1.22 nm, high stability with zeta potential around – 43 mV and FTIR spectroscopy indicated the presence of various functional biological groups that responsible for stabilization of Ag-Carth-NPs. Antimicrobial results revealed that Ag-Carth-NPs has inhibition zone ranged (27 ± 0.30 to 21 ± 0.14 mm) and anti-biofilm formation activities ranged (40.21 to 90.12%) against tested bacteria and fungi. The values of MIC and MBC ranged between 3.126 and 25 and 6.25–50 μg/ml, respectively. Ag-Carth-NPs inhibit the growth of the tested microorganisms at 2MIC after times ranging from 1 h to 2 h. Furthermore Ag-Carth-NPs reduce swarming, swimming motility, pyocyanin and protease production of P. aeruginosa in comparison with the control (untreated). The results show, P. aeruginosa ToxA gene expression was significantly down regulated by 81.5%, while exoU gene expression was reduced by 78.1%. The percentage inhibition in lasR gene expression was 68%, while the reduction in exoU was 66%. Furthermore, there was a 60.1% decrease in lasB gene expression. Ag-Carth-NPs have no significant cytotoxic effects on normal human cell (Hfb4) but have IC50 at 5.6 µg/ml against of HepG-2 cells. Further carefully designed studies should be taken taking into account such as, pharmacokinetic, and formulation of gel based Ag-Carth-NPs are necessary to demonstrate the possibility usage as a promising novel drug for combating pathogenic microbes in topical form.

Supplementary Information

Additional file 1.

Acknowledgements

The authors would like to thank Drug Microbiology Lab, Drug Radiation Research Department, National Center for Radiation Research and Technology (NCRRT), Egypt and Radiation Microbiology Department, National Center for Radiation Research and Technology (NCRRT), Egyptian Atomic Energy Authority (EAEA), Cairo, Egypt as well as microbiology and immunology department, faculty of pharmacy Ahram Canadian University.

Author contributions

All authors have contributed to conception and design or the acquisition and analysis of Data and approval of the final submitted version and drafting or critically revising the manuscript.

Funding

Open access funding provided by The Science, Technology & Innovation Funding Authority (STDF) in cooperation with The Egyptian Knowledge Bank (EKB). No funding provided.

Availability of data and materials

The data and materials that support the findings of this study are available from the corresponding author, upon reasonable request. No datasets were generated or analysed during the current study.

Declarations

Ethics approval and consent to participate

All experimental protocols were done following the ethical standards adopted by National Center for Radiation Research.

Consent for publication

All authors agree to participate and publish

Competing interests

The authors declare there is no competing interests.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
==== Refs
References

1. Faisal S Tariq MH Abdullah Zafar S Un Nisa Z Ullah R Ur Rahman A Bari A Ullah K Khan RU Bio synthesis, comprehensive characterization, and multifaceted therapeutic applications of BSA-resveratrol coated platinum nanoparticles Sci Rep 2024 14 7875 10.1038/s41598-024-57787-4 38570564
Faisal S, Tariq MH, Abdullah, Zafar S, Un Nisa Z, Ullah R, Ur Rahman A, Bari A, Ullah K, Khan RU. Bio synthesis, comprehensive characterization, and multifaceted therapeutic applications of BSA-resveratrol coated platinum nanoparticles. Sci Rep. 2024;14:7875.38570564 10.1038/s41598-024-57787-4
2. Zafar S Faisal S Jan H Ullah R Rizwan M Abdullah Alotaibi A Bibi N Rashid AU Khattak A Development of iron nanoparticles (FeNPs) using biomass of enterobacter: Its characterization, antimicrobial, anti-Alzheimer’s, and enzyme inhibition potential Micromachines 2022 13 1259 10.3390/mi13081259 36014181
Zafar S, Faisal S, Jan H, Ullah R, Rizwan M, Abdullah, Alotaibi A, Bibi N, Rashid AU, Khattak A. Development of iron nanoparticles (FeNPs) using biomass of enterobacter: Its characterization, antimicrobial, anti-Alzheimer’s, and enzyme inhibition potential. Micromachines. 2022;13:1259.36014181 10.3390/mi13081259
3. Dhanalakshmi M Losetty V Investigation of antibacterial, antioxidant, cytotoxicity and photocatalytic dye degradation activity of green synthesized copper oxide nanoparticles using Ceropegia debilis plant extract Clean Technol Environ Policy 2024 10.1007/s10098-024-02776-4
Dhanalakshmi M, Losetty V. Investigation of antibacterial, antioxidant, cytotoxicity and photocatalytic dye degradation activity of green synthesized copper oxide nanoparticles using Ceropegia debilis plant extract. Clean Technol Environ Policy. 2024. 10.1007/s10098-024-02776-4.10.1007/s10098-024-02776-4
4. Saqib S Nazeer A Ali M Zaman W Younas M Shahzad A Sunera Nisar M Catalytic potential of endophytes facilitates synthesis of biometallic zinc oxide nanoparticles for agricultural application Biometals 2022 35 967 985 10.1007/s10534-022-00417-1 35834149
Saqib S, Nazeer A, Ali M, Zaman W, Younas M, Shahzad A, Sunera, Nisar M. Catalytic potential of endophytes facilitates synthesis of biometallic zinc oxide nanoparticles for agricultural application. Biometals. 2022;35:967–85.35834149 10.1007/s10534-022-00417-1
5. Behravan M Panahi AH Naghizadeh A Ziaee M Mahdavi R Mirzapour A Facile green synthesis of silver nanoparticles using Berberis vulgaris leaf and root aqueous extract and its antibacterial activity Int J Biol Macromol 2019 124 148 154 10.1016/j.ijbiomac.2018.11.101 30447360
Behravan M, Panahi AH, Naghizadeh A, Ziaee M, Mahdavi R, Mirzapour A. Facile green synthesis of silver nanoparticles using Berberis vulgaris leaf and root aqueous extract and its antibacterial activity. Int J Biol Macromol. 2019;124:148–54.30447360 10.1016/j.ijbiomac.2018.11.101
6. Kumar B Smita K Cumbal L Debut A Green synthesis of silver nanoparticles using Andean blackberry fruit extract Saudi J Biol Sci 2017 24 45 50 10.1016/j.sjbs.2015.09.006 28053570
Kumar B, Smita K, Cumbal L, Debut A. Green synthesis of silver nanoparticles using Andean blackberry fruit extract. Saudi J Biol Sci. 2017;24:45–50.28053570 10.1016/j.sjbs.2015.09.006
7. Ullah R Shah S Muhammad Z Shah SA Faisal S Khattak U Haq TU Taj Akbar M In vitro and in vivo applications of Euphorbia wallichii shoot extract-mediated gold nanospheres Green Process Synth 2021 10 101 111 10.1515/gps-2021-0013
Ullah R, Shah S, Muhammad Z, Shah SA, Faisal S, Khattak U, Haq TU, Taj Akbar M. In vitro and in vivo applications of Euphorbia wallichii shoot extract-mediated gold nanospheres. Green Process Synth. 2021;10:101–11.10.1515/gps-2021-0013
8. Faisal S Abdullah Jan H Shah SA Shah S Rizwan M Zaman N Hussain Z Uddin MN Bibi N Bio-catalytic activity of novel Mentha arvensis intervened biocompatible magnesium oxide nanomaterials Catalysts 2021 11 780 10.3390/catal11070780
Faisal S, Abdullah, Jan H, Shah SA, Shah S, Rizwan M, Zaman N, Hussain Z, Uddin MN, Bibi N. Bio-catalytic activity of novel Mentha arvensis intervened biocompatible magnesium oxide nanomaterials. Catalysts. 2021;11:780.10.3390/catal11070780
9. Loo YY Rukayadi Y Nor-Khaizura MAR Kuan CH Chieng BW Nishibuchi M Radu S In vitro antimicrobial activity of green synthesized silver nanoparticles against selected gram-negative foodborne pathogens Front Microbiol 2018 9 1555 10.3389/fmicb.2018.01555 30061871
Loo YY, Rukayadi Y, Nor-Khaizura MAR, Kuan CH, Chieng BW, Nishibuchi M, Radu S. In vitro antimicrobial activity of green synthesized silver nanoparticles against selected gram-negative foodborne pathogens. Front Microbiol. 2018;9:1555.30061871 10.3389/fmicb.2018.01555
10. Karthik L Kirthi AV Ranjan S Srinivasan VM Biological synthesis of nanoparticles and their applications 2019 Boca Raton CRC Press
Karthik L, Kirthi AV, Ranjan S, Srinivasan VM. Biological synthesis of nanoparticles and their applications. Boca Raton: CRC Press; 2019.
11. Faisal S Khan S Abdullah Zafar S Rizwan M Ali M Ullah R Albadrani GM Mohamed HR Akbar F Fagonia cretica-mediated synthesis of manganese oxide (MnO2) nanomaterials their characterization and evaluation of their bio-catalytic and enzyme inhibition potential for maintaining flavor and texture in apples Catalysts 2022 12 558 10.3390/catal12050558
Faisal S, Khan S, Abdullah, Zafar S, Rizwan M, Ali M, Ullah R, Albadrani GM, Mohamed HR, Akbar F. Fagonia cretica-mediated synthesis of manganese oxide (MnO2) nanomaterials their characterization and evaluation of their bio-catalytic and enzyme inhibition potential for maintaining flavor and texture in apples. Catalysts. 2022;12:558.10.3390/catal12050558
12. Tareq M Khadrawy YA Rageh MM Mohammed HS Dose-dependent biological toxicity of green synthesized silver nanoparticles in rat’s brain Sci Rep 2022 12 22642 10.1038/s41598-022-27171-1 36587179
Tareq M, Khadrawy YA, Rageh MM, Mohammed HS. Dose-dependent biological toxicity of green synthesized silver nanoparticles in rat’s brain. Sci Rep. 2022;12:22642.36587179 10.1038/s41598-022-27171-1
13. Antunes Filho S Dos Santos MS Dos Santos OAL Backx BP Soran M-L Opriş O Lung I Stegarescu A Bououdina M Biosynthesis of nanoparticles using plant extracts and essential oils Molecules 2023 28 3060 10.3390/molecules28073060 37049821
Antunes Filho S, Dos Santos MS, Dos Santos OAL, Backx BP, Soran M-L, Opriş O, Lung I, Stegarescu A, Bououdina M. Biosynthesis of nanoparticles using plant extracts and essential oils. Molecules. 2023;28:3060.37049821 10.3390/molecules28073060
14. Mosallam FM El-Sayyad GS Fathy RM El-Batal AI Biomolecules-mediated synthesis of selenium nanoparticles using Aspergillus oryzae fermented Lupin extract and gamma radiation for hindering the growth of some multidrug-resistant bacteria and pathogenic fungi Microb Pathog 2018 122 108 116 10.1016/j.micpath.2018.06.013 29894810
Mosallam FM, El-Sayyad GS, Fathy RM, El-Batal AI. Biomolecules-mediated synthesis of selenium nanoparticles using Aspergillus oryzae fermented Lupin extract and gamma radiation for hindering the growth of some multidrug-resistant bacteria and pathogenic fungi. Microb Pathog. 2018;122:108–16.29894810 10.1016/j.micpath.2018.06.013
15. Alwhibi MS Soliman DA Awad MA Rizwana H Marraiki NA Biosynthesis of silver nanoparticles using fenugreek seed extract and evaluation of their antifungal and antibacterial activities J Comput Theor Nanosci 2018 15 1255 1260 10.1166/jctn.2018.7301
Alwhibi MS, Soliman DA, Awad MA, Rizwana H, Marraiki NA. Biosynthesis of silver nanoparticles using fenugreek seed extract and evaluation of their antifungal and antibacterial activities. J Comput Theor Nanosci. 2018;15:1255–60.10.1166/jctn.2018.7301
16. dos Santos Souza LM Dibo M Sarmiento JJP Seabra AB Medeiros LP Lourenço IM Kobayashi RKT Nakazato G Biosynthesis of selenium nanoparticles using combinations of plant extracts and their antibacterial activity Curr Res Green Sustain Chem 2022 5 100303 10.1016/j.crgsc.2022.100303
dos Santos Souza LM, Dibo M, Sarmiento JJP, Seabra AB, Medeiros LP, Lourenço IM, Kobayashi RKT, Nakazato G. Biosynthesis of selenium nanoparticles using combinations of plant extracts and their antibacterial activity. Curr Res Green Sustain Chem. 2022;5:100303.10.1016/j.crgsc.2022.100303
17. Alshammari SO Mahmoud SY Farrag ES Synthesis of green copper nanoparticles using medicinal plant Krameria sp. Root extract and its applications Molecules 2023 28 4629 10.3390/molecules28124629 37375184
Alshammari SO, Mahmoud SY, Farrag ES. Synthesis of green copper nanoparticles using medicinal plant Krameria sp. Root extract and its applications. Molecules. 2023;28:4629.37375184 10.3390/molecules28124629
18. Farooqui MA Chauhan PS Krishnamoorthy P Shaik J Extraction of silver nanoparticles from the leaf extracts of Clerodendrum inerme Dig J Nanomater Biostruct 2010 5 43 49
Farooqui MA, Chauhan PS, Krishnamoorthy P, Shaik J. Extraction of silver nanoparticles from the leaf extracts of Clerodendrum inerme. Dig J Nanomater Biostruct. 2010;5:43–9.
19. Vilatersana R Garnatje T Susanna A Garcia-Jacas N Taxonomic problems in Carthamus (Asteraceae): RAPD markers and sectional classification Bot J Linn Soc 2005 147 375 383 10.1111/j.1095-8339.2005.00375.x
Vilatersana R, Garnatje T, Susanna A, Garcia-Jacas N. Taxonomic problems in Carthamus (Asteraceae): RAPD markers and sectional classification. Bot J Linn Soc. 2005;147:375–83.10.1111/j.1095-8339.2005.00375.x
20. Azab A Total phenolic content, antioxidant capacity and antifungal activity of extracts of Carthamus tenuis and Cephalaria joppensis Eur Chem Bull 2018 7 156 161 10.17628/ecb.2018.7.156-161
Azab A. Total phenolic content, antioxidant capacity and antifungal activity of extracts of Carthamus tenuis and Cephalaria joppensis. Eur Chem Bull. 2018;7:156–61.10.17628/ecb.2018.7.156-161
21. Kuete V Wiench B Hegazy MEF Mohamed TA Fankam AG Shahat AA Efferth T Antibacterial activity and cytotoxicity of selected Egyptian medicinal plants Plant Med 2012 78 193 199 10.1055/s-0031-1280319
Kuete V, Wiench B, Hegazy MEF, Mohamed TA, Fankam AG, Shahat AA, Efferth T. Antibacterial activity and cytotoxicity of selected Egyptian medicinal plants. Plant Med. 2012;78:193–9.10.1055/s-0031-1280319
22. Rodríguez-Félix F López-Cota AG Moreno-Vásquez MJ Graciano-Verdugo AZ Quintero-Reyes IE Del-Toro-Sánchez CL Tapia-Hernández JA Sustainable-green synthesis of silver nanoparticles using safflower (Carthamus tinctorius L.) waste extract and its antibacterial activity Heliyon 2021 10.1016/j.heliyon.2021.e06923 34007921
Rodríguez-Félix F, López-Cota AG, Moreno-Vásquez MJ, Graciano-Verdugo AZ, Quintero-Reyes IE, Del-Toro-Sánchez CL, Tapia-Hernández JA. Sustainable-green synthesis of silver nanoparticles using safflower (Carthamus tinctorius L.) waste extract and its antibacterial activity. Heliyon. 2021. 10.1016/j.heliyon.2021.e06923.34007921 10.1016/j.heliyon.2021.e06923
23. Rodríguez-Félix F Graciano-Verdugo AZ Moreno-Vásquez MJ Lagarda-Díaz I Barreras-Urbina CG Armenta-Villegas L Olguín-Moreno A Tapia-Hernández JA Trends in sustainable green synthesis of silver nanoparticles using agri-food waste extracts and their applications in health J Nanomater 2022 2022 8874003 10.1155/2022/8874003
Rodríguez-Félix F, Graciano-Verdugo AZ, Moreno-Vásquez MJ, Lagarda-Díaz I, Barreras-Urbina CG, Armenta-Villegas L, Olguín-Moreno A, Tapia-Hernández JA. Trends in sustainable green synthesis of silver nanoparticles using agri-food waste extracts and their applications in health. J Nanomater. 2022;2022:8874003.10.1155/2022/8874003
24. Zhou XiDan ZX Tang LiYing TL Xu YiLong XY Zhou GuoHong ZG Wang ZhuJu WZ Towards a better understanding of medicinal uses of Carthamus tinctorius L. in traditional Chinese medicine: a phytochemical and pharmacological review J Ethnopharmacol 2014 15 27 43 10.1016/j.jep.2013.10.050
Zhou XiDan ZX, Tang LiYing TL, Xu YiLong XY, Zhou GuoHong ZG, Wang ZhuJu WZ. Towards a better understanding of medicinal uses of Carthamus tinctorius L. in traditional Chinese medicine: a phytochemical and pharmacological review. J Ethnopharmacol. 2014;15:27–43.10.1016/j.jep.2013.10.050
25. El-Hela A Ibrahim T Abdel-Hady N Al-Massarani S Abd-Allah G Phytochemical and biological investigation of Carthamus tenuis Boiss. growing in Egypt Planta Med 2013 79 PN46 10.1055/s-0033-1352389
El-Hela A, Ibrahim T, Abdel-Hady N, Al-Massarani S, Abd-Allah G. Phytochemical and biological investigation of Carthamus tenuis Boiss. growing in Egypt. Planta Med. 2013;79:PN46.10.1055/s-0033-1352389
26. Negi PS Plant extracts for the control of bacterial growth: Efficacy, stability and safety issues for food application Int J Food Microbiol 2012 156 7 17 10.1016/j.ijfoodmicro.2012.03.006 22459761
Negi PS. Plant extracts for the control of bacterial growth: Efficacy, stability and safety issues for food application. Int J Food Microbiol. 2012;156:7–17.22459761 10.1016/j.ijfoodmicro.2012.03.006
27. Davidson PM Taylor TM Schmidt SE Chemical preservatives and natural antimicrobial compounds Food Microbiol Fundam Front 2012 10.1128/9781555818463.ch30
Davidson PM, Taylor TM, Schmidt SE. Chemical preservatives and natural antimicrobial compounds. Food Microbiol Fundam Front. 2012. 10.1128/9781555818463.ch30.10.1128/9781555818463.ch30
28. Lahiri D Nag M Sheikh HI Sarkar T Edinur HA Pati S Ray RR Microbiologically-synthesized nanoparticles and their role in silencing the biofilm signaling cascade Front Microbiol 2021 12 636588 10.3389/fmicb.2021.636588 33717030
Lahiri D, Nag M, Sheikh HI, Sarkar T, Edinur HA, Pati S, Ray RR. Microbiologically-synthesized nanoparticles and their role in silencing the biofilm signaling cascade. Front Microbiol. 2021;12:636588.33717030 10.3389/fmicb.2021.636588
29. Saqib S Faryad S Afridi MI Arshad B Younas M Naeem M Zaman W Ullah F Nisar M Ali S Bimetallic assembled silver nanoparticles impregnated in Aspergillus fumigatus extract damage the bacterial membrane surface and release cellular contents Coatings 2022 12 1505 10.3390/coatings12101505
Saqib S, Faryad S, Afridi MI, Arshad B, Younas M, Naeem M, Zaman W, Ullah F, Nisar M, Ali S. Bimetallic assembled silver nanoparticles impregnated in Aspergillus fumigatus extract damage the bacterial membrane surface and release cellular contents. Coatings. 2022;12:1505.10.3390/coatings12101505
30. Saqib S Zaman W Ullah F Majeed I Ayaz A Hussain Munis MF Organometallic assembling of chitosan-Iron oxide nanoparticles with their antifungal evaluation against Rhizopus oryzae Appl Organomet Chem 2019 33 e5190 10.1002/aoc.5190
Saqib S, Zaman W, Ullah F, Majeed I, Ayaz A, Hussain Munis MF. Organometallic assembling of chitosan-Iron oxide nanoparticles with their antifungal evaluation against Rhizopus oryzae. Appl Organomet Chem. 2019;33: e5190.10.1002/aoc.5190
31. Dhaka A Mali SC Sharma S Trivedi R A review on biological synthesis of silver nanoparticles and their potential applications Result Chem 2023 6 101108 10.1016/j.rechem.2023.101108
Dhaka A, Mali SC, Sharma S, Trivedi R. A review on biological synthesis of silver nanoparticles and their potential applications. Result Chem. 2023;6:101108.10.1016/j.rechem.2023.101108
32. Dutt Y Pandey RP Dutt M Gupta A Vibhuti A Raj VS Chang C-M Priyadarshini A Silver nanoparticles phytofabricated through Azadirachta indica: anticancer, apoptotic, and wound-healing properties Antibiotics 2023 12 121 10.3390/antibiotics12010121 36671322
Dutt Y, Pandey RP, Dutt M, Gupta A, Vibhuti A, Raj VS, Chang C-M, Priyadarshini A. Silver nanoparticles phytofabricated through Azadirachta indica: anticancer, apoptotic, and wound-healing properties. Antibiotics. 2023;12:121.36671322 10.3390/antibiotics12010121
33. Ahmad A Haneef M Ahmad N Kamal A Jaswani S Khan F Biological synthesis of silver nanoparticles and their medical applications World Acad Sci J 2024 6 1 9 10.3892/wasj.2024.237
Ahmad A, Haneef M, Ahmad N, Kamal A, Jaswani S, Khan F. Biological synthesis of silver nanoparticles and their medical applications. World Acad Sci J. 2024;6:1–9.10.3892/wasj.2024.237
34. Yin IX Zhang J Zhao IS Mei ML Li Q Chu CH The antibacterial mechanism of silver nanoparticles and its application in dentistry Int J Nanomed 2020 15 2555 2562 10.2147/IJN.S246764
Yin IX, Zhang J, Zhao IS, Mei ML, Li Q, Chu CH. The antibacterial mechanism of silver nanoparticles and its application in dentistry. Int J Nanomed. 2020;15:2555–62.10.2147/IJN.S246764
35. Selem E Mekky AF Hassanein WA Reda FM Selim YA Antibacterial and antibiofilm effects of silver nanoparticles against the uropathogen Escherichia coli U12 Saudi J Biol Sci 2022 29 103457 10.1016/j.sjbs.2022.103457 36267912
Selem E, Mekky AF, Hassanein WA, Reda FM, Selim YA. Antibacterial and antibiofilm effects of silver nanoparticles against the uropathogen Escherichia coli U12. Saudi J Biol Sci. 2022;29:103457.36267912 10.1016/j.sjbs.2022.103457
36. Barabadi H Hosseini O Jounaki K Sadeghian-Abadi S Ashouri F Alrikabi AMA Vahidi H Amidi S Mojab F Mohammadi N Bioinspired green-synthesized silver nanoparticles: in vitro physicochemical, antibacterial, biofilm inhibitory, genotoxicity, antidiabetic, antioxidant, and anticoagulant performance Mater Adv 2023 4 3037 3054 10.1039/D3MA00089C
Barabadi H, Hosseini O, Jounaki K, Sadeghian-Abadi S, Ashouri F, Alrikabi AMA, Vahidi H, Amidi S, Mojab F, Mohammadi N. Bioinspired green-synthesized silver nanoparticles: in vitro physicochemical, antibacterial, biofilm inhibitory, genotoxicity, antidiabetic, antioxidant, and anticoagulant performance. Mater Adv. 2023;4:3037–54.10.1039/D3MA00089C
37. Seo M Oh T Bae S Antibiofilm activity of silver nanoparticles against biofilm forming Staphylococcus pseudintermedius isolated from dogs with otitis externa Vet Med Sci 2021 7 1551 1557 10.1002/vms3.554 34156766
Seo M, Oh T, Bae S. Antibiofilm activity of silver nanoparticles against biofilm forming Staphylococcus pseudintermedius isolated from dogs with otitis externa. Vet Med Sci. 2021;7:1551–7.34156766 10.1002/vms3.554
38. Boakye YD Osafo N Danquah CA Adu F Agyare C Antimicrobial agents: antibacterial agents, anti-biofilm agents, antibacterial natural compounds, and antibacterial chemicals Antimicrob Antibiot Res Antib Strateg Activity Methods 2019 13 75
Boakye YD, Osafo N, Danquah CA, Adu F, Agyare C. Antimicrobial agents: antibacterial agents, anti-biofilm agents, antibacterial natural compounds, and antibacterial chemicals. Antimicrob Antibiot Res Antib Strateg Activity Methods. 2019;13:75.
39. Mi G Shi D Wang M Webster TJ Reducing bacterial infections and biofilm formation using nanoparticles and nanostructured antibacterial surfaces Adv Healthcare Mater 2018 7 1800103 10.1002/adhm.201800103
Mi G, Shi D, Wang M, Webster TJ. Reducing bacterial infections and biofilm formation using nanoparticles and nanostructured antibacterial surfaces. Adv Healthcare Mater. 2018;7:1800103.10.1002/adhm.201800103
40. Cortés ME Bonilla JC Sinisterra RD Biofilm formation, control and novel strategies for eradication Sci Against Microbial Pathog Commun Curr Res Technol Adv 2011 2 896 905
Cortés ME, Bonilla JC, Sinisterra RD. Biofilm formation, control and novel strategies for eradication. Sci Against Microbial Pathog Commun Curr Res Technol Adv. 2011;2:896–905.
41. Strateva T Mitov I Contribution of an arsenal of virulence factors to pathogenesis of Pseudomonas aeruginosa infections Ann Microbiol 2011 61 717 732 10.1007/s13213-011-0273-y
Strateva T, Mitov I. Contribution of an arsenal of virulence factors to pathogenesis of Pseudomonas aeruginosa infections. Ann Microbiol. 2011;61:717–32.10.1007/s13213-011-0273-y
42. Høiby N Bjarnsholt T Givskov M Molin S Ciofu O Antibiotic resistance of bacterial biofilms Int J Antimicrob Agents 2010 35 322 332 10.1016/j.ijantimicag.2009.12.011 20149602
Høiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O. Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents. 2010;35:322–32.20149602 10.1016/j.ijantimicag.2009.12.011
43. Bowler PG Antibiotic resistance and biofilm tolerance: a combined threat in the treatment of chronic infections J Wound Care 2018 27 273 277 10.12968/jowc.2018.27.5.273 29738295
Bowler PG. Antibiotic resistance and biofilm tolerance: a combined threat in the treatment of chronic infections. J Wound Care. 2018;27:273–7.29738295 10.12968/jowc.2018.27.5.273
44. Urgancı NN Yılmaz N Alaşalvar GK Yıldırım Z Pseudomonas aeruginosa and its pathogenicity Turk J Agric-Food Sci Technol 2022 10 726 738
Urgancı NN, Yılmaz N, Alaşalvar GK, Yıldırım Z. Pseudomonas aeruginosa and its pathogenicity. Turk J Agric-Food Sci Technol. 2022;10:726–38.
45. Qin S Xiao W Zhou C Pu Q Deng X Lan L Liang H Song X Wu M Pseudomonas aeruginosa: pathogenesis, virulence factors, antibiotic resistance, interaction with host, technology advances and emerging therapeutics Signal Transduct Target Ther 2022 7 199 10.1038/s41392-022-01056-1 35752612
Qin S, Xiao W, Zhou C, Pu Q, Deng X, Lan L, Liang H, Song X, Wu M. Pseudomonas aeruginosa: pathogenesis, virulence factors, antibiotic resistance, interaction with host, technology advances and emerging therapeutics. Signal Transduct Target Ther. 2022;7:199.35752612 10.1038/s41392-022-01056-1
46. Kato J Kim H-E Takiguchi N Kuroda A Ohtake H Pseudomonas aeruginosa as a model microorganism for investigation of chemotactic behaviors in ecosystem J Biosci Bioeng 2008 106 1 7 10.1263/jbb.106.1 18691523
Kato J, Kim H-E, Takiguchi N, Kuroda A, Ohtake H. Pseudomonas aeruginosa as a model microorganism for investigation of chemotactic behaviors in ecosystem. J Biosci Bioeng. 2008;106:1–7.18691523 10.1263/jbb.106.1
47. Rocha AJ Barsottini MRDO Rocha RR Laurindo MV Moraes FLLD Rocha SLD Pseudomonas aeruginosa: virulence factors and antibiotic resistance genes Braz Arch Biol Technol 2019 62 e19180503 10.1590/1678-4324-2019180503
Rocha AJ, Barsottini MRDO, Rocha RR, Laurindo MV, Moraes FLLD, Rocha SLD. Pseudomonas aeruginosa: virulence factors and antibiotic resistance genes. Braz Arch Biol Technol. 2019;62: e19180503.10.1590/1678-4324-2019180503
48. Elshaer SL Shaaban MI Inhibition of quorum sensing and virulence factors of Pseudomonas aeruginosa by biologically synthesized gold and selenium nanoparticles Antibiotics 2021 10 1461 10.3390/antibiotics10121461 34943673
Elshaer SL, Shaaban MI. Inhibition of quorum sensing and virulence factors of Pseudomonas aeruginosa by biologically synthesized gold and selenium nanoparticles. Antibiotics. 2021;10:1461.34943673 10.3390/antibiotics10121461
49. Shah S Gaikwad S Nagar S Kulshrestha S Vaidya V Nawani N Pawar S Biofilm inhibition and anti-quorum sensing activity of phytosynthesized silver nanoparticles against the nosocomial pathogen Pseudomonas aeruginosa Biofouling 2019 35 34 49 10.1080/08927014.2018.1563686 30727758
Shah S, Gaikwad S, Nagar S, Kulshrestha S, Vaidya V, Nawani N, Pawar S. Biofilm inhibition and anti-quorum sensing activity of phytosynthesized silver nanoparticles against the nosocomial pathogen Pseudomonas aeruginosa. Biofouling. 2019;35:34–49.30727758 10.1080/08927014.2018.1563686
50. Gomaa SE Shaker GH Mosallam FM Abbas HA Knocking down Pseudomonas aeruginosa virulence by oral hypoglycemic metformin nano emulsion World J Microbiol Biotechnol 2022 38 119 10.1007/s11274-022-03302-8 35644864
Gomaa SE, Shaker GH, Mosallam FM, Abbas HA. Knocking down Pseudomonas aeruginosa virulence by oral hypoglycemic metformin nano emulsion. World J Microbiol Biotechnol. 2022;38:119.35644864 10.1007/s11274-022-03302-8
51. Dosunmu E Chaudhari AA Singh SR Dennis VA Pillai SR Silver-coated carbon nanotubes downregulate the expression of Pseudomonas aeruginosa virulence genes: a potential mechanism for their antimicrobial effect Int J Nanomed 2015 10.2147/IJN.S85219
Dosunmu E, Chaudhari AA, Singh SR, Dennis VA, Pillai SR. Silver-coated carbon nanotubes downregulate the expression of Pseudomonas aeruginosa virulence genes: a potential mechanism for their antimicrobial effect. Int J Nanomed. 2015. 10.2147/IJN.S85219.10.2147/IJN.S85219
52. Ozkan K Bekiroglu H Bayram Y Sagdic O Erbas S In vitro bioaccessibility, antioxidant and antibacterial activities of three different safflower (Carthamus tinctorius L.) genotypes Food Sci Technol 2021 42 e08921 10.1590/fst.08921
Ozkan K, Bekiroglu H, Bayram Y, Sagdic O, Erbas S. In vitro bioaccessibility, antioxidant and antibacterial activities of three different safflower (Carthamus tinctorius L.) genotypes. Food Sci Technol. 2021;42: e08921.10.1590/fst.08921
53. Vladár AE Hodoroaba V-D Characterization of nanoparticles by scanning electron microscopy Characterization of nanoparticles 2020 Amsterdam Elsevier 7 27
Vladár AE, Hodoroaba V-D. Characterization of nanoparticles by scanning electron microscopy. In: Characterization of nanoparticles. Amsterdam: Elsevier; 2020. p. 7–27.
54. El-Batal AI Nasser HA Mosallam FM Fabrication and characterization of cobalt hyaluronic acid nanostructure via gamma irradiation for improving biomedical applications Int J Biol Macromol 2020 147 1328 1342 10.1016/j.ijbiomac.2019.10.097 31770562
El-Batal AI, Nasser HA, Mosallam FM. Fabrication and characterization of cobalt hyaluronic acid nanostructure via gamma irradiation for improving biomedical applications. Int J Biol Macromol. 2020;147:1328–42.31770562 10.1016/j.ijbiomac.2019.10.097
55. El-Batal AI Mosallam FM El-Sayyad GS Synthesis of metallic silver nanoparticles by fluconazole drug and gamma rays to inhibit the growth of multidrug-resistant microbes J Cluster Sci 2018 29 1003 1015 10.1007/s10876-018-1411-5
El-Batal AI, Mosallam FM, El-Sayyad GS. Synthesis of metallic silver nanoparticles by fluconazole drug and gamma rays to inhibit the growth of multidrug-resistant microbes. J Cluster Sci. 2018;29:1003–15.10.1007/s10876-018-1411-5
56. Sharma R Dhillon A Kumar D Mentha-stabilized silver nanoparticles for highperformance colorimetric detection of Al (III) in aqueous systems Sci rep 2018 8 5189 5202 10.1038/s41598-018-23469-1 29581515
Sharma R, Dhillon A, Kumar D. Mentha-stabilized silver nanoparticles for highperformance colorimetric detection of Al (III) in aqueous systems. Sci rep. 2018;8:5189–202.29581515 10.1038/s41598-018-23469-1
57. Badi’Ah H Seedeh F Supriyanto G Zaidan A Synthesis of silver nanoparticles and the development in analysis method IOP Conf Ser Earth Enviro Sci 2019 217 012005 10.1088/1755-1315/217/1/012005
Badi’Ah H, Seedeh F, Supriyanto G, Zaidan A. Synthesis of silver nanoparticles and the development in analysis method. IOP Conf Ser Earth Enviro Sci. 2019;217:012005.10.1088/1755-1315/217/1/012005
58. Sanders ER Aseptic laboratory techniques: plating methods JoVE J Vis Exp 2012 10.3791/3064 22688118
Sanders ER. Aseptic laboratory techniques: plating methods. JoVE J Vis Exp. 2012. 10.3791/3064.22688118 10.3791/3064
59. Baraka A Dickson S Gobara M El-Sayyad GS Zorainy M Awaad MI Hatem H Kotb MM Tawfic A Synthesis of silver nanoparticles using natural pigments extracted from Alfalfa leaves and its use for antimicrobial activity Chem Pap 2017 71 2271 2281 10.1007/s11696-017-0221-9
Baraka A, Dickson S, Gobara M, El-Sayyad GS, Zorainy M, Awaad MI, Hatem H, Kotb MM, Tawfic A. Synthesis of silver nanoparticles using natural pigments extracted from Alfalfa leaves and its use for antimicrobial activity. Chem Pap. 2017;71:2271–81.10.1007/s11696-017-0221-9
60. Mosallam FM Helmy EA Bendary MM El-Batal AI Potency of a novel synthesized Ag-eugenol nanoemulsion for treating some bacterial and fungal pathogens J Mater Res 2021 36 1524 1537 10.1557/s43578-021-00226-1
Mosallam FM, Helmy EA, Bendary MM, El-Batal AI. Potency of a novel synthesized Ag-eugenol nanoemulsion for treating some bacterial and fungal pathogens. J Mater Res. 2021;36:1524–37.10.1557/s43578-021-00226-1
61. Abdel-Fatah SS El-Sherbiny GM Khalaf M Baz AFE El-Sayed AS El-Batal AI Boosting the anticancer activity of Aspergillus flavus “endophyte of Jojoba” Taxol via conjugation with gold nanoparticles mediated by γ-Irradiation Appl Biochem Biotechnol 2022 194 3558 3581 10.1007/s12010-022-03906-8 35438406
Abdel-Fatah SS, El-Sherbiny GM, Khalaf M, Baz AFE, El-Sayed AS, El-Batal AI. Boosting the anticancer activity of Aspergillus flavus “endophyte of Jojoba” Taxol via conjugation with gold nanoparticles mediated by γ-Irradiation. Appl Biochem Biotechnol. 2022;194:3558–81.35438406 10.1007/s12010-022-03906-8
62. El-Sherbiny GM Abou El-Nour SA Askar AA Mohammad NH Hammad AA Solar radiation-induced synthesis of bacterial cellulose/silver nanoparticles (BC/AgNPs) composite using BC as reducing and capping agent Bioprocess Biosyst Eng 2022 45 1 12 10.1007/s00449-021-02655-y 34373951
El-Sherbiny GM, Abou El-Nour SA, Askar AA, Mohammad NH, Hammad AA. Solar radiation-induced synthesis of bacterial cellulose/silver nanoparticles (BC/AgNPs) composite using BC as reducing and capping agent. Bioprocess Biosyst Eng. 2022;45:1–12.34373951 10.1007/s00449-021-02655-y
63. Charannya S Duraivel D Padminee K Poorni S Nishanthine C Srinivasan MR Comparative evaluation of antimicrobial efficacy of silver nanoparticles and 2% chlorhexidine gluconate when used alone and in combination assessed using agar diffusion method: an in vitro study Contemp Clin Dent 2018 9 S204 10.4103/ccd.ccd_869_17 30294145
Charannya S, Duraivel D, Padminee K, Poorni S, Nishanthine C, Srinivasan MR. Comparative evaluation of antimicrobial efficacy of silver nanoparticles and 2% chlorhexidine gluconate when used alone and in combination assessed using agar diffusion method: an in vitro study. Contemp Clin Dent. 2018;9:S204.30294145 10.4103/ccd.ccd_869_17
64. Bairagi B Khan F Nath D Identification of bacterial population from diabetic wound of mice to study the bactericidal efficacy of green synthesized silver nanoparticle by saraca asoca bark extract BioNanoSci 2023 13 436 449 10.1007/s12668-023-01086-1
Bairagi B, Khan F, Nath D. Identification of bacterial population from diabetic wound of mice to study the bactericidal efficacy of green synthesized silver nanoparticle by saraca asoca bark extract. BioNanoSci. 2023;13:436–49.10.1007/s12668-023-01086-1
65. Elbasuney S El-Sayyad GS Radwan SM Correa-Duarte MA Antimicrobial, and antibiofilm activities of silver doped hydroxyapatite: a novel bioceramic material for dental filling J Inorg Organomet Polym Mater 2022 32 4559 4575 10.1007/s10904-022-02459-x
Elbasuney S, El-Sayyad GS, Radwan SM, Correa-Duarte MA. Antimicrobial, and antibiofilm activities of silver doped hydroxyapatite: a novel bioceramic material for dental filling. J Inorg Organomet Polym Mater. 2022;32:4559–75.10.1007/s10904-022-02459-x
66. Kalishwaralal K BarathManiKanth S Pandian SRK Deepak V Gurunathan S Silver nanoparticles impede the biofilm formation by Pseudomonas aeruginosa and Staphylococcus epidermidis Colloids Surf, B 2010 79 340 344 10.1016/j.colsurfb.2010.04.014
Kalishwaralal K, BarathManiKanth S, Pandian SRK, Deepak V, Gurunathan S. Silver nanoparticles impede the biofilm formation by Pseudomonas aeruginosa and Staphylococcus epidermidis. Colloids Surf, B. 2010;79:340–4.10.1016/j.colsurfb.2010.04.014
67. Tabassum N Khan F Jeong G-J Oh D Kim Y-M Antibiofilm and antivirulence activities of laminarin-gold nanoparticles in standard and host-mimicking media Appl Microbiol Biotechnol 2024 108 1 15 10.1007/s00253-024-13050-4 38153551
Tabassum N, Khan F, Jeong G-J, Oh D, Kim Y-M. Antibiofilm and antivirulence activities of laminarin-gold nanoparticles in standard and host-mimicking media. Appl Microbiol Biotechnol. 2024;108:1–15.38153551 10.1007/s00253-024-13050-4
68. Ha D-G Kuchma SL O’Toole GA Plate-based assay for swarming motility in Pseudomonas aeruginosa Pseudomonas Methods Protoc 2014 1149 67 72 10.1007/978-1-4939-0473-0_8
Ha D-G, Kuchma SL, O’Toole GA. Plate-based assay for swarming motility in Pseudomonas aeruginosa. Pseudomonas Methods Protoc. 2014;1149:67–72.10.1007/978-1-4939-0473-0_8
69. Ha D-G Kuchma SL O’Toole GA Plate-based assay for swimming motility in Pseudomonas aeruginosa Pseudomonas Methods Protoc 2014 1149 59 65 10.1007/978-1-4939-0473-0_7
Ha D-G, Kuchma SL, O’Toole GA. Plate-based assay for swimming motility in Pseudomonas aeruginosa. Pseudomonas Methods Protoc. 2014;1149:59–65.10.1007/978-1-4939-0473-0_7
70. Wang S Feng Y Han X Cai X Yang L Liu C Shen L Inhibition of virulence factors and biofilm formation by wogonin attenuates pathogenicity of Pseudomonas aeruginosa PAO1 via targeting pqs quorum-sensing system Int J Mol Sci 2021 22 12699 10.3390/ijms222312699 34884499
Wang S, Feng Y, Han X, Cai X, Yang L, Liu C, Shen L. Inhibition of virulence factors and biofilm formation by wogonin attenuates pathogenicity of Pseudomonas aeruginosa PAO1 via targeting pqs quorum-sensing system. Int J Mol Sci. 2021;22:12699.34884499 10.3390/ijms222312699
71. Bogožalec Košir A Lužnik D Tomič V Milavec M Evaluation of DNA extraction methods for reliable quantification of Acinetobacter baumannii, Klebsiella pneumoniae, and Pseudomonas aeruginosa Biosensors 2023 13 463 10.3390/bios13040463 37185538
Bogožalec Košir A, Lužnik D, Tomič V, Milavec M. Evaluation of DNA extraction methods for reliable quantification of Acinetobacter baumannii, Klebsiella pneumoniae, and Pseudomonas aeruginosa. Biosensors. 2023;13:463.37185538 10.3390/bios13040463
72. Winstanley C Kaye SB Neal TJ Chilton HJ Miksch S Hart CA Group MO Genotypic and phenotypic characteristics of Pseudomonas aeruginosa isolates associated with ulcerative keratitis J Med Microbiol 2005 54 519 526 10.1099/jmm.0.46005-0 15888458
Winstanley C, Kaye SB, Neal TJ, Chilton HJ, Miksch S, Hart CA, Group MO. Genotypic and phenotypic characteristics of Pseudomonas aeruginosa isolates associated with ulcerative keratitis. J Med Microbiol. 2005;54:519–26.15888458 10.1099/jmm.0.46005-0
73. Finnan S Morrissey JP O’gara F Boyd EF Genome diversity of Pseudomonas aeruginosa isolates from cystic fibrosis patients and the hospital environment J Clin Microbiol 2004 42 5783 5792 10.1128/JCM.42.12.5783-5792.2004 15583313
Finnan S, Morrissey JP, O’gara F, Boyd EF. Genome diversity of Pseudomonas aeruginosa isolates from cystic fibrosis patients and the hospital environment. J Clin Microbiol. 2004;42:5783–92.15583313 10.1128/JCM.42.12.5783-5792.2004
74. Matar GM Ramlawi F Hijazi N Khneisser I Abdelnoor AM Transcription levels of Pseudomonas aeruginosa exotoxin A gene and severity of symptoms in patients with otitis externa Curr Microbiol 2002 45 350 354 10.1007/s00284-002-3703-z 12232666
Matar GM, Ramlawi F, Hijazi N, Khneisser I, Abdelnoor AM. Transcription levels of Pseudomonas aeruginosa exotoxin A gene and severity of symptoms in patients with otitis externa. Curr Microbiol. 2002;45:350–4.12232666 10.1007/s00284-002-3703-z
75. Mukherjee K Tribedi P Chowdhury A Ray T Joardar A Giri S Sil AK Isolation of a Pseudomonas aeruginosa strain from soil that can degrade polyurethane diol Biodegradation 2011 22 377 388 10.1007/s10532-010-9409-1 20803164
Mukherjee K, Tribedi P, Chowdhury A, Ray T, Joardar A, Giri S, Sil AK. Isolation of a Pseudomonas aeruginosa strain from soil that can degrade polyurethane diol. Biodegradation. 2011;22:377–88.20803164 10.1007/s10532-010-9409-1
76. El-Azzouny MM El-Demerdash AS Seadawy HG Abou-Khadra SH Antimicrobial effect of garlic (Allium sativum) and thyme (Zataria multiflora Boiss) extracts on some food borne pathogens and their effect on virulence gene expression Cell Mol Biol 2018 64 79 86 10.14715/cmb/2018.64.10.13 30084799
El-Azzouny MM, El-Demerdash AS, Seadawy HG, Abou-Khadra SH. Antimicrobial effect of garlic (Allium sativum) and thyme (Zataria multiflora Boiss) extracts on some food borne pathogens and their effect on virulence gene expression. Cell Mol Biol. 2018;64:79–86.30084799 10.14715/cmb/2018.64.10.13
77. Livak KJ Schmittgen TD Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method Methods 2001 25 402 408 10.1006/meth.2001.1262 11846609
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods. 2001;25:402–8.11846609 10.1006/meth.2001.1262
78. Mosmann T Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays J Immunol Methods 1983 65 55 63 10.1016/0022-1759(83)90303-4 6606682
Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 1983;65:55–63.6606682 10.1016/0022-1759(83)90303-4
79. Liu F-K Hsu Y-C Tsai M-H Chu T-C Using γ-irradiation to synthesize Ag nanoparticles Mater Lett 2007 61 2402 2405 10.1016/j.matlet.2006.07.193
Liu F-K, Hsu Y-C, Tsai M-H, Chu T-C. Using γ-irradiation to synthesize Ag nanoparticles. Mater Lett. 2007;61:2402–5.10.1016/j.matlet.2006.07.193
80. Bayik GD Baykal B Optimization of green synthesis parameters of silver nanoparticles with factorial design for dye removal Gazi Univ J Sci Part A: Eng Innov 2023 10 327 340 10.54287/gujsa.1294774
Bayik GD, Baykal B. Optimization of green synthesis parameters of silver nanoparticles with factorial design for dye removal. Gazi Univ J Sci Part A: Eng Innov. 2023;10:327–40.10.54287/gujsa.1294774
81. Hanora A Ghorab M El-Batal AI Mosalam FA Synthesis and characterization of gold nanoparticles and their anticancer activity using gamma radiation J Chem Pharm Res 2016 8 405 423
Hanora A, Ghorab M, El-Batal AI, Mosalam FA. Synthesis and characterization of gold nanoparticles and their anticancer activity using gamma radiation. J Chem Pharm Res. 2016;8:405–23.
82. Huang H Yang X Synthesis of polysaccharide-stabilized gold and silver nanoparticles: a green method Carbohyd Res 2004 339 2627 2631 10.1016/j.carres.2004.08.005
Huang H, Yang X. Synthesis of polysaccharide-stabilized gold and silver nanoparticles: a green method. Carbohyd Res. 2004;339:2627–31.10.1016/j.carres.2004.08.005
83. Bar H Bhui DK Sahoo GP Sarkar P De SP Misra A Green synthesis of silver nanoparticles using latex of Jatropha curcas Colloids Surf, A 2009 339 134 139 10.1016/j.colsurfa.2009.02.008
Bar H, Bhui DK, Sahoo GP, Sarkar P, De SP, Misra A. Green synthesis of silver nanoparticles using latex of Jatropha curcas. Colloids Surf, A. 2009;339:134–9.10.1016/j.colsurfa.2009.02.008
84. El-Batal AI Al-Hazmi NE Mosallam FM El-Sayyad GS Biogenic synthesis of copper nanoparticles by natural polysaccharides and Pleurotus ostreatus fermented fenugreek using gamma rays with antioxidant and antimicrobial potential towards some wound pathogens Microb Pathog 2018 118 159 169 10.1016/j.micpath.2018.03.013 29530808
El-Batal AI, Al-Hazmi NE, Mosallam FM, El-Sayyad GS. Biogenic synthesis of copper nanoparticles by natural polysaccharides and Pleurotus ostreatus fermented fenugreek using gamma rays with antioxidant and antimicrobial potential towards some wound pathogens. Microb Pathog. 2018;118:159–69.29530808 10.1016/j.micpath.2018.03.013
85. El-Batal AI Mosalam FM Ghorab M Hanora A Elbarbary AM Antimicrobial, antioxidant and anticancer activities of zinc nanoparticles prepared by natural polysaccharides and gamma radiation Int J Biol Macromol 2018 107 2298 2311 10.1016/j.ijbiomac.2017.10.121 29097216
El-Batal AI, Mosalam FM, Ghorab M, Hanora A, Elbarbary AM. Antimicrobial, antioxidant and anticancer activities of zinc nanoparticles prepared by natural polysaccharides and gamma radiation. Int J Biol Macromol. 2018;107:2298–311.29097216 10.1016/j.ijbiomac.2017.10.121
86. Mosalam M, Marzouk F. Effect of gamma radiation on the microbial synthesis of metal nanoparticles. 2013.
87. Campos EA Pinto DVBS Oliveira JISD Mattos EDC Dutra RDCL Synthesis, characterization and applications of iron oxide nanoparticles-a short review J Aerosp Technol Manag 2015 7 267 276 10.5028/jatm.v7i3.471
Campos EA, Pinto DVBS, Oliveira JISD, Mattos EDC, Dutra RDCL. Synthesis, characterization and applications of iron oxide nanoparticles-a short review. J Aerosp Technol Manag. 2015;7:267–76.10.5028/jatm.v7i3.471
88. Agustina TE, Handayani W, Imawan C: The UV-VIS spectrum analysis from silver nanoparticles synthesized using Diospyros maritima blume. Leaves extract. In: 3rd KOBI Congress, International and National Conferences (KOBICINC 2020). Atlantis Press; 2021: 411–419.
89. González A Noguez C Optical properties of silver nanoparticles Phys Stat Sol C 2007 4 4118 4126
González A, Noguez C. Optical properties of silver nanoparticles. Phys Stat Sol C. 2007;4:4118–26.
90. Varenne F Botton J Merlet C Vachon J-J Geiger S Infante IC Chehimi MM Vauthier C Standardization and validation of a protocol of zeta potential measurements by electrophoretic light scattering for nanomaterial characterization Colloids Surf, A 2015 486 218 231 10.1016/j.colsurfa.2015.08.044
Varenne F, Botton J, Merlet C, Vachon J-J, Geiger S, Infante IC, Chehimi MM, Vauthier C. Standardization and validation of a protocol of zeta potential measurements by electrophoretic light scattering for nanomaterial characterization. Colloids Surf, A. 2015;486:218–31.10.1016/j.colsurfa.2015.08.044
91. Brar SK Verma M Measurement of nanoparticles by light-scattering techniques TrAC, Trends Anal Chem 2011 30 4 17 10.1016/j.trac.2010.08.008
Brar SK, Verma M. Measurement of nanoparticles by light-scattering techniques. TrAC, Trends Anal Chem. 2011;30:4–17.10.1016/j.trac.2010.08.008
92. Maguire CM Rösslein M Wick P Prina-Mello A Characterisation of particles in solution–a perspective on light scattering and comparative technologies Sci Technol Adv Mater 2018 19 732 745 10.1080/14686996.2018.1517587 30369998
Maguire CM, Rösslein M, Wick P, Prina-Mello A. Characterisation of particles in solution–a perspective on light scattering and comparative technologies. Sci Technol Adv Mater. 2018;19:732–45.30369998 10.1080/14686996.2018.1517587
93. Bhattacharjee S DLS and zeta potential–what they are and what they are not? J Control Release 2016 235 337 351 10.1016/j.jconrel.2016.06.017 27297779
Bhattacharjee S. DLS and zeta potential–what they are and what they are not? J Control Release. 2016;235:337–51.27297779 10.1016/j.jconrel.2016.06.017
94. Raja S Ramesh V Thivaharan V Green biosynthesis of silver nanoparticles using Calliandra haematocephala leaf extract, their antibacterial activity and hydrogen peroxide sensing capability Arab J Chem 2017 10 253 261 10.1016/j.arabjc.2015.06.023
Raja S, Ramesh V, Thivaharan V. Green biosynthesis of silver nanoparticles using Calliandra haematocephala leaf extract, their antibacterial activity and hydrogen peroxide sensing capability. Arab J Chem. 2017;10:253–61.10.1016/j.arabjc.2015.06.023
95. Erdogan O Abbak M Demirbolat GM Birtekocak F Aksel M Pasa S Cevik O Green synthesis of silver nanoparticles via Cynara scolymus leaf extracts: the characterization, anticancer potential with photodynamic therapy in MCF7 cells PLoS ONE 2019 14 e0216496 10.1371/journal.pone.0216496 31220110
Erdogan O, Abbak M, Demirbolat GM, Birtekocak F, Aksel M, Pasa S, Cevik O. Green synthesis of silver nanoparticles via Cynara scolymus leaf extracts: the characterization, anticancer potential with photodynamic therapy in MCF7 cells. PLoS ONE. 2019;14: e0216496.31220110 10.1371/journal.pone.0216496
96. Padhi S Behera A Biosynthesis of silver nanoparticles: synthesis, mechanism, and characterization Agri-waste and microbes for production of sustainable nanomaterials 2022 Amsterdam Elsevier 397 440
Padhi S, Behera A. Biosynthesis of silver nanoparticles: synthesis, mechanism, and characterization. In: Agri-waste and microbes for production of sustainable nanomaterials. Amsterdam: Elsevier; 2022. p. 397–440.
97. Tuoriniemi J Johnsson ACJ Holmberg JP Gustafsson S Gallego-Urrea JA Olsson E Pettersson JB Hassellöv M Intermethod comparison of the particle size distributions of colloidal silica nanoparticles Sci Technol Adv Mater 2014 15 035009 10.1088/1468-6996/15/3/035009 27877685
Tuoriniemi J, Johnsson ACJ, Holmberg JP, Gustafsson S, Gallego-Urrea JA, Olsson E, Pettersson JB, Hassellöv M. Intermethod comparison of the particle size distributions of colloidal silica nanoparticles. Sci Technol Adv Mater. 2014;15:035009.27877685 10.1088/1468-6996/15/3/035009
98. Salvi VR Pawar P Nanostructured lipid carriers (NLC) system: a novel drug targeting carrier J Drug Deliv Sci Technol 2019 51 255 267 10.1016/j.jddst.2019.02.017
Salvi VR, Pawar P. Nanostructured lipid carriers (NLC) system: a novel drug targeting carrier. J Drug Deliv Sci Technol. 2019;51:255–67.10.1016/j.jddst.2019.02.017
99. Baran MF Green synthesis, characterization and antimicrobial activity of silver nanoparticles (AgNPs) from maize (Zea mays L.) Dergi 2019 6 165 173
Baran MF. Green synthesis, characterization and antimicrobial activity of silver nanoparticles (AgNPs) from maize (Zea mays L.). Dergi. 2019;6:165–73.
100. Shah S Shah SA Faisal S Khan A Ullah R Ali N Bilal M Engineering novel gold nanoparticles using Sageretia thea leaf extract and evaluation of their biological activities J Nanostructure Chem 2022 12 129 140 10.1007/s40097-021-00407-8
Shah S, Shah SA, Faisal S, Khan A, Ullah R, Ali N, Bilal M. Engineering novel gold nanoparticles using Sageretia thea leaf extract and evaluation of their biological activities. J Nanostructure Chem. 2022;12:129–40.10.1007/s40097-021-00407-8
101. Stan M Popa A Toloman D Silipas T-D Vodnar DC Antibacterial and antioxidant activities of ZnO nanoparticles synthesized using extracts of Allium sativum, Rosmarinus officinalis and Ocimum basilicum Acta Metallurgica Sinica (Engl Lett) 2016 29 228 236 10.1007/s40195-016-0380-7
Stan M, Popa A, Toloman D, Silipas T-D, Vodnar DC. Antibacterial and antioxidant activities of ZnO nanoparticles synthesized using extracts of Allium sativum, Rosmarinus officinalis and Ocimum basilicum. Acta Metallurgica Sinica (Engl Lett). 2016;29:228–36.10.1007/s40195-016-0380-7
102. Chen Y Cao J Wei H Wu Z Wang X Pei Y Synthesis of polyvinyl alcohol/Ag electrospun nanofibers as highly efficient flexible SERS substrates Vib Spectrosc 2021 114 103246 10.1016/j.vibspec.2021.103246
Chen Y, Cao J, Wei H, Wu Z, Wang X, Pei Y. Synthesis of polyvinyl alcohol/Ag electrospun nanofibers as highly efficient flexible SERS substrates. Vib Spectrosc. 2021;114:103246.10.1016/j.vibspec.2021.103246
103. Nyabola A Kareru P Madivoli E Wanakai S Maina EG Formation of silver nanoparticles via Aspilia pluriseta extracts their antimicrobial and catalytic activity J Inorg Organomet Polym Mater 2020 30 3493 3501 10.1007/s10904-020-01497-7
Nyabola A, Kareru P, Madivoli E, Wanakai S, Maina EG. Formation of silver nanoparticles via Aspilia pluriseta extracts their antimicrobial and catalytic activity. J Inorg Organomet Polym Mater. 2020;30:3493–501.10.1007/s10904-020-01497-7
104. Mosallam FM Helmy EA Nasser HA El-Batal AI Novel griseofulvin zinc nanohybrid emulsion for intensifying the antimicrobial control of dermatophytes and some opportunistic pathogens J Med Mycol 2024 34 101489 10.1016/j.mycmed.2024.101489
Mosallam FM, Helmy EA, Nasser HA, El-Batal AI. Novel griseofulvin zinc nanohybrid emulsion for intensifying the antimicrobial control of dermatophytes and some opportunistic pathogens. J Med Mycol. 2024;34:101489.10.1016/j.mycmed.2024.101489
105. Unterweger H Dézsi L Matuszak J Janko C Poettler M Jordan J Bäuerle T Szebeni J Fey T Boccaccini AR Dextran-coated superparamagnetic iron oxide nanoparticles for magnetic resonance imaging: evaluation of size-dependent imaging properties, storage stability and safety Int J Nanomed 2018 13 1899 1915 10.2147/IJN.S156528
Unterweger H, Dézsi L, Matuszak J, Janko C, Poettler M, Jordan J, Bäuerle T, Szebeni J, Fey T, Boccaccini AR. Dextran-coated superparamagnetic iron oxide nanoparticles for magnetic resonance imaging: evaluation of size-dependent imaging properties, storage stability and safety. Int J Nanomed. 2018;13:1899–915.10.2147/IJN.S156528
106. Hoang V-T Mai M Thi Tam L Vu NP Tien Khi N Dinh Tam P Quang Huy T Le A-T Xuan Dinh N Tran V-H Functionalized-AgNPs for long-term stability and its applicability in the detection of manganese Ions Adv Polym Technol 2020 2020 9437108 10.1155/2020/9437108
Hoang V-T, Mai M, Thi Tam L, Vu NP, Tien Khi N, Dinh Tam P, Quang Huy T, Le A-T, Xuan Dinh N, Tran V-H. Functionalized-AgNPs for long-term stability and its applicability in the detection of manganese Ions. Adv Polym Technol. 2020;2020:9437108.10.1155/2020/9437108
107. Semeniuc CA Pop CR Rotar AM Antibacterial activity and interactions of plant essential oil combinations against gram-positive and gram-negative bacteria J Food Drug Anal 2017 25 403 408 10.1016/j.jfda.2016.06.002 28911683
Semeniuc CA, Pop CR, Rotar AM. Antibacterial activity and interactions of plant essential oil combinations against gram-positive and gram-negative bacteria. J Food Drug Anal. 2017;25:403–8.28911683 10.1016/j.jfda.2016.06.002
108. Susanti D Haris MS Taher M Khotib J Natural products-based metallic nanoparticles as antimicrobial agents Front Pharmacol 2022 13 895616 10.3389/fphar.2022.895616 35721199
Susanti D, Haris MS, Taher M, Khotib J. Natural products-based metallic nanoparticles as antimicrobial agents. Front Pharmacol. 2022;13:895616.35721199 10.3389/fphar.2022.895616
109. Sung K Chon J Kweon O Nho S Kim S Park M Paredes A Lim J-H Khan SA Phillips KS Dynamic adaptive response of Pseudomonas aeruginosa to clindamycin/rifampicin-impregnated catheters Antibiotics 2021 10 752 10.3390/antibiotics10070752 34206280
Sung K, Chon J, Kweon O, Nho S, Kim S, Park M, Paredes A, Lim J-H, Khan SA, Phillips KS. Dynamic adaptive response of Pseudomonas aeruginosa to clindamycin/rifampicin-impregnated catheters. Antibiotics. 2021;10:752.34206280 10.3390/antibiotics10070752
110. Sharma A Sagar A Rana J Rani R Green synthesis of silver nanoparticles and its antibacterial activity using fungus Talaromyces purpureogenus isolated from Taxus baccata Linn Micro and Nano Systems Letters 2022 10 2 10.1186/s40486-022-00144-9
Sharma A, Sagar A, Rana J, Rani R. Green synthesis of silver nanoparticles and its antibacterial activity using fungus Talaromyces purpureogenus isolated from Taxus baccata Linn. Micro and Nano Systems Letters. 2022;10:2.10.1186/s40486-022-00144-9
111. Mostafa AA Sayed SR Solkamy EN Khan M Shaik MR Al-Warthan A Adil SF Evaluation of biological activities of chemically synthesized silver nanoparticles J Nanomater 2015 2015 789178 10.1155/2015/789178
Mostafa AA, Sayed SR, Solkamy EN, Khan M, Shaik MR, Al-Warthan A, Adil SF. Evaluation of biological activities of chemically synthesized silver nanoparticles. J Nanomater. 2015;2015:789178.10.1155/2015/789178
112. Trzcińska-Wencel J Wypij M Rai M Golińska P Biogenic nanosilver bearing antimicrobial and antibiofilm activities and its potential for application in agriculture and industry Front Microbiol 2023 14 1125685 10.3389/fmicb.2023.1125685 36891391
Trzcińska-Wencel J, Wypij M, Rai M, Golińska P. Biogenic nanosilver bearing antimicrobial and antibiofilm activities and its potential for application in agriculture and industry. Front Microbiol. 2023;14:1125685.36891391 10.3389/fmicb.2023.1125685
113. Kora AJ Sashidhar RB Antibacterial activity of biogenic silver nanoparticles synthesized with gum ghatti and gum olibanum: a comparative study J Antibiot 2015 68 88 97 10.1038/ja.2014.114
Kora AJ, Sashidhar RB. Antibacterial activity of biogenic silver nanoparticles synthesized with gum ghatti and gum olibanum: a comparative study. J Antibiot. 2015;68:88–97.10.1038/ja.2014.114
114. Kora AJ Sashidhar R Biogenic silver nanoparticles synthesized with rhamnogalacturonan gum: Antibacterial activity, cytotoxicity and its mode of action Arab J Chem 2018 11 313 323 10.1016/j.arabjc.2014.10.036
Kora AJ, Sashidhar R. Biogenic silver nanoparticles synthesized with rhamnogalacturonan gum: Antibacterial activity, cytotoxicity and its mode of action. Arab J Chem. 2018;11:313–23.10.1016/j.arabjc.2014.10.036
115. Abdel Moneim E Sherif M Ahmed A Mohanad A Vajid N Evaluation of antimicrobial activity of safflower (Carthamus tinctorius) and its synergistic effect with antibiotic EC Microbiol 2018 14 160 166
Abdel Moneim E, Sherif M, Ahmed A, Mohanad A, Vajid N. Evaluation of antimicrobial activity of safflower (Carthamus tinctorius) and its synergistic effect with antibiotic. EC Microbiol. 2018;14:160–6.
116. Le Ouay B Stellacci F Antibacterial activity of silver nanoparticles: a surface science insight Nano Today 2015 10 339 354 10.1016/j.nantod.2015.04.002
Le Ouay B, Stellacci F. Antibacterial activity of silver nanoparticles: a surface science insight. Nano Today. 2015;10:339–54.10.1016/j.nantod.2015.04.002
117. Chen S Guo Y Zhong H Chen S Li J Ge Z Tang J Synergistic antibacterial mechanism and coating application of copper/titanium dioxide nanoparticles Chem Eng J 2014 256 238 246 10.1016/j.cej.2014.07.006
Chen S, Guo Y, Zhong H, Chen S, Li J, Ge Z, Tang J. Synergistic antibacterial mechanism and coating application of copper/titanium dioxide nanoparticles. Chem Eng J. 2014;256:238–46.10.1016/j.cej.2014.07.006
118. Hu B Das P Lv X Shi M Aa J Wang K Duan L Gilbert JA Nie Y Wu X-L Effects of ‘healthy’fecal microbiota transplantation against the deterioration of depression in fawn-hooded rats Msystems 2022 7 e00218 00222 35481347
Hu B, Das P, Lv X, Shi M, Aa J, Wang K, Duan L, Gilbert JA, Nie Y, Wu X-L. Effects of ‘healthy’fecal microbiota transplantation against the deterioration of depression in fawn-hooded rats. Msystems. 2022;7:e00218-00222.35481347
119. Salomoni R Léo P Montemor A Rinaldi B Rodrigues M Antibacterial effect of silver nanoparticles in Pseudomonas aeruginosa Nanotechnol Sci Appl 2017 10 115 121 10.2147/NSA.S133415 28721025
Salomoni R, Léo P, Montemor A, Rinaldi B, Rodrigues M. Antibacterial effect of silver nanoparticles in Pseudomonas aeruginosa. Nanotechnol Sci Appl. 2017;10:115–21.28721025 10.2147/NSA.S133415
120. Bruna T Maldonado-Bravo F Jara P Caro N Silver nanoparticles and their antibacterial applications Int J Mol Sci 2021 22 7202 10.3390/ijms22137202 34281254
Bruna T, Maldonado-Bravo F, Jara P, Caro N. Silver nanoparticles and their antibacterial applications. Int J Mol Sci. 2021;22:7202.34281254 10.3390/ijms22137202
121. Sheng Y Narayanan M Basha S Elfasakhany A Brindhadevi K Xia C Pugazhendhi A In vitro and in vivo efficacy of green synthesized AgNPs against gram negative and gram positive bacterial pathogens Process Biochem 2022 112 241 247 10.1016/j.procbio.2021.12.012
Sheng Y, Narayanan M, Basha S, Elfasakhany A, Brindhadevi K, Xia C, Pugazhendhi A. In vitro and in vivo efficacy of green synthesized AgNPs against gram negative and gram positive bacterial pathogens. Process Biochem. 2022;112:241–7.10.1016/j.procbio.2021.12.012
122. Ayaz M Ullah F Sadiq A Ullah F Ovais M Ahmed J Devkota HP Synergistic interactions of phytochemicals with antimicrobial agents: potential strategy to counteract drug resistance Chem Biol Interact 2019 308 294 303 10.1016/j.cbi.2019.05.050 31158333
Ayaz M, Ullah F, Sadiq A, Ullah F, Ovais M, Ahmed J, Devkota HP. Synergistic interactions of phytochemicals with antimicrobial agents: potential strategy to counteract drug resistance. Chem Biol Interact. 2019;308:294–303.31158333 10.1016/j.cbi.2019.05.050
123. Almatroudi A Silver nanoparticles: synthesis, characterisation and biomedical applications Open life sciences 2020 15 819 839 10.1515/biol-2020-0094 33817269
Almatroudi A. Silver nanoparticles: synthesis, characterisation and biomedical applications. Open life sciences. 2020;15:819–39.33817269 10.1515/biol-2020-0094
124. Franci G Falanga A Galdiero S Palomba L Rai M Morelli G Galdiero M Silver nanoparticles as potential antibacterial agents Molecules 2015 20 8856 8874 10.3390/molecules20058856 25993417
Franci G, Falanga A, Galdiero S, Palomba L, Rai M, Morelli G, Galdiero M. Silver nanoparticles as potential antibacterial agents. Molecules. 2015;20:8856–74.25993417 10.3390/molecules20058856
125. Qing Y Cheng L Li R Liu G Zhang Y Tang X Wang J Liu H Qin Y Potential antibacterial mechanism of silver nanoparticles and the optimization of orthopedic implants by advanced modification technologies Int J Nanomed 2018 13 3311 3327 10.2147/IJN.S165125
Qing Y, Cheng L, Li R, Liu G, Zhang Y, Tang X, Wang J, Liu H, Qin Y. Potential antibacterial mechanism of silver nanoparticles and the optimization of orthopedic implants by advanced modification technologies. Int J Nanomed. 2018;13:3311–27.10.2147/IJN.S165125
126. Gurunathan S Qasim M Park C Yoo H Kim J-H Hong K Cytotoxic potential and molecular pathway analysis of silver nanoparticles in human colon cancer cells HCT116 Int J Mol Sci 2018 19 2269 10.3390/ijms19082269 30072642
Gurunathan S, Qasim M, Park C, Yoo H, Kim J-H, Hong K. Cytotoxic potential and molecular pathway analysis of silver nanoparticles in human colon cancer cells HCT116. Int J Mol Sci. 2018;19:2269.30072642 10.3390/ijms19082269
127. Wang L Xu H Gu L Han T Wang S Meng F Bioinspired synthesis, characterization and antibacterial activity of plant-mediated silver nanoparticles using purple sweet potato root extract Mater Technol 2016 31 437 442 10.1080/10667857.2015.1105575
Wang L, Xu H, Gu L, Han T, Wang S, Meng F. Bioinspired synthesis, characterization and antibacterial activity of plant-mediated silver nanoparticles using purple sweet potato root extract. Mater Technol. 2016;31:437–42.10.1080/10667857.2015.1105575
128. Jangjou A Zareshahrabadi Z Abbasi M Talaiekhozani A Kamyab H Chelliapan S Vaez A Golchin A Tayebi L Vafa E Time to conquer fungal infectious diseases: employing nanoparticles as powerful and versatile antifungal nanosystems against a wide variety of fungal species Sustainability 2022 14 12942 10.3390/su141912942
Jangjou A, Zareshahrabadi Z, Abbasi M, Talaiekhozani A, Kamyab H, Chelliapan S, Vaez A, Golchin A, Tayebi L, Vafa E. Time to conquer fungal infectious diseases: employing nanoparticles as powerful and versatile antifungal nanosystems against a wide variety of fungal species. Sustainability. 2022;14:12942.10.3390/su141912942
129. Radhakrishnan VS Reddy Mudiam MK Kumar M Dwivedi SP Singh SP Prasad T Silver nanoparticles induced alterations in multiple cellular targets, which are critical for drug susceptibilities and pathogenicity in fungal pathogen (Candida albicans) Int J Nanomed 2018 13 2647 2663 10.2147/IJN.S150648
Radhakrishnan VS, Reddy Mudiam MK, Kumar M, Dwivedi SP, Singh SP, Prasad T. Silver nanoparticles induced alterations in multiple cellular targets, which are critical for drug susceptibilities and pathogenicity in fungal pathogen (Candida albicans). Int J Nanomed. 2018;13:2647–63.10.2147/IJN.S150648
130. Xu L Wang Y-Y Huang J Chen C-Y Wang Z-X Xie H Silver nanoparticles: synthesis, medical applications and biosafety Theranostics 2020 10 8996 10.7150/thno.45413 32802176
Xu L, Wang Y-Y, Huang J, Chen C-Y, Wang Z-X, Xie H. Silver nanoparticles: synthesis, medical applications and biosafety. Theranostics. 2020;10:8996.32802176 10.7150/thno.45413
131. Kumari M Pandey S Giri VP Bhattacharya A Shukla R Mishra A Nautiyal C Tailoring shape and size of biogenic silver nanoparticles to enhance antimicrobial efficacy against MDR bacteria Microb Pathog 2017 105 346 355 10.1016/j.micpath.2016.11.012 27889528
Kumari M, Pandey S, Giri VP, Bhattacharya A, Shukla R, Mishra A, Nautiyal C. Tailoring shape and size of biogenic silver nanoparticles to enhance antimicrobial efficacy against MDR bacteria. Microb Pathog. 2017;105:346–55.27889528 10.1016/j.micpath.2016.11.012
132. Hong X Wen J Xiong X Hu Y Shape effect on the antibacterial activity of silver nanoparticles synthesized via a microwave-assisted method Environ Sci Pollut Res 2016 23 4489 4497 10.1007/s11356-015-5668-z
Hong X, Wen J, Xiong X, Hu Y. Shape effect on the antibacterial activity of silver nanoparticles synthesized via a microwave-assisted method. Environ Sci Pollut Res. 2016;23:4489–97.10.1007/s11356-015-5668-z
133. Jiang M Chen S Lu X Guo H Chen S Yin X Li H Dai G Liu L Integrating genomics and metabolomics for the targeted discovery of new cyclopeptides with antifungal activity from a marine-derived fungus Beauveria felina J Agric Food Chem 2023 71 9782 9795 10.1021/acs.jafc.3c02415 37310400
Jiang M, Chen S, Lu X, Guo H, Chen S, Yin X, Li H, Dai G, Liu L. Integrating genomics and metabolomics for the targeted discovery of new cyclopeptides with antifungal activity from a marine-derived fungus Beauveria felina. J Agric Food Chem. 2023;71:9782–95.37310400 10.1021/acs.jafc.3c02415
134. Abbaszadegan A Ghahramani Y Gholami A Hemmateenejad B Dorostkar S Nabavizadeh M Sharghi H The effect of charge at the surface of silver nanoparticles on antimicrobial activity against gram-positive and gram-negative bacteria: a preliminary study J Nanomater 2015 2015 720654 10.1155/2015/720654
Abbaszadegan A, Ghahramani Y, Gholami A, Hemmateenejad B, Dorostkar S, Nabavizadeh M, Sharghi H. The effect of charge at the surface of silver nanoparticles on antimicrobial activity against gram-positive and gram-negative bacteria: a preliminary study. J Nanomater. 2015;2015:720654.10.1155/2015/720654
135. Mandal D Dash SK Das B Chattopadhyay S Ghosh T Das D Roy S Bio-fabricated silver nanoparticles preferentially targets gram positive depending on cell surface charge Biomed Pharmacother 2016 83 548 558 10.1016/j.biopha.2016.07.011 27449536
Mandal D, Dash SK, Das B, Chattopadhyay S, Ghosh T, Das D, Roy S. Bio-fabricated silver nanoparticles preferentially targets gram positive depending on cell surface charge. Biomed Pharmacother. 2016;83:548–58.27449536 10.1016/j.biopha.2016.07.011
136. Rolim WR Pelegrino MT de Araújo LB Ferraz LS Costa FN Bernardes JS Rodigues T Brocchi M Seabra AB Green tea extract mediated biogenic synthesis of silver nanoparticles: characterization, cytotoxicity evaluation and antibacterial activity Appl Surf Sci 2019 463 66 74 10.1016/j.apsusc.2018.08.203
Rolim WR, Pelegrino MT, de Araújo LB, Ferraz LS, Costa FN, Bernardes JS, Rodigues T, Brocchi M, Seabra AB. Green tea extract mediated biogenic synthesis of silver nanoparticles: characterization, cytotoxicity evaluation and antibacterial activity. Appl Surf Sci. 2019;463:66–74.10.1016/j.apsusc.2018.08.203
137. Bémer P Plouzeau C Tande D Léger J Giraudeau B Valentin AS Jolivet-Gougeon A Vincent P Corvec S Gibaud S Evaluation of 16S rRNA gene PCR sensitivity and specificity for diagnosis of prosthetic joint infection: a prospective multicenter cross-sectional study J Clin Microbiol 2014 52 3583 3589 10.1128/JCM.01459-14 25056331
Bémer P, Plouzeau C, Tande D, Léger J, Giraudeau B, Valentin AS, Jolivet-Gougeon A, Vincent P, Corvec S, Gibaud S. Evaluation of 16S rRNA gene PCR sensitivity and specificity for diagnosis of prosthetic joint infection: a prospective multicenter cross-sectional study. J Clin Microbiol. 2014;52:3583–9.25056331 10.1128/JCM.01459-14
138. Raza S Wdowiak M Grotek M Adamkiewicz W Nikiforow K Mente P Paczesny J Enhancing the antimicrobial activity of silver nanoparticles against ESKAPE bacteria and emerging fungal pathogens by using tea extracts Nanos Adv 2023 5 5786 5798 10.1039/D3NA00220A
Raza S, Wdowiak M, Grotek M, Adamkiewicz W, Nikiforow K, Mente P, Paczesny J. Enhancing the antimicrobial activity of silver nanoparticles against ESKAPE bacteria and emerging fungal pathogens by using tea extracts. Nanos Adv. 2023;5:5786–98.10.1039/D3NA00220A
139. Naganthran A Verasoundarapandian G Khalid FE Masarudin MJ Zulkharnain A Nawawi NM Karim M Che Abdullah CA Ahmad SA Synthesis, characterization and biomedical application of silver nanoparticles Materials 2022 15 427 10.3390/ma15020427 35057145
Naganthran A, Verasoundarapandian G, Khalid FE, Masarudin MJ, Zulkharnain A, Nawawi NM, Karim M, Che Abdullah CA, Ahmad SA. Synthesis, characterization and biomedical application of silver nanoparticles. Materials. 2022;15:427.35057145 10.3390/ma15020427
140. Khan MA Ali F Faisal S Rizwan M Hussain Z Zaman N Afsheen Z Uddin MN Bibi N Exploring the therapeutic potential of Hibiscus rosa sinensis synthesized cobalt oxide (Co3O4-NPs) and magnesium oxide nanoparticles (MgO-NPs) Saudi J Biol Sci 2021 28 5157 5167 10.1016/j.sjbs.2021.05.035 34466093
Khan MA, Ali F, Faisal S, Rizwan M, Hussain Z, Zaman N, Afsheen Z, Uddin MN, Bibi N. Exploring the therapeutic potential of Hibiscus rosa sinensis synthesized cobalt oxide (Co3O4-NPs) and magnesium oxide nanoparticles (MgO-NPs). Saudi J Biol Sci. 2021;28:5157–67.34466093 10.1016/j.sjbs.2021.05.035
141. Meher A Tandi A Moharana S Chakroborty S Mohapatra SS Mondal A Dey S Chandra P Silver nanoparticle for biomedical applications: a review Hybrid Adv 2024 6 100184 10.1016/j.hybadv.2024.100184
Meher A, Tandi A, Moharana S, Chakroborty S, Mohapatra SS, Mondal A, Dey S, Chandra P. Silver nanoparticle for biomedical applications: a review. Hybrid Adv. 2024;6:100184.10.1016/j.hybadv.2024.100184
142. Faisal S Jan H Shah SA Shah S Khan A Akbar MT Rizwan M Jan F Wajidullah Akhtar N Green synthesis of zinc oxide (ZnO) nanoparticles using aqueous fruit extracts of Myristica fragrans: their characterizations and biological and environmental applications ACS Omega 2021 6 9709 9722 10.1021/acsomega.1c00310 33869951
Faisal S, Jan H, Shah SA, Shah S, Khan A, Akbar MT, Rizwan M, Jan F, Wajidullah, Akhtar N. Green synthesis of zinc oxide (ZnO) nanoparticles using aqueous fruit extracts of Myristica fragrans: their characterizations and biological and environmental applications. ACS Omega. 2021;6:9709–22.33869951 10.1021/acsomega.1c00310
143. Pasparakis G Recent developments in the use of gold and silver nanoparticles in biomedicine Wiley interdiscip Rev Nanomed Nanobiotechnol 2022 14 e1817 10.1002/wnan.1817 35775611
Pasparakis G. Recent developments in the use of gold and silver nanoparticles in biomedicine. Wiley interdiscip Rev Nanomed Nanobiotechnol. 2022;14: e1817.35775611 10.1002/wnan.1817
144. Jamal M Ahmad W Andleeb S Jalil F Imran M Nawaz MA Hussain T Ali M Rafiq M Kamil MA Bacterial biofilm and associated infections J Chin Med Assoc 2018 81 7 11 10.1016/j.jcma.2017.07.012 29042186
Jamal M, Ahmad W, Andleeb S, Jalil F, Imran M, Nawaz MA, Hussain T, Ali M, Rafiq M, Kamil MA. Bacterial biofilm and associated infections. J Chin Med Assoc. 2018;81:7–11.29042186 10.1016/j.jcma.2017.07.012
145. Mohanta YK Biswas K Jena SK Hashem A Abd-Allah EF Mohanta TK Anti-biofilm and antibacterial activities of silver nanoparticles synthesized by the reducing activity of phytoconstituents present in the Indian medicinal plants Front Microbiol 2020 11 1143 10.3389/fmicb.2020.01143 32655511
Mohanta YK, Biswas K, Jena SK, Hashem A, Abd_Allah EF, Mohanta TK. Anti-biofilm and antibacterial activities of silver nanoparticles synthesized by the reducing activity of phytoconstituents present in the Indian medicinal plants. Front Microbiol. 2020;11:1143.32655511 10.3389/fmicb.2020.01143
146. Elshaer S Shaaban MI Antibiofilm activity of biosynthesized silver and copper nanoparticles using Streptomyces S29 AMB Express 2023 13 139 10.1186/s13568-023-01647-3 38055099
Elshaer S, Shaaban MI. Antibiofilm activity of biosynthesized silver and copper nanoparticles using Streptomyces S29. AMB Express. 2023;13:139.38055099 10.1186/s13568-023-01647-3
147. Hussain A Alajmi MF Khan MA Pervez SA Ahmed F Amir S Husain FM Khan MS Shaik GM Hassan I Biosynthesized silver nanoparticle (AgNP) from Pandanus odorifer leaf extract exhibits anti-metastasis and anti-biofilm potentials Front Microbiol 2019 10 8 10.3389/fmicb.2019.00008 30853939
Hussain A, Alajmi MF, Khan MA, Pervez SA, Ahmed F, Amir S, Husain FM, Khan MS, Shaik GM, Hassan I. Biosynthesized silver nanoparticle (AgNP) from Pandanus odorifer leaf extract exhibits anti-metastasis and anti-biofilm potentials. Front Microbiol. 2019;10:8.30853939 10.3389/fmicb.2019.00008
148. Martinez-Gutierrez F Boegli L Agostinho A Sánchez EM Bach H Ruiz F James G Anti-biofilm activity of silver nanoparticles against different microorganisms Biofouling 2013 29 651 660 10.1080/08927014.2013.794225 23731460
Martinez-Gutierrez F, Boegli L, Agostinho A, Sánchez EM, Bach H, Ruiz F, James G. Anti-biofilm activity of silver nanoparticles against different microorganisms. Biofouling. 2013;29:651–60.23731460 10.1080/08927014.2013.794225
149. Rolim WR Lamilla C Pieretti JC Díaz M Tortella GR Cristina Diez M Barrientos L Seabra AB Rubilar O Comparison of antibacterial and antibiofilm activities of biologically synthesized silver nanoparticles against several bacterial strains of medical interest Energy, Ecol Environ 2019 4 143 159 10.1007/s40974-019-00123-8
Rolim WR, Lamilla C, Pieretti JC, Díaz M, Tortella GR, Cristina Diez M, Barrientos L, Seabra AB, Rubilar O. Comparison of antibacterial and antibiofilm activities of biologically synthesized silver nanoparticles against several bacterial strains of medical interest. Energy, Ecol Environ. 2019;4:143–59.10.1007/s40974-019-00123-8
150. Weber DJ Rutala WA Anderson DJ Sickbert-Bennett EE Biofilms on medical instruments and surfaces: do they interfere with instrument reprocessing and surface disinfection Am J Infect Control 2023 51 A114 A119 10.1016/j.ajic.2023.04.158 37890940
Weber DJ, Rutala WA, Anderson DJ, Sickbert-Bennett EE. Biofilms on medical instruments and surfaces: do they interfere with instrument reprocessing and surface disinfection. Am J Infect Control. 2023;51:A114–9.37890940 10.1016/j.ajic.2023.04.158
151. Mikhailova EO Silver nanoparticles: mechanism of action and probable bio-application J Funct Biomater 2020 11 84 10.3390/jfb11040084 33255874
Mikhailova EO. Silver nanoparticles: mechanism of action and probable bio-application. J Funct Biomater. 2020;11:84.33255874 10.3390/jfb11040084
152. Joshi AS Singh P Mijakovic I Interactions of gold and silver nanoparticles with bacterial biofilms: molecular interactions behind inhibition and resistance Int J Mol Sci 2020 21 7658 10.3390/ijms21207658 33081366
Joshi AS, Singh P, Mijakovic I. Interactions of gold and silver nanoparticles with bacterial biofilms: molecular interactions behind inhibition and resistance. Int J Mol Sci. 2020;21:7658.33081366 10.3390/ijms21207658
153. Sondi I Salopek-Sondi B Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for Gram-negative bacteria J Colloid Interface Sci 2004 275 177 182 10.1016/j.jcis.2004.02.012 15158396
Sondi I, Salopek-Sondi B. Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for Gram-negative bacteria. J Colloid Interface Sci. 2004;275:177–82.15158396 10.1016/j.jcis.2004.02.012
154. Bagur H Poojari CC Melappa G Rangappa R Chandrasekhar N Somu P Biogenically synthesized silver nanoparticles using endophyte fungal extract of Ocimum tenuiflorum and evaluation of biomedical properties J Cluster Sci 2020 31 1241 1255 10.1007/s10876-019-01731-4
Bagur H, Poojari CC, Melappa G, Rangappa R, Chandrasekhar N, Somu P. Biogenically synthesized silver nanoparticles using endophyte fungal extract of Ocimum tenuiflorum and evaluation of biomedical properties. J Cluster Sci. 2020;31:1241–55.10.1007/s10876-019-01731-4
155. Verma VC Kharwar RN Gange AC Biosynthesis of antimicrobial silver nanoparticles by the endophytic fungus Aspergillus clavatus Nanomedicine 2010 5 33 40 10.2217/nnm.09.77 20025462
Verma VC, Kharwar RN, Gange AC. Biosynthesis of antimicrobial silver nanoparticles by the endophytic fungus Aspergillus clavatus. Nanomedicine. 2010;5:33–40.20025462 10.2217/nnm.09.77
156. Khan S Rukayadi Y Jaafar AH Ahmad NH Antibacterial potential of silver nanoparticles (SP-AgNPs) synthesized from Syzygium polyanthum (Wight) Walp. against selected foodborne pathogens Heliyon 2023 9 e22771 10.1016/j.heliyon.2023.e22771 38125456
Khan S, Rukayadi Y, Jaafar AH, Ahmad NH. Antibacterial potential of silver nanoparticles (SP-AgNPs) synthesized from Syzygium polyanthum (Wight) Walp. against selected foodborne pathogens. Heliyon. 2023;9: e22771.38125456 10.1016/j.heliyon.2023.e22771
157. Malawong S Thammawithan S Sirithongsuk P Daduang S Klaynongsruang S Wong PT Patramanon R Silver nanoparticles enhance antimicrobial efficacy of antibiotics and restore that efficacy against the melioidosis pathogen Antibiotics 2021 10 839 10.3390/antibiotics10070839 34356761
Malawong S, Thammawithan S, Sirithongsuk P, Daduang S, Klaynongsruang S, Wong PT, Patramanon R. Silver nanoparticles enhance antimicrobial efficacy of antibiotics and restore that efficacy against the melioidosis pathogen. Antibiotics. 2021;10:839.34356761 10.3390/antibiotics10070839
158. Thombre R Jangid K Shukla R Dutta NK Alternative therapeutics against antimicrobial-resistant pathogens Front Media SA 2019 10 2173
Thombre R, Jangid K, Shukla R, Dutta NK. Alternative therapeutics against antimicrobial-resistant pathogens. Front Media SA. 2019;10:2173.
159. Oei JD Zhao WW Chu L DeSilva MN Ghimire A Rawls HR Whang K Antimicrobial acrylic materials with in situ generated silver nanoparticles J Biomed Mater Res B Appl Biomater 2012 100 409 415 10.1002/jbm.b.31963 22102276
Oei JD, Zhao WW, Chu L, DeSilva MN, Ghimire A, Rawls HR, Whang K. Antimicrobial acrylic materials with in situ generated silver nanoparticles. J Biomed Mater Res B Appl Biomater. 2012;100:409–15.22102276 10.1002/jbm.b.31963
160. Kim K-J Sung WS Suh BK Moon S-K Choi J-S Kim JG Lee DG Antifungal activity and mode of action of silver nano-particles on Candida albicans Biometals 2009 22 235 242 10.1007/s10534-008-9159-2 18769871
Kim K-J, Sung WS, Suh BK, Moon S-K, Choi J-S, Kim JG, Lee DG. Antifungal activity and mode of action of silver nano-particles on Candida albicans. Biometals. 2009;22:235–42.18769871 10.1007/s10534-008-9159-2
161. Zhang X-F Liu Z-G Shen W Gurunathan S Silver nanoparticles: synthesis, characterization, properties, applications, and therapeutic approaches Int J Mol Sci 2016 17 1534 10.3390/ijms17091534 27649147
Zhang X-F, Liu Z-G, Shen W, Gurunathan S. Silver nanoparticles: synthesis, characterization, properties, applications, and therapeutic approaches. Int J Mol Sci. 2016;17:1534.27649147 10.3390/ijms17091534
162. O'Toole GA Kolter R Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development Mol Microbiol 1998 30 295 304 10.1046/j.1365-2958.1998.01062.x 9791175
O’Toole GA, Kolter R. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol. 1998;30:295–304.9791175 10.1046/j.1365-2958.1998.01062.x
163. Kang M-G Khan F Jo D-M Oh D Tabassum N Kim Y-M Antibiofilm and antivirulence activities of gold and zinc oxide nanoparticles synthesized from kimchi-isolated Leuconostoc sp. Strain C2 Antibiotics 2022 11 1524 10.3390/antibiotics11111524 36358180
Kang M-G, Khan F, Jo D-M, Oh D, Tabassum N, Kim Y-M. Antibiofilm and antivirulence activities of gold and zinc oxide nanoparticles synthesized from kimchi-isolated Leuconostoc sp. Strain C2. Antibiotics. 2022;11:1524.36358180 10.3390/antibiotics11111524
164. Khan F Manivasagan P Lee J-W Pham DTN Oh J Kim Y-M Fucoidan-stabilized gold nanoparticle-mediated biofilm inhibition, attenuation of virulence and motility properties in Pseudomonas aeruginosa PAO1 Mar Drugs 2019 17 208 10.3390/md17040208 30987163
Khan F, Manivasagan P, Lee J-W, Pham DTN, Oh J, Kim Y-M. Fucoidan-stabilized gold nanoparticle-mediated biofilm inhibition, attenuation of virulence and motility properties in Pseudomonas aeruginosa PAO1. Mar Drugs. 2019;17:208.30987163 10.3390/md17040208
165. El-Deeb NM Abo-Eleneen MA Al-Madboly LA Sharaf MM Othman SS Ibrahim OM Mubarak MS Biogenically synthesized polysaccharides-capped silver nanoparticles: immunomodulatory and antibacterial potentialities against resistant Pseudomonas aeruginosa Front Bioeng Biotechnol 2020 8 643 10.3389/fbioe.2020.00643 32793561
El-Deeb NM, Abo-Eleneen MA, Al-Madboly LA, Sharaf MM, Othman SS, Ibrahim OM, Mubarak MS. Biogenically synthesized polysaccharides-capped silver nanoparticles: immunomodulatory and antibacterial potentialities against resistant Pseudomonas aeruginosa. Front Bioeng Biotechnol. 2020;8:643.32793561 10.3389/fbioe.2020.00643
166. Najafi M Moghaddam MN Yousefi E The effect of silver nanoparticles on pyocyanin production of Pseudomonas aeruginosa isolated from clinical specimens Avicenna J Med Biotechnol 2021 13 98 34012526
Najafi M, Moghaddam MN, Yousefi E. The effect of silver nanoparticles on pyocyanin production of Pseudomonas aeruginosa isolated from clinical specimens. Avicenna J Med Biotechnol. 2021;13:98.34012526
167. Price-Whelan AM Physiology and mechanisms of pyocyanin reduction in Pseudomonas aeruginosa 2009 Pasadena California Institute of Technology
Price-Whelan AM. Physiology and mechanisms of pyocyanin reduction in Pseudomonas aeruginosa. Pasadena: California Institute of Technology; 2009.
168. Kipnis E Sawa T Wiener-Kronish J Targeting mechanisms of Pseudomonas aeruginosa pathogenesis Med Mal Infect 2006 36 78 91 10.1016/j.medmal.2005.10.007 16427231
Kipnis E, Sawa T, Wiener-Kronish J. Targeting mechanisms of Pseudomonas aeruginosa pathogenesis. Med Mal Infect. 2006;36:78–91.16427231 10.1016/j.medmal.2005.10.007
169. Kumar S Paliya BS Singh BN Superior inhibition of virulence and biofilm formation of Pseudomonas aeruginosa PAO1 by phyto-synthesized silver nanoparticles through anti-quorum sensing activity Microb Pathog 2022 170 105678 10.1016/j.micpath.2022.105678 35820580
Kumar S, Paliya BS, Singh BN. Superior inhibition of virulence and biofilm formation of Pseudomonas aeruginosa PAO1 by phyto-synthesized silver nanoparticles through anti-quorum sensing activity. Microb Pathog. 2022;170:105678.35820580 10.1016/j.micpath.2022.105678
170. Wei L Wu Q Zhang J Guo W Gu Q Wu H Wang J Lei T Xue L Zhang Y Prevalence, virulence, antimicrobial resistance, and molecular characterization of Pseudomonas aeruginosa isolates from drinking water in China Front Microbiol 2020 11 544653 10.3389/fmicb.2020.544653 33343513
Wei L, Wu Q, Zhang J, Guo W, Gu Q, Wu H, Wang J, Lei T, Xue L, Zhang Y. Prevalence, virulence, antimicrobial resistance, and molecular characterization of Pseudomonas aeruginosa isolates from drinking water in China. Front Microbiol. 2020;11:544653.33343513 10.3389/fmicb.2020.544653
171. Nikbin V Aslani MM Sharafi Z Hashemipour M Shahcheraghi F Ebrahimipour G Molecular identification and detection of virulence genes among Pseudomonas aeruginosa isolated from different infectious origins Iran J Microbiol 2012 4 118 23066485
Nikbin V, Aslani MM, Sharafi Z, Hashemipour M, Shahcheraghi F, Ebrahimipour G. Molecular identification and detection of virulence genes among Pseudomonas aeruginosa isolated from different infectious origins. Iran J Microbiol. 2012;4:118.23066485
172. Abozahra R El-Kholy MA Baraka K Virulence genotyping of drug resistant Pseudomonas aeruginosa clinical isolates in Egypt using multiplex PCR Gene Reports 2021 22 101000 10.1016/j.genrep.2020.101000
Abozahra R, El-Kholy MA, Baraka K. Virulence genotyping of drug resistant Pseudomonas aeruginosa clinical isolates in Egypt using multiplex PCR. Gene Reports. 2021;22:101000.10.1016/j.genrep.2020.101000
173. Saeki EK Martins HM Camargo LCD Anversa L Tavares ER Yamada-Ogatta SF Lioni LMY Kobayashi RKT Nakazato G Effect of biogenic silver nanoparticles on the quorum-sensing system of Pseudomonas aeruginosa PAO1 and PA14 Microorganisms 2022 10 1755 10.3390/microorganisms10091755 36144357
Saeki EK, Martins HM, Camargo LCD, Anversa L, Tavares ER, Yamada-Ogatta SF, Lioni LMY, Kobayashi RKT, Nakazato G. Effect of biogenic silver nanoparticles on the quorum-sensing system of Pseudomonas aeruginosa PAO1 and PA14. Microorganisms. 2022;10:1755.36144357 10.3390/microorganisms10091755
174. Singh BR Singh BN Singh A Khan W Naqvi AH Singh HB Mycofabricated biosilver nanoparticles interrupt Pseudomonas aeruginosa quorum sensing systems Sci Rep 2015 5 13719 10.1038/srep13719 26347993
Singh BR, Singh BN, Singh A, Khan W, Naqvi AH, Singh HB. Mycofabricated biosilver nanoparticles interrupt Pseudomonas aeruginosa quorum sensing systems. Sci Rep. 2015;5:13719.26347993 10.1038/srep13719
175. Liu L Li J-H Zi S-F Liu F-R Deng C Ao X Zhang P AgNP combined with quorum sensing inhibitor increased the antibiofilm effect on Pseudomonas aeruginosa Appl Microbiol Biotechnol 2019 103 6195 6204 10.1007/s00253-019-09905-w 31129741
Liu L, Li J-H, Zi S-F, Liu F-R, Deng C, Ao X, Zhang P. AgNP combined with quorum sensing inhibitor increased the antibiofilm effect on Pseudomonas aeruginosa. Appl Microbiol Biotechnol. 2019;103:6195–204.31129741 10.1007/s00253-019-09905-w
176. Hetta HF Al-Kadmy IM Khazaal SS Abbas S Suhail A El-Mokhtar MA Ellah NHA Ahmed EA Abd-Ellatief RB El-Masry EA Antibiofilm and antivirulence potential of silver nanoparticles against multidrug-resistant Acinetobacter baumannii Sci Rep 2021 11 10751 10.1038/s41598-021-90208-4 34031472
Hetta HF, Al-Kadmy IM, Khazaal SS, Abbas S, Suhail A, El-Mokhtar MA, Ellah NHA, Ahmed EA, Abd-Ellatief RB, El-Masry EA. Antibiofilm and antivirulence potential of silver nanoparticles against multidrug-resistant Acinetobacter baumannii. Sci Rep. 2021;11:10751.34031472 10.1038/s41598-021-90208-4
177. Stabryla LM Johnston KA Millstone JE Gilbertson LM Emerging investigator series: it’s not all about the ion: support for particle-specific contributions to silver nanoparticle antimicrobial activity Environ Sci Nano 2018 5 2047 2068 10.1039/C8EN00429C
Stabryla LM, Johnston KA, Millstone JE, Gilbertson LM. Emerging investigator series: it’s not all about the ion: support for particle-specific contributions to silver nanoparticle antimicrobial activity. Environ Sci Nano. 2018;5:2047–68.10.1039/C8EN00429C
178. Chaudhary V Mostafavi E Kaushik A De-coding Ag as an efficient antimicrobial nano-system for controlling cellular/biological functions Matter 2022 5 7 1995 1998 10.1016/j.matt.2022.06.024
Chaudhary V, Mostafavi E, Kaushik A. De-coding Ag as an efficient antimicrobial nano-system for controlling cellular/biological functions. Matter. 2022;5(7):1995–8.10.1016/j.matt.2022.06.024
179. Akter M Sikder MT Rahman MM Ullah AA Hossain KFB Banik S Hosokawa T Saito T Kurasaki M A systematic review on silver nanoparticles-induced cytotoxicity: physicochemical properties and perspectives J Adv Res 2018 9 1 16 10.1016/j.jare.2017.10.008 30046482
Akter M, Sikder MT, Rahman MM, Ullah AA, Hossain KFB, Banik S, Hosokawa T, Saito T, Kurasaki M. A systematic review on silver nanoparticles-induced cytotoxicity: physicochemical properties and perspectives. J Adv Res. 2018;9:1–16.30046482 10.1016/j.jare.2017.10.008
180. Hamida RS Ali MA Goda DA Khalil MI Al-Zaban MI Novel biogenic silver nanoparticle-induced reactive oxygen species inhibit the biofilm formation and virulence activities of methicillin-resistant Staphylococcus aureus (MRSA) strain Front Bioeng Biotechnol 2020 8 433 10.3389/fbioe.2020.00433 32548095
Hamida RS, Ali MA, Goda DA, Khalil MI, Al-Zaban MI. Novel biogenic silver nanoparticle-induced reactive oxygen species inhibit the biofilm formation and virulence activities of methicillin-resistant Staphylococcus aureus (MRSA) strain. Front Bioeng Biotechnol. 2020;8:433.32548095 10.3389/fbioe.2020.00433
181. Ihtisham M Noori A Yadav S Sarraf M Kumari P Brestic M Imran M Jiang F Yan X Rastogi A Silver nanoparticle’s toxicological effects and phytoremediation Nanomaterials 2021 11 2164 10.3390/nano11092164 34578480
Ihtisham M, Noori A, Yadav S, Sarraf M, Kumari P, Brestic M, Imran M, Jiang F, Yan X, Rastogi A. Silver nanoparticle’s toxicological effects and phytoremediation. Nanomaterials. 2021;11:2164.34578480 10.3390/nano11092164
182. Padmapriya S Murugan N Ragavendran C Thangabalu R Natarajan D Phytoremediation potential of some agricultural plants on heavy metal contaminated mine waste soils, salem district, tamilnadu Int J Phytorem 2016 18 288 294 10.1080/15226514.2015.1085832
Padmapriya S, Murugan N, Ragavendran C, Thangabalu R, Natarajan D. Phytoremediation potential of some agricultural plants on heavy metal contaminated mine waste soils, salem district, tamilnadu. Int J Phytorem. 2016;18:288–94.10.1080/15226514.2015.1085832
183. Yan A Wang Y Tan SN Mohd Yusof ML Ghosh S Chen Z Phytoremediation: a promising approach for revegetation of heavy metal-polluted land Front Plant Sci 2020 11 359 10.3389/fpls.2020.00359 32425957
Yan A, Wang Y, Tan SN, Mohd Yusof ML, Ghosh S, Chen Z. Phytoremediation: a promising approach for revegetation of heavy metal-polluted land. Front Plant Sci. 2020;11:359.32425957 10.3389/fpls.2020.00359
184. Gnanakani PE Santhanam P Premkumar K Kumar KE Dhanaraju MD Nannochloropsis extract–mediated synthesis of biogenic silver nanoparticles, characterization and in vitro assessment of antimicrobial, antioxidant and cytotoxic activities Asian Pac J Cancer Prev APJCP 2019 20 2353 10.31557/APJCP.2019.20.8.2353 31450906
Gnanakani PE, Santhanam P, Premkumar K, Kumar KE, Dhanaraju MD. Nannochloropsis extract–mediated synthesis of biogenic silver nanoparticles, characterization and in vitro assessment of antimicrobial, antioxidant and cytotoxic activities. Asian Pac J Cancer Prev APJCP. 2019;20:2353.31450906 10.31557/APJCP.2019.20.8.2353
185. Chahardoli A Karimi N Fattahi A Biosynthesis, characterization, antimicrobial and cytotoxic effects of silver nanoparticles using Nigella arvensis seed extract Iran J Pharm Res IJPR 2017 16 1167 29201104
Chahardoli A, Karimi N, Fattahi A. Biosynthesis, characterization, antimicrobial and cytotoxic effects of silver nanoparticles using Nigella arvensis seed extract. Iran J Pharm Res IJPR. 2017;16:1167.29201104
186. Liu X Shan K Shao X Shi X He Y Liu Z Jacob JA Deng L Nanotoxic effects of silver nanoparticles on normal HEK-293 cells in comparison to cancerous HeLa cell line Int J Nanomed 2021 16 753 761 10.2147/IJN.S289008
Liu X, Shan K, Shao X, Shi X, He Y, Liu Z, Jacob JA, Deng L. Nanotoxic effects of silver nanoparticles on normal HEK-293 cells in comparison to cancerous HeLa cell line. Int J Nanomed. 2021;16:753–61.10.2147/IJN.S289008
187. Lima R Feitosa L Ballottin D Marcato PD Tasic L Durán N Cytotoxicity and genotoxicity of biogenic silver nanoparticles J Phys Conf Ser 2013 429 012020 10.1088/1742-6596/429/1/012020
Lima R, Feitosa L, Ballottin D, Marcato PD, Tasic L, Durán N. Cytotoxicity and genotoxicity of biogenic silver nanoparticles. J Phys Conf Ser. 2013;429:012020.10.1088/1742-6596/429/1/012020
188. Arshad F Naikoo GA Hassan IU Chava SR El-Tanani M Aljabali AA Tambuwala MM Bioinspired and green synthesis of silver nanoparticles for medical applications: a green perspective Appl Biochem Biotechnol 2024 196 3636 3669 10.1007/s12010-023-04719-z 37668757
Arshad F, Naikoo GA, Hassan IU, Chava SR, El-Tanani M, Aljabali AA, Tambuwala MM. Bioinspired and green synthesis of silver nanoparticles for medical applications: a green perspective. Appl Biochem Biotechnol. 2024;196:3636–69.37668757 10.1007/s12010-023-04719-z
