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. 2022 Aug 30;16(7-8):284–294. doi: 10.1049/nbt2.12096

Biosynthesis of silver nanoparticles using Lawsonia inermis and their biomedical application

Eman Alhomaidi 1, Saade Abdalkareem Jasim 2, Hawraz Ibrahim M Amin 3,4, Marcos Augusto Lima Nobre 5, Mehrdad Khatami 6, Abduladheem Turki Jalil 7,✉, Saja Hussain Dilfy 8,9
PMCID: PMC9469786  PMID: 36039655

Abstract

Developing biosynthesis of silver nanoparticles (Ag‐NPs) using plant extract is an environmentally friendly method to reduce the use of harmful chemical substances. The green synthesis of Ag‐NPs by Lawsonia inermis extract and its cellular toxicity and the antimicrobial effect was studied. The physical and chemical properties of synthesised Ag‐NPs were investigated using UV‐visible spectroscopy, infrared spectroscopy, X‐ray diffraction (XRD), scanning, and transmission electron microscopy. The average size of Ag‐NPs was 40 nm. The XRD result shows peaks at 2θ = 38.07°, 44.26°, 64.43°, and 77.35° are related to the FCC structure of Ag‐NPs. Cytotoxicity of synthesised nanoparticles was evaluated by MTT toxicity test on breast cancer MCF7 cell line. Observations showed that the effect of cytotoxicity of nanoparticles on the studied cell line depended on concentration and time. The obtained IC50 was considered for cells at a dose of 250 μg/ml. Growth and survival rates decreased exponentially with the dose. Antimicrobial properties of Ag‐NPs synthesised with extract were investigated against Escherichia coli, Salmonella typhimurium, Bacillus cereus, and Staphylococcus aureus to calculate the minimum inhibitory concentration and the minimum bactericidal concentration of (MBC). The results showed that the synthesised Ag‐NPs and the plant extract have antimicrobial properties. The lowest concentration of Ag‐NPs that can inhibit the growth of bacterial strains was 25 μg/ml.

Keywords: AgNPs, antibacterial activity, Lawsonia inermis, UV‐visible spectroscopy, X‐ray diffraction

1. INTRODUCTION

Nano comes from an ancient Greek word, and in the metric system, the term ‘nanometre’ means one‐billionth of a metre [1]. Nano‐sized particles are called nanoparticles [2]. Nanotechnology is an interdisciplinary knowledge of various disciplines [3, 4], including physics [5, 6], materials [7, 8, 9], engineering [10, 11, 12], mechanical engineering [13, 14, 15, 16], agriculture [17], energy [18, 19, 20] and biology [21, 22, 23, 24, 25]. Recently, nanoparticles have been successfully used for sustained drug release [26], photo‐catalytic [27, 28, 29], degradation [30, 31, 32, 33, 34], detection [35, 36, 37, 38, 39], treatment of infections [40], and in the food industry as potent anti‐oxidant [41, 42], larvicidal [43], antifungal [44] and antibacterial agents [45, 46]. Various methods for producing nanoparticles are classified into three general methods: physical, chemical, and biological [47, 48]. Production is carried out by a simple chemical method, but there is a possibility that toxic substances resulting from the reaction will remain on the produced nanoparticles. There are standard chemical methods for preparing and manufacturing nanomaterials, such as sol‐gel [49]. Due to the use of hazardous chemical substances, the nanoparticles resulting from these methods carry out reactions under particular conditions (temperature and pressure), which are expensive and time‐consuming and create potential environmental risks. The physical method of nanoparticles has low toxicity, but it is most time consuming, dependent on expensive equipment, and has high energy consumption [50]. Due to these disadvantages and problems of using physical and chemical methods, the biological production method using plant extract is of interest today [48, 51, 52]. Plant extracts are considered to be the most pressing sources of biomolecules [53, 54, 55, 56] such as proteins, nucleic acids [57], oils [58, 59, 60, 61] and carbohydrates [62, 63]. Plant biomolecules have been identified to play an active role in the formation of nanostructures [64]. Biological methods are easy and cheap and have less toxicity [65] and production of toxic byproducts than common chemical and physical methods [66]. This method of producing nanoparticles is called the green method [67]. The energy consumption in this method is much less than chemical methods, and due to the compatibility with the environment, it is necessary to develop green methods [68]. New developments in science [69, 70, 71, 72, 73, 74, 75] and technology [76] have significant impact on human health [77, 78, 79, 80, 81] and life [82, 83].

Green methods [84] produced various silver [85], gold [86], copper [87], zinc [88], yttrium oxide [89], chromium (III) oxide [90], iron [91, 92], gallium nitride [93], boron nitride [94], aluminum nitride [95], calcium [96], zirconium/zirconium dioxide [97, 98, 99], palladium [100, 101], and tin oxide [102] nanoparticles. Gold and Ag‐NPs have many applications in producing antimicrobial substances and diagnostic kits. Silver and gold have been used since ancient times because they have strong antibacterial [103], antifungal and antiviral properties [104]. Ag‐NPs are helpful in different research fields such as medicine research [105] and nanoelectronics. Also, they can destroy cancer cells [106]. These particles can bind to cancer cells through a molecular coating and destroy the cancer cells. Also, new technologies have recently been developed to treat infection [83, 107, 108, 109, 110, 111] and cancerous tumours [112, 113, 114].

Ag‐NPs are a suitable option for preparing a new generation of anticancer and antimicrobial agents due to their intense biocidal activity and specific mechanism of action [115, 116]. Ag‐NPs also disrupt biofilm formation. Although silver has been used as an antibacterial agent for centuries, recently, scientists have paid much attention to this element to solve the problem of drug resistance due to the improper use of antibiotics [117, 118, 119]. Studies show that by binding to the bacterial cell wall, Ag‐NPs disrupt the cell wall's permeability and damage the cell. Ag‐NPs also penetrate the cell and form a complex with thiol groups in the amino acid cysteine, thereby inactivating the vital enzymes of cell growth. Also, nanoparticles cause the formation of toxic free radicals such as superoxide, hydrogen peroxide, and hydroxyl ions and affect cellular respiration [120].

They were considering that the study on the toxicity of biogenic Ag‐NPs produced by a green method using Lawsonia inermis has not been reported so far. Therefore, the present study aims to produce Ag‐NPs by plant extract and investigate their antimicrobial and cytotoxic effects on Breast cancer cell lines.

2. MATERIAL AND METHOD

2.1. Synthesis of Ag‐NPs

Lawsonia inermis leaves were collected from a local market in Kerman, Iran. To remove any dust contents from leaves, the surface was washed with water, then washed twice with sterile distilled water and dried at 25°C.

The method reported by Khatami et al. [121] was used for the green synthesis of Ag‐NPs. Briefly, silver nitrate stock was prepared with a concentration of 500 mg in 50 ml of deionised water. Five grams of L. inermis dry leaf powder was added to 100 ml of deionised water and heated at 75°C for 15 min. After filtering through Whatman No. 40 filter paper, the filtered extract was used to synthesise Ag‐NPs.

For the synthesis of Ag‐NPs, leaf extract and AgNO3 were mixed. In order to determine the optimal ratios, the extract and silver nitrate solution was used in ratios of 1:1, 2:1, and 3:1, respectively, and the optimal ratio at which the synthesis of Ag‐NPs occurred was determined. In order to determine the optimal ratios, the visual colour change was the first visible sign of Ag‐NPs synthesis with the naked eye. Concentrations in which no colour change was observed were determined as non‐optimal ratios and were excluded from further study. Finally, the optimal concentration of the extract and AgNO3 solution was used for the synthesis and determination of the properties of the synthesised Ag‐NPs. The synthesis of Ag‐NPs was investigated by UV‐vis spectral analysis after observing the colour change of the reaction mixture to dark brown. Nanoparticles synthesised with plant extract were first centrifuged at 12,000 rpm for 10 min and settled. They have dissolved again in deionised water. Then, centrifugation was performed at 13,000 rpm to separate the synthesised nanoparticles. It was repeated two times between the operations. Then the synthesised Ag‐NPs were dried and used to determine other physicochemical properties.

2.2. Determination of physicochemical properties

To determine the size, structural properties, and morphology of Ag‐NPs synthesised from plant extract, spectrophotometer devices (Biotek, US), X‐ray diffraction (XRD) devices, field emission scanning electron microscope (FESEM), and transmission electron microscope (TEM) were analysed. The XRD pattern was used to determine the crystalline phases of synthesised Ag‐NPs, measure the crystal constants of Ag‐NPs and calculate the crystal size. To prepare the XRD pattern, a Philips X'pert Pro device made in the Netherlands was used with a Cu Kα copper anode lamp source with a wavelength of λ = 1.5406 Å. To determine the size and dispersion distribution of Ag‐NPs synthesised from plant extract, an LEO‐912AB TEM with an applied voltage of 120 kV was used to emit electron beams [122]. The morphology of Ag‐NPs synthesised from the extract was investigated by FESEM. To prepare the sample for imaging, the nanoparticle powder is covered with a skinny layer of gold to make the surface conductive so that it does not change the path of the returning electron beams. Also, the Ag‐NP powder should be spread on a surface that is more conductive than aluminum. The FTIR spectroscopic test was performed to identify active groups and reducing groups of silver ions in the range of 500–3500 cm−1 [123, 124].

2.3. Investigation of cytotoxicity

In the MTT method, the viability or non‐viability of cells in the mitochondrial respiratory cycle was investigated. For this purpose, the MCF7 cell line was obtained from the Pasteur Institute of Iran and cultured in an RPMI1640 culture medium enriched with 10% FBS serum. Then, they were kept in a cell culture flask at 37°C in a humid atmosphere with a concentration of 5% CO2. The cells were collected from the flask, and after adding the culture medium, the cell suspension was transferred to each well of the 96‐well plate with a volume of 100 ml of the cell suspension and the amount of 10,000 cells. Then it was incubated under culture conditions. After 24 h, the culture medium was drained, and Ag‐NPs with concentrations of 1–500 μg/ml were added to each well. In the control group in this test, wells containing untreated cells were considered. After incubation, 10 μL of MTT dye (tetrazolium salt) with a concentration of 5 mg/ml were added to each well in the dark, and the incubation was done for 4 h. Then, 100 ml of Dimethyl Sulfoxide (DMSO) were added to each well. The optical absorbance of the samples was read with an ELISA device, and the results of the absorbance value were recorded at a wavelength of 570 nm. The results were calculated in terms of the percentage of living cells treated compared to untreated from the following equation: 100* (optical absorbance of untreated cells/optical absorbance of cells treated with nanoparticles) = % living cells.

2.4. Cell viability percentage using cell proliferation kit

After the culture cells covered more than 85% of the culture flasks, they were re‐suspended by trypsinisation. Cell viability was determined with trypan blue solution; after 24 h of incubation, the cells were exposed to different concentrations of Ag‐NPs. They were incubated for 24 h. Cell viability was determined at the end of the period using a cell proliferation kit. The absorbance values of the cells in each well were checked at 450 nm. Cell viability percentage values were calculated.

2.5. Investigating the antioxidant effect

Cell extracts were first prepared to investigate the effect of Ag‐NPs on the activity of antioxidant enzymes in the tested cells. After cultivation and treatment, the cells were separated using EDTA trypsin. After centrifugation, they were washed twice with cold PBS. Then 300 ml of lysate buffer were added to the sediment of the cells, and after 20 min of centrifugation at 4°C With 10,000 RPM, the resulting supernatant was used to perform the test. The measurement of the total protein of the samples was done using the Bradford method. Also, the superoxide dismutase enzyme was measured based on the inhibition of nitroblue tetrazolium reduction by the enzyme present in the sample. The measurement of catalase was also based on the reduction of hydrogen peroxide per unit of time due to the enzyme activity in the sample.

2.6. Investigation of antimicrobial effect

Bacterial pathogens of Escherichia coli, Salmonella typhimurium, Bacillus cereus, and Staphylococcus aureus were obtained from the Centre of Biological and Genetic Resources of Iran. The antimicrobial activity of the Ag‐NPs was measured by measuring the halo of non‐growth and diffusion method from the well on the agar surface. In this method, after preparing a microbial suspension with turbidity equal to half McFarland (CFU/ml 108), cultivation was done using a sterile glass rod on the surface of the Mueller Hinton agar culture medium. After drying the surface of the culture medium plates, with the help of a sterile Pasteur pipette, three wells with a diameter of 5 mm were created at a suitable distance from each other. Then, 50 ml of the Ag‐NPs were poured into the created wells after being dispersed in sterile deionised water using an ultrasonic bath. The plates were incubated for 24 h at 37°C. Double distilled water on a blank disk was used as a negative control. Finally, the sensitivity of bacteria was measured by measuring the diameter of the non‐growth halo with the help of callipers. This experiment was repeated three times for each bacterium, and the arithmetic mean of the area diameter (mm) was reported.

2.7. Statistical analysis

Data were recorded as mean with standard deviation. One‐way analysis of variance (ANOVA) was used to identify significant differences between the tested groups. All data analyses were evaluated based on significance at the 0.05 level.

3. RESULTS

Ag‐NPs were synthesised by aqueous extract. The colour change from pale yellow to dark brown indicates the production of Ag‐NPs (Figure 1).

FIGURE 1.

FIGURE 1

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Colour change from pale yellow (plant extract) to dark brown (Ag‐NPs)

The results of the spectrophotometric analysis with ultraviolet light in the control sample (extract alone) and after the synthesis of Ag‐NPs are shown in Figure 2. The increase in absorbance in the range of 450–500 nm indicates the synthesis of Ag‐NPs. The UV‐Vis spectrum shows a surface plasmon resonance (SPR) of Ag‐NPs at about 420 nm [125, 126].

FIGURE 2.

FIGURE 2

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UV‐visible spectrum of Ag‐NPs synthesised with different ratios (0:1, 1:1, 2:1, and 3:1) of extract and silver nitrate solution

The results of FTIR spectroscopic analysis before and after the reaction with silver nitrate are shown in Figure 3. The comparison of two spectroscopic graphs shows the aqueous extract's biological power in reducing silver ions. There are peaks related to vibrations at wavelengths of 599, 674, 1151, 2357, and 3446, which are, respectively, related to alkyl, alkene, carbonyl (CO), CO2, and hydroxyl (OH) groups [127, 128].

FIGURE 3.

FIGURE 3

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FTIR spectrum before (a) and after (b) the synthesis of Ag‐NPs

Figure 4 shows electron microscope images (TEM) of Ag‐NPs synthesised with plant extract. As it is clear from the images, the Ag‐NPs in the image have a spherical shape and have a proper distribution, and around the nanoparticles, a bright background can be seen, which is related to the extract because the density of the extract is different from the light passing through the density. Ag‐NPs are few, so Ag‐NPs are darker in the image, and the solvent is brighter. According to the TEM image, the size of nanoparticles has a diameter ranging from 20 to 70 nm; with a normal distribution, the average diameter is around 40 nm.

FIGURE 4.

FIGURE 4

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TEM images of synthesised Ag‐NPs

Figure 5a shows FESEM images of Ag‐NPs synthesised with plant extract. The FESEM image shows the silver particles' nm dimensions and an almost spherical shape in all magnifications. Determining the size of Ag‐NPs through FESEM is not accurate because the resolving power of FESEM is lower than that of TEM, so TEM analysis was used to report the average size. According to FESEM images, the cumulative size of nanoparticles is below 100 nm. In the EDX analysis, the peak related to silver metal was seen, indicating that the Ag‐NPs observed in the SEM images are made of silver (Figure 5b). Observing the optical absorption band at 3 Kev indicates the presence of silver metal nanoparticles. Of course, the presence of peaks of elements C and O in the EDX spectrum is related to the residues caused by the substances in the supernatant of the extract, such as enzyme or protein residues.

FIGURE 5.

FIGURE 5

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FESEM image (a) and EDX spectrum (b) of resulting green synthesised Ag‐NPs

Figure 6 shows the XRD pattern of plant extract alone (Figure 6a) and Ag‐NPs (Figure 6b). As can be seen, the peaks at 2θ = 38.07°, 44.26°, 64.43°, and 77.35° corresponding to (111), (200), (220), and (311) are related to the FCC structure of Ag‐NPs, which is in perfect agreement with the standard XRD pattern of silver. The crystal size of Ag‐NPs is obtained from Scherrer equation: L = Kλ/β. Cosθ. In this equation, k = 0.9 is the shape factor and λ is the wavelength of the X‐ray and is equal to 1.5406 Å. ß is the full width at half the maximum of the diffraction peak, and θ is the angle corresponding to the diffraction peak. From the calculation of Scherrer's relation, the crystal size of nanoparticles is 40 nm, which is consistent with TEM images.

FIGURE 6.

FIGURE 6

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XRD pattern of plant extract (a) and resulting synthesised Ag‐NPs (b)

MTT test was performed to investigate the effect of Ag‐NPs on cell viability for 24 h and with concentrations of 1–500 μg/ml. The statistical results showed that the viability of the cells after exposure to these doses of Ag‐NPs decreased significantly compared to the control sample (Figure 7). The obtained IC50 was considered for cells at a dose of 250 μg/ml. Growth and survival rates decreased exponentially with the dose.

FIGURE 7.

FIGURE 7

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The cell viability of MCF‐7 cells treated with Ag‐NPs

In cell treatment groups, the IC50 concentration of Ag‐NPs overtime on days 1%, 2% and 5% of cell survival decreased. The trypan blue staining method was also used to confirm the results of the MTT assay. Cells after treatment with IC50 concentration of Ag‐NPs treatment on days 1, 2 and 5 with trypan blue dye were counted using a neobar slide. This method confirmed the results of the MTT assay. On the fifth day after the treatment, all the cells of the treatment group were separated from the bottom of the well and placed in cell count under the neobar slide was not seen.

After treatment with IC50 concentration of Ag‐NPs, cancer cells were observed and examined with a microscope. Compared to the control group, changes were observed in the cell morphology of the treatment groups, including cell spheroidisation and shrivelling. Over time, these changes were observed in a more significant number of treatment cells so that after 2 days, the cells of the treatment group were suspended and dead. In order to more closely examine the morphological changes after the treatment of the cells, they were stained with Giemsa dye and observed by an optical microscope. The morphology of the cells in the control sample was utterly ordinary, so the cells were with healthy membranes and some were seen dividing. However, the treated cells showed changes such as a reduction in cell volume, cell granulation, chromatin condensation inside the nucleus, and the production of apoptotic bodies.

To determine the type of cell death induced by nanoparticles on the cell line, the acridine orange/ethidium bromide staining method was used. In this staining, living cells are seen in green, while cells in the apoptosis stage are seen in orange. In the groups treated with Ag‐NPs, the number of cells with orange colour increased significantly compared to the control group.

The Bradford method was used to measure the protein concentration in all samples (treatment and control), and its standard diagram was first drawn. Then, using the standard graph and its line equation, the protein concentration was measured. Protein concentration was measured to express the amount of enzyme activity in milligrams of protein. After calculating the amount of superoxide dismutase and catalase enzymes in the control group, the treated group with IC50 concentration of Ag‐NPs and statistical analysis, a diagram was drawn. The results showed that the activity of the superoxide dismutase enzyme in the Ag‐NP treatment group was significantly increased compared to the control (P < 0.001). The results showed that the catalase enzyme activity increased significantly in the Ag‐NP treatment group compared to the control group (P < 0.05).

In short, the most common mechanism for the antibacterial effect of Ag‐NPs is that Ag‐NPs release ionic silver and deactivate the thiol groups in the enzymes, which cause the inactivation of bacterial enzymes. The released silver ions inhibit bacterial DNA replication, damage the cell cytoplasm, decrease the level of adenosine triphosphate (ATP) and ultimately lead to the death of the bacterial cell. Increasing the ratio of the surface area to the volume of nanoparticles increases the level of attachment of nanoparticles to bacterial cells and increases the release of silver ions to bacteria, thus improving the antibacterial effect of silver [129].

DPPH radical was used to evaluate natural antioxidants' free radical scavenging activity [130]. The results showed that Ag‐NPs synthesised with leaf extract showed free radical inhibition activity. The antioxidant activity or, in other words, the free radical scavenging activity of Ag‐NPs synthesised by the leaf extract increased dose‐dependent (Figure 8).

FIGURE 8.

FIGURE 8

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DPPH radical Ag‐NPs

4. CONCLUSION

In this research, the possibility of producing Ag‐NPs by L. inermis extract and its antimicrobial and anticancer effects were studied. Based on the results, Ag‐NPs produced by aqueous extract had a size of less than 100 and showed effective antimicrobial and anticancer activity. These particles caused the non‐growth of tested bacteria, and gram‐negative bacteria are more sensitive than gram‐positive bacteria. The synthesis of Ag‐NPs can be produced on an industrial scale without needing expensive raw materials. Considering the antimicrobial property of these particles on the tested strains, they can be used as an effective disinfectant for sterilising the hospital environment and disinfecting hospital waste. Ag‐NPs reduce the survival of cancer cells in a dose‐dependent manner. Ag‐NPs synthesised from L. inermis extract can be used in breast cancer treatment.

CONFLICT OF INTEREST

The authors declare that they have no conflict of interest.

ACKNOWLEDGEMENT

This work was funded by Princess Nourah Bint Abdulrahman University Researchers Supporting Project number (PNURSP2022R317), Princess Nourah bint Abdulrahman University, Riyadh, Saudi Arabia.

Alhomaidi, E. , et al.: Biosynthesis of silver nanoparticles using Lawsonia inermis and their biomedical application. IET Nanobiotechnol. 16(7-8), 284–294 (2022). 10.1049/nbt2.12096

DATA AVAILABILITY STATEMENT

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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