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Original article
12 (
8
); 3977-3992
doi:
10.1016/j.arabjc.2016.02.017

Gummy gold and silver nanoparticles of apricot (Prunus armeniaca) confer high stability and biological activity

, , ,
a Department of Pharmacy, Sarhad University of Science and Information Technology, Peshawar, Pakistan
b Institute of Chemical Sciences, University of Peshawar, Peshawar, Pakistan
c Department of Chemistry, Islamia College University, Peshawar, Pakistan

⁎Corresponding author at: Department of Pharmacy, Sarhad University of Science and Information Technology, Peshawar 25000, Pakistan. Tel.: +92 919239305. islanaz@yahoo.com (Nazar Ul Islam),

Received: , Accepted: ,
© The Author(s) 2016
Disclaimer:
This article was originally published by Elsevier and was migrated to Scientific Scholar after the change of Publisher.

Peer review under responsibility of King Saud University.

Abstract

Gold and silver nanoparticles (Au- and Ag-NPs) were biosynthesized using the gum extract of Prunus armeniaca. These were characterized with UV–Vis spectroscopy, FTIR, SEM, EDX, XRD and atomic absorption (AA). The effect of gum and metal ions concentration, reaction temperature and time on the synthetic stability of nanoparticles was studied along with their post-synthetic stability against varying pH and salt concentrations, long term storage and extreme of temperature. Au- and Ag-NPs were also tested for antibacterial, antinociceptive and anti-inflammatory activities. Formation of Au- and Ag-NPs was confirmed from the surface plasmon resonance centered at 555 and 450 nm respectively and was further corroborated from the results of FTIR, EDX, XRD and AA. SEM analysis showed that Au- and Ag-NPs were mostly spherical and in the size range of 5–40 nm. It was observed that 0.5% w/v gum, 3 mM Au/Ag ions solution, reaction temperature of 80 °C and reaction time of 4 h were suitable for the efficient synthesis of Au- and Ag-NPs. The results of post-synthetic stability revealed that Au- and Ag-NPs were stable in different concentrations of NaCl (1–3 M), neutral to acidic pH (7–2) and without any long term storage (eight months) or thermal (100 °C) induced degradable changes. The TGA spectrum further confirmed their thermal stability, where three successive weight losses were observed in the temperature range of 50–800 °C. Au- and Ag-NPs possessed mild to moderate antibacterial activity as observed from their zone of inhibition against Staphylococcus aureus (10 ± 0.3 mm, 18 ± 0.5 mm), Escherichia coli (9 ± 0.5 mm, 10.2 ± 0.8 mm) and Pseudomonas aeruginosa (7.9 ± 0.3 mm, 11.2 ± 0.3 mm). Au-NPs significantly alleviated the acetic acid induced writhes at much lower doses of 40 mg/kg (P < 0.01) and 80 mg/kg (P < 0.001) compared to that of gum extract at 200 and 400 mg/kg (P < 0.001). At similar doses, Au-NPs also significantly inhibited the carrageenan induced paw edema during the 1st h (P < 0.05) and 2–5 h (P < 0.001) of the study duration.

Keywords

Gold and silver nanoparticles
Prunus armeniaca
Gum
Stability
Antinociceptive
Anti-inflammatory
1

1 Introduction

Plant mediated synthesis of nanoparticles is a promising area of research and recently there has been an upsurge in the use of various medicinal plants for the synthesis of metallic nanoparticles (Kumar and Yadav, 2009). Nanoparticles are of great scientific interest as they bridge the gap between bulk materials and atomic or molecular structures. Metallic nanoparticles find widespread applications in electronics, cosmetics, coatings, packaging, medicine, and biotechnology (Thakkar et al., 2010). Among the various metal nanoparticles, gold and silver nanoparticles have attracted great interest due to their unique electrical, electronic, thermal, optical, magnetic, catalytic, sensing and antimicrobial functionalities compared to their corresponding bulk metals (Sharma et al., 2009). The synthesis of nanoparticles by various physical and chemical methods, such as laser radiation (Sivakumar et al., 2009), ultrasound irradiation (Kundu et al., 2007), chemical reduction (Song et al., 2009), evaporative cooling (Fisenko and Khodyko, 2009), chemical vapor deposition (Li et al., 2004), explosion (Wu et al., 2003), impregnation (Tsoncheva et al., 2008), co-precipitation (Yang et al., 2003), sol–gel (Lu et al., 2002), and deposition–precipitation (You et al., 2005) have been extensively reported.

The importance of plants in the synthesis of nanoparticles, so called “green synthesis” or “bio-inspired synthesis” can be verified from the fact that the various physical and chemical methods used for the efficient synthesis of nanoparticles are expensive and hazardous to the environment. This is due to the use of certain toxic chemicals in the synthesis protocol or formation of harmful by-products. Synthesis of metallic nanoparticles using plant extracts is inexpensive, easily scaled up, environmentally benign and especially suited for making nanoparticles that are free of toxic contaminants as required in therapeutic applications (Mittal et al., 2013). Moreover, most of the biologically active constituents of plants extracts, such as flavonoids, tannins, and terpenoids, are highly water-soluble, but demonstrate a low absorption, because they are unable to cross lipid membranes, have high molecular sizes, and are poorly absorbed, resulting in loss of bioavailability and efficacy. Nano delivery system has the ability not only to increase the bioavailability of active components, but also improve their selectivity and efficacy, protecting against thermal- or photo-degradation, reducing side effects, and controlling the release of active constituents (Bonifácio et al., 2014; Islam et al., 2015).

Apricot, Prunus armeniaca L., (family; Rosaceae) is widely consumed in abundant amounts either as fresh fruit or processed into apricot juice, nectar, jam, or dried fruit during the summer season. It is a traditional drug that is used in oriental medicine to treat various diseases, including asthma, bronchitis, emphysema, constipation, nausea, leprosy, and leucoderma (Hwang et al., 2008). Apricot has been studied for its hepatoprotective (Ozturk et al., 2009; Yurt and Celik, 2011), antinociceptive (Hwang et al., 2008), anti-inflammatory (Minaiyan et al., 2013), antioxidant and antiradical capacities (Durmaz and Alpaslan, 2007; Engel et al., 2010; Erden et al., 2013), gastro-protective (Vardi et al., 2008), nephroprotective (Vardi et al., 2013), anti-mutagenic (Yoo et al., 2007), anti-carcinogenic (Karabulut et al., 2014), antibacterial, antifungal (Yiğit et al., 2009), cardio-protective (Parlakpinar et al., 2009), testicular protective (Kurus et al., 2009; Ugras et al., 2010) and tyrosinase (Matsuda et al., 1994) as well as trypsin (Gahloth and Sharma, 2010) inhibition activities. The purported medicinal properties of apricot have been attributed to the presence of rich phytochemical compounds including phytosterols, flavonoids, polyphenols and vitamins (Erden et al., 2013).

P. armeniaca fruit has been used as a reducing agent for the efficient synthesis of gold and silver nanoparticles and showed considerable potential for free radical scavenging activity (Dauthal and Mukhopadhyay, 2013). In the majority of plant mediated synthesis of nanoparticles, generally the leaves, roots or fruit parts of plants are used while the gum part is usually ignored. Natural plant based gums offers a number of advantages as they are biodegradable, bio-compatible, non-toxic, having low cost and are widely available (Jani et al., 2009). We therefore reported for the first time the biosynthesis of gold and silver nanoparticles (Au- and Ag-NPs) using the gum solution of P. armeniaca which proves to be much cheaper compared to the other reported methods. P. armeniaca gum has previously undergone phytochemical evaluation and disclosed the presence of 4–0-methyl-d-glucuronic acid, d-glucuronic acid, d-xylose, l-arabinose, d-galactose in a molar ratio of 0.6:1:0.3:3.2:3.2, and traces of d-mannose (Rosik, 1968). Au- and Ag-NPs were characterized using various spectroscopic and microscopic techniques. We elucidated their stability and studied the effect of gum, tetrachloroauric acid trihydrate (HAuCl4·3H2O) and silver nitrate (AgNO3) concentration, reaction temperature and time on the synthesis of Au- and Ag-NPs. We subjected the biosynthesized nanoparticles to varying NaCl concentration, pH, long term storage conditions and high temperature. The apricot gum functionalized Au- and Ag-NPs were also tested for the first time against various pathogenic bacterial strains. Moreover, the gold nanoparticles (Au-NPs) were assessed for antinociceptive and anti-inflammatory activities, but at much lower doses compared to that of gum alone.

2

2 Experimental

2.1

2.1 Materials

Tetrachloroauric acid trihydrate (HAuCl4·3H2O, 99.5%) and silver nitrate (AgNO3, 99.9%) were purchased from Merck, Germany. P. armeniaca fresh gum (PAG) was purchased from the local market in April 2013. Water was purified through Milli-Q-SP ultra pure water purification system.

2.2

2.2 Synthesis of gold and silver nanoparticles

For the synthesis of Au- and Ag-NPs, 1 mM stock solutions of tetrachloroauric acid trihydrate and silver nitrate were prepared. Similarly 0.5% w/v stock solution of PAG was prepared in purified water. The solutions were centrifuged at 6000 rpm for 10 min to remove bulk impurities. The aqueous solutions of tetrachloroauric acid and silver nitrate were reduced by mixing with 0.5% PAG solution in differing ratios and stirred gently at temperatures of 20, 40, 60 and 80 °C. The optimized product having surface plasmon resonance (SPR) at 555 nm for Au-NPs was obtained by mixing 8 ml of tetrachloroauric acid solution (1 mM) and 5 ml of 0.5% w/v PAG solution at a temperature of 80 °C and a reaction time of 5 h. Similarly, in case of Ag-NPs, the optimized product having SPR at 450 nm was obtained by mixing 20 ml of silver nitrate solution (1 mM) and 8 ml of 0.5% w/v PAG solution at a temperature of 80 °C.

2.3

2.3 Characterization of gold and silver nanoparticles

The formation of gold and silver nanoparticles was assessed on a double beam UV–Vis spectrophotometer (Lambda 25, Perkin Elmer) in the spectral range of 250–800 nm. The nanoparticles were further characterized with an FTIR spectrophotometer (Prestege-21 Shimadzu, Japan), scanning electron microscope (JSM-5910, England), energy dispersive X-ray spectrometer (INCA-200, England), X-ray diffractometer (RX-III, Shimadzu, Japan) at 40 kV and 30 mA with Cu Kα radiation (λ = 0.1542 nm) and atomic absorption spectrophotometer (AAS-700 Perkin Elmer, USA). Thermo gravimetric analysis was performed on a Diamond TG/DTA Perkin Elmer, USA thermogravimetric analyzer.

2.4

2.4 Assessment of stability

The effect of gum concentration on the synthesis of Au- and Ag-NPs was studied by heating different concentrations (0.1–0.5%) of gum solutions containing 1 mM of tetrachloroauric acid and silver nitrate solutions respectively for 1 h. The effect of Au or Ag ions concentration was studied by changing their concentration from 1 to 5 mM and then heated at constant temperature of 80 °C for 3 h. The effect of temperature on the synthesis of Au- and Ag-NPs was studied at temperatures of 20, 40, 60, 80 °C, each for 3 h. Nanoparticles synthesis was also evaluated at varying reaction time (1–5 h) and reduction was studied with 0.5% gum at 1 mM Au or Ag salt solution.

The effect of NaCl on the stability of nanoparticles was checked by preparing different concentration of NaCl solution (1, 2 and 3 M) in purified water. Accurately measured 3 ml nanoparticles solutions of gum extract with Au or Ag were taken in vials. 20 μl of different concentrations of NaCl solution was added to vials and kept for 3 h to ensure thorough mixing of both solutions before measurement.

For the effect of pH on the stability of nanoparticles, the biosynthesized nanoparticles solutions were taken in vials and pH was adjusted to different values (2–3, 4–5, 6–7, 8–9, 10–11, 12–13) by drop wise addition of 1 M HCl or NaOH solution. These were kept for some time and their absorption was then recorded. The long term stability of the biosynthesized Au- and Ag-NPs was assessed by keeping the nanoparticles at room temperature for eight months. The extreme thermal stability was evaluated by heating the nanoparticles at 100 °C for 30 min.

2.5

2.5 Biological activity

2.5.1

2.5.1 Antibacterial activity

The antibacterial activity of Au- and Ag-NPs was determined by the disk well diffusion method against the Gram positive and Gram negative strains of Staphylococcus aureus (ATCC 25923), Escherichia coli (ATCC 25922), and Pseudomonas aeruginosa (ATCC 27853) respectively. Three independent experiments were carried out for each bacterial strain using streptomycin as standard. 5 μg of dried Au- and Ag-NPs was dissolved in DMSO and incubated at 30 °C for 24 h.

2.5.2

2.5.2 Animals

BALB/c mice of either sex weighing 25–30 g and purchased from the National Institute of Health (NIH), Islamabad, were used in the experiments. The animals were maintained in a 12 h light/dark cycle at 22 ± 2 °C for one week prior to experiments. Access to food and water was ad libitum. Experiments on animals were performed according to the NIH guidelines for the care and use of laboratory animals.

2.5.3

2.5.3 Acetic acid induced writhing test

BALB/c mice of either sex weighing 25–28 g were used for the determination of antinociceptive activity of P. armeniaca gum and its Au-NPs using the acetic acid induced abdominal constriction assay (Collier et al., 1968). The animals were withdrawn from food 2 h before the start of experiment. These animals were then divided into six groups. Group I received normal saline. Group II was administered with the standard diclofenac sodium (50 mg/kg, i.p). Group III and IV received P. armeniaca gum extract at 200 and 400 mg/kg, while groups V and VI were treated with Au-NPs at doses of 40 and 80 mg/kg, respectively through an oral gavage tube. After 30 min of treatment the animals were injected with 1% acetic acid (10 ml/kg, i.p). Writhes were counted after 5 min of acetic acid injection and the observation was continued for 20 min.

2.5.4

2.5.4 Anti-inflammatory activity of nanoparticles

BALB/c mice of either sex weighing 27–30 g were used for the determination of anti-inflammatory activity of P. armeniaca gum and its Au-NPs using carrageenan induced paw edema assay (Morris, 2003). The animals were fasted for 4 h before the start of experiment and were then divided into seven groups. P. armeniaca extract (200 and 400 mg/kg) and Au-NPs (40 and 80 mg/kg) were administered by an oral gavage tube. Diclofenac sodium was used as standard and was injected i.p at a dose of 50 mg/kg. After 30 min of treatment, all the animals were challenged with 50 μl of 1% solution of carrageenan, injected into the plantar surface of the left hind paw. The anti-inflammatory effect was evaluated by measuring the paw volume of each animal using a digital plethysmometer after each hour of 5 h study duration.

2.6

2.6 Statistical analysis

Data were expressed as mean ± SD or SEM. Statistical analysis was done by one way ANOVA followed by Dunnett’s or Tukey’s post hoc test where appropriate using GraphPad Prism 5 (GraphPad Software Inc. San Diego CA, USA).

3

3 Results and discussion

3.1

3.1 UV–Vis spectroscopy

Formation of gold and silver nanoparticles in aqueous colloidal solution was confirmed from the UV–Vis spectra as well as from the appearance of ruby red and light yellow color after 1 h of heating. The color became intensified as the reaction proceeds with the passage of time. As shown in Fig. 1, in comparison with the UV–Vis spectra of gold, silver nitrate and gum solution, a typical surface plasmon resonance band at 550 and 450 nm appeared for Au- and Ag-NPs respectively after 4 h of heating, therefore indicating the successful biosynthesis of gold and silver nanoparticles in the solution. The formation of Au- and Ag-NPs was further confirmed from the color of the corresponding solutions, where the ruby red color indicated the biosynthesis of gold nanoparticles and yellow color for silver nanoparticles. In comparison, silver nitrate and gum solutions appeared colorless while HAuCl4 solution had light yellow color. A change in the size or shape of the nanoparticles results in change of the observed color. Gold spheres have a characteristic red color, while silver spheres are yellow and it has been shown that the color is due to the collective oscillation of the electrons in the conduction band, known as the surface plasmon oscillation. The oscillation frequency is usually in the visible region for gold and silver giving rise to the strong surface plasmon resonance absorption (Eustis and El-Sayed, 2006).

UV–Vis spectra of gold (A) and silver (B) nanoparticles. The inset photographs show the corresponding color of the biosynthesized nanoparticles solutions.
Figure 1
UV–Vis spectra of gold (A) and silver (B) nanoparticles. The inset photographs show the corresponding color of the biosynthesized nanoparticles solutions.

3.2

3.2 FTIR

The FTIR spectra of gum extract and the biosynthesized Au- and Ag-NPs are shown in Fig. 2. The apricot gum has mainly polysaccharide compounds which along with glucuronic acid and its 4-O-methyl ether having O—H, —COOH, hemiacetal and ether groups showed a broad O—H stretching band at 3300 cm−1. A small peak at 2840 cm−1 merged with a broad carboxylic acid peak was due to C—H stretching. A strong peak at 1717 cm−1 was due to C⚌O stretching of —COOH. Similarly, a strong peak at 1600 cm−1 can be attributed to the conjugated C⚌C bond stretching which might be due to the presence of flavonoids and/or carotenoids. Bending vibration of C—H bond was observed at 1417 cm−1 and O—H bending at 1373 cm−1. A strong peak at 1037 cm−1 was due to C—O stretching vibrations. In case of gold nanoparticles, the bonded O—H stretching shifted from 3300 cm−1 to higher frequency of 3311 cm−1, and this shows the involvement of OH groups in the reduction and capping processes. A sharp peak of carbonyl carbon at 1717 cm−1 disappeared completely, thus representing the participation of carboxylic acid group as reducing as well as capping agent. The bending vibrations at 1417, 1373 cm−1 also disappeared due to attraction by the gold nanometal. A shift in C—O acyclic bond stretching from 1037 to 1022 cm−1 can be attributed to attraction by the gold nanometal during the capping process. Almost similar FTIR spectrum was observed for Ag-NPs. Moreover, the small merged peak at 2840 cm−1 can be seen as a separate entity in the FTIR spectra of biosynthesized Au- and Ag-NPs and was attributed to the interaction of carboxylic acid with gold and silver nanoparticles. These results confirmed that O—H, carbonyl and C—O groups not only reduced the Au and Ag metals but also acted as stabilizing agents.

FTIR spectra of gum (A) and its gold (B), and silver (C) nanoparticles.
Figure 2
FTIR spectra of gum (A) and its gold (B), and silver (C) nanoparticles.

3.3

3.3 SEM

The size and shape of Au- and Ag-NPs were determined using a scanning electron microscope (Fig. 3). It was observed from the SEM images that the biosynthesized Au- and Ag-NPs were in the range of 10–40 nm and 5–30 nm respectively. Au- and Ag-NPs were mostly spherical with different sizes but a small number of anisotropic nanostructures such as nanotriangles, a few nanorods, hexagonal and polygonal nanoprisms were also observed. The uniform size distribution of nanoparticles in this study indicated the efficient stabilization of nanoparticles while the large size and/or anisotropic shapes of some nanoparticles might be due to the aggregation of smaller nanoparticles.

SEM images of gold (A) and silver (B) nanoparticles.
Figure 3
SEM images of gold (A) and silver (B) nanoparticles.

3.4

3.4 EDX and XRD

The EDX analysis confirmed the presence of Au and Ag in the samples (Fig. 4). Strong signals were observed from Au atoms in Au-NPs at approximately 0.6 and 2.6 keV while weak signals were observed at 9.7 and 11.6 keV. In the case of Ag-NPs, strong signals were observed at 0.6 and 2.6 keV while a weak signal was observed at 3.7 keV. The appearance of Si signal might be due to the use of silicon grid in the EDX analysis while the signal for N indicated the presence of nitrogen containing organic compounds in the gum. Moreover, other strong signals for C and O were also due to the presence of bio-organic molecules that were involved in capping the Au- and Ag-NPs. The presence of chlorine atom in the EDX spectra of gold nanoparticles was due to the presence of chlorine in tetrachloroauric acid molecule. The signals for K and Mg were due to the X-ray emission from different bio-molecules of the gum. The appearance of elemental Au and Ag in the EDX analysis supported the XRD results, which indicated the reduction of metal cations to elemental form.

EDX spectra of gold (A) and silver (B) nanoparticles.
Figure 4
EDX spectra of gold (A) and silver (B) nanoparticles.

The nature of Au- and Ag-NPs formed in this approach was evaluated with XRD analysis. Fig. 5 shows the XRD profile of the synthesized gum stabilized Au- and Ag-NPs. The XRD peak positions are consistent with the metallic silver. The peaks at 35° or double peak at 45° also depicts the presence of silver oxide in addition to silver (Kuzma et al., 2012) and this might be due to air oxidation of silver ions during Ag-NPs synthesis as the reactions were carried out in open atmosphere. The XRD pattern of Ag-NPs exhibited characteristic peaks at scattering angles (2 Ø) of 38.431, 44.623, 64.531, 77.781 that can be indexed to the (1 1 1), (2 0 0), (2 2 0), (3 1 1) Bragg’s reflections of face centered cubic (FCC) structure of metallic silver similar to the Joint Committee on Powder Diffraction Standards (JCPDS) file no: ICDD-PDF2, revealing that the biosynthesized Ag-NPs were of pure crystalline silver. In the case of gold containing sample, the characteristic diffraction peaks of FCC metallic gold phase (4-0784) at 38.21°, 44.39°, 64.62°, and 77.59° were observed. No peaks similar to other crystalline phases were observed indicating high purity of the products. The diffraction peak at 38° was the only highly intense peak among the observed peaks for both Au- and Ag-NPs. In addition, the ratio between the (2 2 0) and (1 1 1) peaks was quite lower than the standard value (0.1 versus 0.4). The mean particle diameters of Au- and Ag-NPs were calculated from the XRD data which can be derived from the Debye Scherrer equation D = k λ/β½ cos θ. This equation exploits the reference peak width at angle θ, where λ is the X-ray wavelength (1.5418), β½ is the width of the XRD peak at half height and k is the shape factor. Average particle size was around 22 and 20 nm for Au- and Ag-NPs respectively.

XRD patterns of gold (A) and silver (B) nanoparticles.
Figure 5
XRD patterns of gold (A) and silver (B) nanoparticles.

3.5

3.5 Atomic absorption spectroscopy

Atomic absorption analysis was carried out to determine the amount of Au and Ag in pure HAuCl4 and AgNO3 solution and the resultant nanoparticles. In HAuCl4 solution, the concentration of Au was 197 mg/l while in the resultant Au-NPs it was 71 mg/ml. Similarly, it was 107 and 34 mg/ml in AgNO3 solution and silver nanoparticles respectively. The decrease in the concentration of Au and Ag in the nanoparticles might be due to the dilution effect and was due to the addition of gum solution to Au and Ag ions solution during the biosynthesis of nanoparticles. These results confirmed the formation of Au- and Ag-NPs bioreduced with apricot gum.

3.6

3.6 TGA

For a comparative study of thermal stability, equal amounts (7.5 mg) of gum and nanoparticles were heated in alumina crucibles and the TGA profiles were recorded from 50–800 °C, at a scan rate of 10 °C/min, under nitrogen atmosphere. Within the same temperature range, different weight loss was observed for gum and biosynthesized nanoparticles. Three successive weight losses were observed for gum and nanoparticles in the temperature range of 50–800 °C (Fig. 6). The first observed weight loss was attributed to the loss of entrapped water molecules from the polymer matrix. The second observed weight loss could be due to the thermal degradation of the polymer as well as the polymer capping around the nanoparticles (Kasthuri et al., 2009). While, the third weight loss might be due to the conversion of remaining polymer to carbon residue. The observed thermal degradation pattern for the gum is in best agreement with the earlier studies (Naidu et al., 2009; Vinod et al., 2010). These findings indicated that the gum stabilized Au- and Ag-NPs were thermally more stable than the gum alone.

TGA spectra of gold (A) and silver (B) nanoparticles.
Figure 6
TGA spectra of gold (A) and silver (B) nanoparticles.

3.7

3.7 Effect of gum concentration on the synthesis of Au- and Ag-NPs

As shown in Fig. 7, the UV–visible spectra revealed an increase in the absorbance at 555 and 450 nm with an increase in gum concentration, therefore showing an enhancement in the concentration of nanoparticles. However, the characteristic SPR peak at 555 and 450 nm showed a red shift, which might be due to an increase in the particle size and this is in agreement with the earlier studies (Kumar et al., 2005). Moreover, the UV–Vis spectra were broader at lower and higher gum concentrations. It can be argued that the broad peaks at lower gum concentration were due to insufficient protection of the nanoparticles, while at high gum concentration, the increase in intermolecular force of gum molecules possibly hinders the dispersion of nanoparticles (Wu and Chen, 2010). Furthermore, with an increasing gum concentration (0.1–0.5%), the color of solution also intensified from ruby red to dark red and light yellow to dark yellow, therefore showing an increase in the concentration of Au- and Ag-NPs respectively.

UV–Vis spectra showing the effect of gum concentration on the synthesis of gold (A) and silver (B) nanoparticles.
Figure 7
UV–Vis spectra showing the effect of gum concentration on the synthesis of gold (A) and silver (B) nanoparticles.

3.8

3.8 Effect of gold or silver ions concentration on the synthesis of Au- and Ag-NPs

As shown in Fig. 8, with an increase in the concentration of Au or Ag ions, the intensities of SPR peaks at 555 and 450 nm increase with a slight red shift, and this is in agreement with the earlier reports (Yu et al., 2004). The increase in the intensities of SPR peaks might be due to an enhancement in the nuclei formation that resulted in the synthesis of larger number of nanoparticles. On the other hand, the shift in the position of SPR peaks might be due to an increase in the particle size as a result of high collision frequency among the metal atoms or nuclei. When Au or Ag ions concentration was 5 mM, quite larger particle size and size distributions were observed. This might be due to the less protective effect by gum and could account for the longitudinal plasmon around 558 and 455 nm for Au- and Ag-NPs respectively.

UV–Vis spectra showing the effect of gold and silver ions concentration on the synthesis of gold (A) and silver (B) nanoparticles.
Figure 8
UV–Vis spectra showing the effect of gold and silver ions concentration on the synthesis of gold (A) and silver (B) nanoparticles.

3.9

3.9 Effect of reaction temperature on the synthesis of Au- and Ag-NPs

Reaction temperature is one of the most important factors that can affect nanoparticles synthesis (Song and Kim, 2009). The effect of different temperatures (20, 40, 60, 80 °C) on the synthesis of nanoparticles was studied and it was observed that the intensity of the UV–Vis spectra increased linearly without any shift in the position of SPR peaks, therefore indicating an increase in the concentration of nanoparticles having similar sizes. The maximum intensity of the characteristic absorption bands was noted at 80 °C and was indicative of optimum temperature for the synthesis of maximum concentration of nanoparticles in the solution (Fig. 9).

UV–Vis spectra showing the effect of reaction temperature on the synthesis of gold (A) and silver (B) nanoparticles.
Figure 9
UV–Vis spectra showing the effect of reaction temperature on the synthesis of gold (A) and silver (B) nanoparticles.

3.10

3.10 Effect of reaction time on the synthesis of Au- and Ag-NPs

The effect of reaction time on the biosynthesis of nanoparticles was evaluated and an increased reduction capacity of gum was observed with reaction time. The SPR occurred at 555 and 450 nm and the intensity of the absorption peaks increased linearly, without any shift in their wavelength with time respectively for Au- and Ag-NPs. This might be due to the continuous reduction of metal ions, leading to an increase number of nanoparticles. No change in the intensity of the SPR peaks was observed after 5 h for Au-NPs and 4 h for Ag-NPs, therefore indicating the completion of the reactions (Fig. 10).

UV–Vis spectra showing the effect of reaction time on the synthesis of gold (A) and silver (B) nanoparticles.
Figure 10
UV–Vis spectra showing the effect of reaction time on the synthesis of gold (A) and silver (B) nanoparticles.

3.11

3.11 Effect of NaCl on the biosynthesized Au- and Ag-NPs

The stability of Au- and Ag-NPs was checked against different concentrations of NaCl solutions, that is, 1, 2 and 3 M. The salt solutions were added to colloidal solutions of Au- and Ag-NPs but no obvious color change was observed. In the UV–Vis absorption spectra, no changes were observed in the position of SPR with varying concentration of the salt solution; however, a decrease in the intensity of the SPR peaks was observed with an increase in salt concentration compared to the salt free nanoparticles solutions as shown in Fig. 11. The stability of nanoparticles in solution is mainly dependent on the surface properties of nanoparticles such as surface charge and ligand structure. Generally, an increase in the electrostatic repulsion and steric hindrance of nanoparticles surfaces can significantly improve the stability of nanoparticles in solution. In this case, a slight decrease in the surface charge of nanoparticles was observed with an increase in the electrolyte concentration (NaCl), that led to aggregation of nanoparticles and this might be due to reduction in the electrostatic repulsion of nanoparticles. The biological activity of nanoparticles depends on many physico-chemical factors and is regulated by their stability, with a reduction in stability results in aggregation and consequently leads to total or partial loss of nanoscale properties (Liu et al., 2011).

UV–Vis spectra showing the effect of different NaCl concentrations on the biosynthesized gold (A) and silver (B) nanoparticles.
Figure 11
UV–Vis spectra showing the effect of different NaCl concentrations on the biosynthesized gold (A) and silver (B) nanoparticles.

3.12

3.12 Effect of pH on the biosynthesized Au- and Ag-NPs

The effect of varying pH on the stability of biosynthesized Au- and Ag-NPs was studied. Optimized samples of Au- and Ag-NPs were slightly acidic having a pH value of 6–7 and showed maximum absorption in their UV–Vis spectra (Fig. 12). It was observed that the gold nanoparticles were stable in acidic medium as there was a less significant change in their UV–Vis absorption spectra. However, in basic medium, the nanoparticles were unstable as significant peak broadening was observed in their UV–Vis spectra. The UV–Vis absorption spectra of nanoparticles were significantly dependent on their sizes. It was reported that the aggregation of nanoparticles led to peak broadening and a dramatic red shift in the absorption spectra which depends on the distance between nanoparticles, the density of the assembly and the size of the particles (Storhoff et al., 2000; Schöne et al., 2015). Thus, at basic pH, the Au- and Ag-NPs exhibited aggregation, which increased their particle size and therefore peak broadening was observed in their respective UV–Vis absorption spectra. The extreme alkaline pH induced nanoparticles aggregation was further confirmed from the SEM images (Fig. 13). pH plays an important role not only in the formation of stable nanoparticles but also in the stabilization of redispersed nanoparticles (Das et al., 2015). Solution pH affects the dissociation equilibrium of a complexing agent, the protonation or hydroxylation of the ionic groups released by nanoparticles dissolution, and nanoparticles interfacial free energy (Zhang et al., 2010).

UV–Vis spectra showing the effect of different pH on the biosynthesized gold (A) and silver (B) nanoparticles.
Figure 12
UV–Vis spectra showing the effect of different pH on the biosynthesized gold (A) and silver (B) nanoparticles.
SEM images showing the effect of acidic (2–3), neutral (6–7) and basic (12–13) pH on the biosynthesized gold and silver nanoparticles.
Figure 13
SEM images showing the effect of acidic (2–3), neutral (6–7) and basic (12–13) pH on the biosynthesized gold and silver nanoparticles.

3.13

3.13 Effect of long term storage on the biosynthesized Au- and Ag-NPs

The effect of long term storage on the biosynthesized Au- and Ag-NPs was studied by keeping the samples at room temperature for eight months. No change in the color and visual aggregation was observed during the entire storage duration. Moreover, no significant change was observed in the position of SPR peak of the UV–Vis spectra as shown in Fig. 14. Thus the biosynthesized Au- and Ag-NPs were highly stable and well dispersed for prolonged period, without undergoing any degradable changes. In order for the nanoparticles to be useful in biomedicine, they must satisfy certain criteria which include among other factors, their long term stability under physiological conditions (Thanh and Green, 2010). The stability of nanoparticles in environment plays an important role in determining their mobility, bioavailability and toxicity (Kim et al., 2012).

UV–Vis spectra showing the effect of long term storage on the biosynthesized gold (A) and silver (B) nanoparticles.
Figure 14
UV–Vis spectra showing the effect of long term storage on the biosynthesized gold (A) and silver (B) nanoparticles.

3.14

3.14 Effect of high temperature on the biosynthesized Au- and Ag-NPs

The biosynthesized Au- and Ag-NPs were subjected to extreme of temperature by heating at 100 °C for 30 min, and it was observed that they were quite stable as no significant change was observed in their position of SPR peaks (Fig. 15). This high stability of Au- and Ag-NPs might be attributed to the protective effect of gum on the surface of nanoparticles. Temperature is one of the important environmental factors that influence the stability, activity and chemical characteristics of materials (Liu et al., 2011). Nanocoating of active components is effective in protecting the active therapeutic moiety from oxidative, hydrolytic and environmental degradation processes and hence enhances its shelf-life (Thakur et al., 2011).

UV–Vis spectra showing the effect of high temperature (100 °C) on the biosynthesized gold (A) and silver (B) nanoparticles.
Figure 15
UV–Vis spectra showing the effect of high temperature (100 °C) on the biosynthesized gold (A) and silver (B) nanoparticles.

3.15

3.15 Antibacterial activity

Au- and Ag-NPs were evaluated for antibacterial activity using the disk diffusion method against S. aureus, E. coli and P. aeruginosa. Growth suppression was observed in plates loaded with Au- and Ag-NPs, while the negative control plates with autoclaved gum were devoid of any zone of inhibition. The positive control plates loaded with the standard streptomycin antibiotic disks produced greater inhibition zones. The zones of inhibition for Au-NPs measuring 10 ± 0.3 mm, 9 ± 0.5 mm and 7.9 ± 0.3 mm were recorded, while that for the Ag-NPs were 18 ± 0.5 mm, 10.2 ± 0.8 mm, 11.2 ± 0.3 mm against the bacterial strains of S. aureus, E. coli and P. aeruginosa respectively (Table 1).

Table 1 Antibacterial activity of the biosynthesized gold and silver nanoparticles (zone of inhibition in millimeter).
Sample Staphylococcus aureus Escherichia coli Pseudomonas aeruginosa
Prunus armeniaca gum NA NA NA
Au-NPs 10 ± 0.3 9 ± 0.5 7.9 ± 0.3
Ag-NPs 18 ± 0.5 10.2 ± 0.8 11.2 ± 0.3
DMSO NA NA NA
Streptomycin 22.5 ± 0.5 20.2 ± 0.3 15 ± 0.5

Values are expressed as mean ± SEM of three separate experiments. NA = Not active.

As no antibacterial activity was observed for the gum extract, it can be argued that the bactericidal activity might be due to the synergistic activity of gum stabilized Au- and Ag-NPs and unreduced Au (III) or Ag+ ions. A greater zone of inhibition was observed against gram positive bacteria; S. aureus as compared to gram negative strains, E. coli and P. aeruginosa, and this is in agreement with the earlier studies (Kora et al., 2010; Suresh et al., 2010). Nanoparticles have emerged as novel antimicrobial agents and several classes of antimicrobial nanoparticles and nanosized carriers for antibiotics delivery have proven their effectiveness for treating infectious diseases. Nanoparticles disrupt the integrity of the bacterial membrane and trigger the induction of oxidative stress by free radical formation (Hajipour et al., 2012). Gold nanoparticles are valuable in the development of antibacterial agents as they are biocompatible than the other nanometals and can be engineered to possess chemical or photothermal functionality (Ravishankar Rai and Jamuna Bai, 2011; Dizaj et al., 2014). Silver nanoparticles are the most popular inorganic nano-materials used as antimicrobial agents. Silver nanoparticles show a high antimicrobial activity comparable with its ionic form and have demonstrated potential antibacterial effect against drug resistant bacteria (Allahverdiyev et al., 2011; Prabhu and Poulose, 2012; Dizaj et al., 2014). Development of simple and low cost inorganic antimicrobial agents such as metal and metal oxide nanoparticles as alternative of traditional antibiotics might be promising for future of pharmaceuticals and medicine (Dizaj et al., 2014).

3.16

3.16 Antinociceptive activity

As shown in Fig. 16, significant antinociceptive effect (P < 0.001) was produced by the gum extract at doses of 200 and 400 mg/kg. Similarly, the Au-NPs significantly relieved the acetic acid induced nociception at doses of 40 mg/kg (P < 0.01) and 80 mg/kg (P < 0.001). The antinociceptive effect of both the extract and its Au-NPs was comparable to that of standard diclofenac sodium which significantly decreased (P < 0.001) the acetic acid induced writhes at 50 mg/kg.

Antinociceptive activity of the biosynthesized gold and silver nanoparticles in the acetic acid induced abdominal constriction assay. One way ANOVA followed by Dunnett’s post hoc test. ⁎⁎P < 0.01, ⁎⁎⁎P < 0.001. n = 6.
Figure 16
Antinociceptive activity of the biosynthesized gold and silver nanoparticles in the acetic acid induced abdominal constriction assay. One way ANOVA followed by Dunnett’s post hoc test. ⁎⁎P < 0.01, ⁎⁎⁎P < 0.001. n = 6.

The nociceptive response in the acetic acid induced writhing test results from the action of cyclooxygenase-1 (COX-1) and COX-2 enzymes that produce prostaglandins which stimulate the sensory pathways in the mouse peritoneum and incite a viscero-somatic reflex manifested as strong abdominal constrictions (Matsumoto et al., 1998; Mazario et al., 2001). The acetic acid induced writhing method is sensitive to analgesics (Bentley et al., 1981) and sensory afferents in the peritoneum that carry various receptors on their terminals (Bentley et al., 1983) are activated by appropriate agonists and therefore depress the generation of pain impulses (Gray et al., 1998, 1999). The antinociceptive activity of P. armeniaca has been shown to be attributed to the presence of amygdalin which significantly reduced the formalin-induced tonic pain in both early (the initial 10 min after formalin injection) and late phases (10–30 min following the initial formalin injection). It also inhibited c-Fos expression in the spinal cord and the gene expression of TNF-α and IL-1b in the skin of the hind paw induced by formalin injection (Hwang et al., 2008).

In this study, a dose dependent antinociceptive activity was observed for the gum extract and its Au-NPs; however, the antinociceptive doses employed for the Au-NPs (40 and 80 mg/kg) were much lower than that of the gum extract (200 and 400 mg/kg). The lower doses of Au-NPs significantly reduced the tonic chemical induced nociception and the effect is analogous to that of the standard, diclofenac sodium. Acute and chronic pain conditions affect a significant portion of society. Individuals suffering from chronic pain experience a host of pain-related problems, including diminished functionality, increased psychological co-morbidities, sleep disturbances, and an overall decrease in their quality of life. Nanomedicine offers the potential for development of novel technologies, drugs and drug delivery technologies to address many of the global unmet needs in pain management (Sprintz et al., 2011). Phyto-therapeutics needs a scientific approach in the form of nano drug delivery systems, which not only reduce their repeated administration, but also help to increase their therapeutic value by reducing toxicity and increasing the bioavailability (Ansari and Farha Islam, 2012).

3.17

3.17 Anti-inflammatory activity

As shown in Table 2, carrageenan alone treated animals exhibited significant elevation (P < 0.001) of paw volume at each hour of the study period. The gum extract at the tested doses (200 and 400 mg/kg) significantly reduced the carrageenan induced paw edema. The Au-NPs at doses of 40 and 80 mg/kg produced a less significant (P < 0.01) anti-inflammatory effect at the 1st hour of study; however, a high significant (P < 0.001) protective effect was observed for the next 2–5 h. The standard diclofenac sodium was found to have a robust anti-inflammatory activity (P < 0.001) at 50 mg/kg for the whole 5 h study duration.

Table 2 Anti-inflammatory activity of the biosynthesized gold and silver nanoparticles against carrageenan induced paw edema in mice.
Treatment 1st h 2nd h 3rd h 4th h 5th h
Group 1
Saline		 0.240 ± 0.022 0.244 ± 0.020 0.258 ± 0.017 0.242 ± 0.013 0.254 ± 0.011
Group 2
Carrageenan		 0.344 ± 0.023a 0.368 ± 0.027a 0.376 ± 0.027a 0.400 ± 0.025a 0.432 ± 0.037a
Group 3
Diclofenac (50 mg/kg)		 0.252 ± 0.031⁎⁎⁎ 0.254 ± 0.020⁎⁎⁎ 0.268 ± 0.028⁎⁎⁎ 0.292 ± 0.027⁎⁎⁎ 0.302 ± 0.017⁎⁎⁎
Group 4
(PAG 200 mg/kg)		 0.248 ± 0.025⁎⁎⁎ 0.266 ± 0.020⁎⁎⁎ 0.276 ± 0.011⁎⁎⁎ 0.304 ± 0.023⁎⁎⁎ 0.312 ± 0.022⁎⁎⁎
Group 5
(PAG 400 mg/kg)		 0.254 ± 0.028⁎⁎⁎ 0.258 ± 0.031⁎⁎⁎ 0.270 ± 0.029⁎⁎⁎ 0.300 ± 0.033⁎⁎⁎ 0.306 ± 0.023⁎⁎⁎
Group 6
(Au-NPs 40 mg/kg)		 0.276 ± 0.029⁎⁎ 0.288 ± 0.025⁎⁎⁎ 0.306 ± 0.011⁎⁎⁎ 0.302 ± 0.017⁎⁎⁎ 0.330 ± 0.034⁎⁎⁎
Group 7
(Au-NPs 80 mg/kg)		 0.268 ± 0.028⁎⁎ 0.282 ± 0.025⁎⁎⁎ 0.294 ± 0.011⁎⁎⁎ 0.284 ± 0.026⁎⁎⁎ 0.314 ± 0.028⁎⁎⁎

Values expressed as mean ± SD. One way ANOVA followed by Tukey’s post hoc test. n = 6.

a P < 0.001 compared to group 1.
⁎⁎ P < 0.01.
⁎⁎⁎ P < 0.001 compared to group 2.

Edema formation due to carrageenan administration in mouse paw is a biphasic event. The initial phase lasting about 1–5 h is predominately characterized by a non-phagocytic edema and has been attributed to the action of various mediators including histamine, serotonin and bradykinin on vascular permeability (Maity et al., 1998). The initial phase is followed by a second phase having a duration of 2–5 h and results from overproduction of prostaglandins (Pérez-Guerrero et al., 2001). It has been reported that the second phase of edema is sensitive to drugs like hydrocortisone, phenylbutazone and indomethacin. P. armeniaca exhibit anti-inflammatory properties and have been tested against lipopolysaccharide (LPS)-induced inflammation model on mouse BV2 microglial cells, where the extract suppress the synthesis of prostaglandin E2 and nitric oxide production via inhibiting the LPS-stimulated enhancement of cyclooxygenase-2 and inducible nitric oxide synthase mRNA expression (Chang et al., 2005). The presence of amygdalin in P. armeniaca is effective in alleviating inflammatory pain and can be used as an analgesic with anti-inflammatory and antinociceptive properties (Hwang et al., 2008).

In our study, the gum extract and its Au-NPs produced highly efficient and prolonged reduction of carrageenan induced inflammation in mice paw. The anti-inflammatory effect of Au-NPs was observed at much lower doses (40 and 80 mg/kg) as compared to the gum extract (200 and 400 mg/kg) and the effect was as effective as the standard, diclofenac sodium. Nanoparticles can be used for passive targeting of anti-inflammatory medication that are able to extravagate into interstitial spaces and can be retained at the site of inflammation by enhanced permeability and retention effect (Khaja et al., 2012). Recently, various nanoscale technologies have been used for targeting anti-inflammatory drugs in different inflammatory conditions (Pison et al., 2006; Lobatto et al., 2010, 2011; Crielaard et al., 2012). Nanoparticle-based drug carriers can increase the efficacy and safety of drugs by enhancing capacity, improving solubility, combining multiple drugs, protecting against metabolism, and controlling release. Nanoparticles can also form the basis of multifunctional drug delivery vehicles by combining targeting, imaging, and therapeutic moieties (Szelenyi, 2012).

4

4 Conclusion

The present study reports a green synthesis of Au- and Ag-NPs from tetrachloroauric acid and silver nitrate using the gum extract of P. armeniaca which served the role of self reducing and stabilizing agent and thus the harmful effects associated with the use of synthetic agents can be avoided. The natural availability of gum makes this process most suitable for large scale production. The average diameter of the obtained spherical Au- and Ag-NPs was 20 and 18 nm respectively. There was an enhancement in the overall concentration of nanoparticles with increasing gum and Au/Ag metal ions concentration, reaction temperature and time. The nanoparticles possessed efficient stability under varying concentration of NaCl, neutral to acidic pH and can be stored for prolong time at any temperature up to 80 °C without undergoing any loss in potency. The extremely resistant nature of these nanoparticles shows their potential for formulation into various dosage forms. The nanoparticles produced significant antibacterial effect against both Gram positive and Gram negative bacteria. Moreover, these nanoparticles possessed pain and inflammation relieving properties at much lower doses which show their utility in drug delivery. Knowledge of suitable conditions for the efficient synthesis of stable nanoparticles is important for their potential as candidates for various pharmaceutical and environmental applications.

Acknowledgment

The authors gratefully acknowledge the financial support of the Higher Education Commission of Pakistan.

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