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Table of Contents
Year : 2020  |  Volume : 3  |  Issue : 3  |  Page : 182-188

Studying the effect of silver nanoparticles synthesized by ulva fasciata aqueous extract against liver toxicity induced by CCl4in rats

Department of Biochemistry, Faculty of Science, King Abdulaziz University, Jeddah, Kingdom of Saudi Arabia

Date of Submission01-Jan-2020
Date of Decision22-Feb-2020
Date of Acceptance16-Mar-2020
Date of Web Publication02-Jul-2020

Correspondence Address:
Fawzia A Alshubaily
Department of Biochemistry, Faculty of Science, King Abdulaziz University, Jeddah
Kingdom of Saudi Arabia
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/JNSM.JNSM_2_20

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Background: Researchers in recent years have been increasingly concerned with the production of synthesizing nanoparticles (NPs) applying plant extracts, as these NPs have low environmental risk and low human toxicity. The present study aimed to use Ulva fasciata (UF) as a reducing agent for the green synthesis of silver NPs (AgNPs) and to investigate the hepatoprotective effect of these NPs against CCl4. Methods: In this study, aqueous extract of UF was used for the reduction of silver nitrate. Results: The results revealed a spherical shape of the AgNPs that are well distributed in solution with a size ranging 9–37 nm and an optical absorption at 430 nm. A total of 28 rats used in this study were randomly divided into four groups each of seven animals; control group, UF AgNPs group (150 mg/kg body weight/20 days), CCl4group (2 ml/kg/20 days of 1:1 v/v mixture of CCl4and olive oil), and CCl4and UF-AgNPs group. The results showed that CCl4injection increases in liver function enzymes, level of urea and creatinine, hepatic oxidative stress (a significant increase in lipid peroxidation with a significant decrease in glutathione and antioxidant enzyme activities), and histopathological disorders of liver tissues as compared to control group. Rats received CCl4with UF- AgNPs showed significantly less severe damage and a remarkable improvement in the measured parameters when compared to CCl4rats. Conclusion: It is concluded that the aqueous extract UF can be used as an effective and eco-friendly reducing agent for the biosynthesis of AgNPs. Furthermore, AgNPs capped with UF can be used as a potent antioxidant and a hepatoprotective agent against the biochemical and histopathological alterations induced by CCl4toxicity in the liver tissues.

Keywords: CCl4toxicity, green synthesis, silver nanoparticles, Ulva fasciata

How to cite this article:
Alshubaily FA, Jambi EJ, Khojah SM, Balgoon MJ, Al-Zahrani MH, Alkhattabi NA. Studying the effect of silver nanoparticles synthesized by ulva fasciata aqueous extract against liver toxicity induced by CCl4in rats. J Nat Sci Med 2020;3:182-8

How to cite this URL:
Alshubaily FA, Jambi EJ, Khojah SM, Balgoon MJ, Al-Zahrani MH, Alkhattabi NA. Studying the effect of silver nanoparticles synthesized by ulva fasciata aqueous extract against liver toxicity induced by CCl4in rats. J Nat Sci Med [serial online] 2020 [cited 2022 Aug 12];3:182-8. Available from: https://www.jnsmonline.org/text.asp?2020/3/3/182/288823

  Introduction Top

The green biosynthesis of nanoparticles (NPs) employing either biological microorganism or plant extracts has emerged as a simple cost-effective and environment-friendly method.[1],[2],[3] This process is scaled up for large-scale synthesis alternative to more complex chemical synthetic procedures to obtain nanomaterials. Furthermore, there is no need to use high pressure, energy, temperature, and toxic chemicals during the green biosynthesis of NPs.[4] Different types of metals can be used for the production of NPs with a dimension <100 nm including gold, silver, copper, and zinc, silver NPs (AgNPs) have attracted great attention due to their specialized magnetic, electrical, and optical properties. AgNPs can be considered as powerful antibacterial, antifungal, and antioxidant agents [4] and have a wide range of applications in different fields such as agriculture, medicine, and industry.[5]

Green biosynthesis of AgNPs by algal extract is more advantageous than other biological processes due to rapid growth rates of algae, high biomass production in a short time, cost-effective, eco-safe, and helpful for human therapeutic use.[6]Ulvafasciata (UF) (sea lettuce) is one of the green seaweeds that composed of highly active contents that have antitumor, antioxidant, hypocholesterolemic, and antimicrobial potentials.[7] The antioxidant activity of UF could be arising from bioactive compounds, such as carotenoids, tocopherols, and polyphenols that can directly or indirectly induce inhibition or suppression of free radical generation.[6] In addition, these green algae can be used as an effective and eco-friendly reducing agent for the synthesis of AgNPs.[6]

Treatment of liver disorders by the usage of synthetic drugs could be associated with risk of relapses and danger of side effects. Therefore, natural products can be used as an effective, safe, and alternative therapy for the treatment of liver diseases without any side effects.[8] CCl4 is one of the toxic agents that can be used to induce liver damage and can be used for the evaluation of hepatoprotective agents. Trichloromethyl free radicals formed during CCl4 metabolism can lead to oxidative damage by reacting with biological substances, such as fatty acids, proteins, and nucleic acids.[9] Thus, this article aimed to use UF as a reducing agent for the biosynthesis of AgNPs and investigation of their hepatoprotective effect against CCl4.

  Materials and Methods Top

Chemicals and reagents were purchased from Sigma Chemical Co. (St. Louis, MO, USA).

Collection and preparation of Ulva fasciata

The algal sample [Figure 1] was manually collected from shallow water besides the shore of Abu-Qur coast Alexandria, Egypt, and was identified according to Aleem [10] and Coppejans et al.[11] Samples were immediately brought to the laboratory in new plastic bags containing seawater, washed thoroughly with tap water, and filtered seawater to remove extraneous materials. Algal material was shade-dried for 5 days and oven-dried at 60°C until constant weight was obtained, then was ground into fine powder using electric mixer, and stored at 0°C [6] for future use.
Figure 1: Ulva fasciata

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Preparation of Ulva fasciata aqueous extracts

One gram of dry powder UF was added to 100 mL distilled deionized water, boiled for 1 h, and then filtrated.

Biosynthesis of silver nanoparticles

AgNPs were prepared by the reduction of Ag + ions to Ag 0 according to the methods of Devi and Bhimba.[12] 10 mL of UF aqueous extract was added slowly to 90 mL of freshly prepared 0.1 mM of silver nitrate (AgNO3) with stirring and heating at 40°C until reduction of silver ions (Ag +) and changing the color were observed. Bio-reduction of Ag + ions in the aqueous extracts and the formation of AgNPs were monitored using spectroscopic analysis at 300–700 nm.[6] Morphological analysis of the size, shape, and the AgNPs state was monitored using transmission electron microscopic (TEM) analysis. A drop of aqueous AgNPs sample was loaded on carbon-coated copper grid and allowed to dry completely for an hour at room temperature. The clear microscopic views were observed and documented in different ranges of magnifications as in [Figure 2], showing the summarized steps.
Figure 2: Steps for the preparation of Ulva fasciata aqueous extracts and biosynthesis of silver nanoparticles

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Biochemical study


The experiment was conducted on 28 male albino rats (12 ± 2 weeks old; 170 ± 20 g body weight [b.wt]). Rats were acclimated to controlled laboratory conditions for 2 weeks. The chosen animals were housed in plastic cages with good aerated covers at normal atmospheric temperature (25°C ± 5°C) as well as 12 h daily normal light periods. Moreover, they were maintained on stock rodent diet and tap water that were allowed adlibitum. This study was carried out in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health (NIH publication No. 85-23, 1996). The protocol was approved by the Committee on the Ethics of Animal Experiments of King Fahd Medical Research Center. All surgery was performed under diethyl ether anesthesia, and all efforts were made to minimize suffering.

Experimental design

Animals (28 rats) were randomly divided into four groups, each of seven rats as follows:

Control group: Rats fed on a balanced diet containing 2% olive oil for 20 days. UF-AgNPs group: Rats were administrated daily by NPs UF aqueous extract by gastric intubation at dose level of 150 mg/kg b.wt.[6] CCl4 group: Rats were treated daily with hepatotoxic agent CCl4(CCl4 was solved in olive oil with the ratio of 1:1 v/v and was injected to rats intraperitoneally at dose 2 ml/kg)[13] for 20 days. CCl4 and UF-AgNPs: Rats received UF-AgNPs (150 mg/kg b.wt/day) along with intraperitoneal injection of CCl4 (2 ml/kg of 1:1 v/v mixture of CCl4 and olive oil) for 20 days as in [Table 1].
Table 1: Animal groups as divided and used in the study with planned treatments for 20 days

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By the end of the experimental periods, animals from each group were sacrificed 24 h after the last dose of treatment. Blood samples were collected through heart puncture and centrifuged to obtain serum for biochemical analysis. In addition, liver tissue was removed for biochemical investigation and histological examination.

Biochemical analysis

The activity of serum aspartate transaminase (AST), alanine transaminase (ALT), gamma-glutamyl transferase (GGT), urea, and serum creatinine was measured according to previously documented methods.[14],[15],[16],[17] Liver was dissected, thoroughly washed with ice-cold 0.9% NaCl, weighed, minced, and homogenized (10% w/v) using 66 mmol/L chilled phosphate buffer (pH 7.0). The tissue homogenates were centrifuged at 6000 rpm for 15 min, and the supernatants were used to estimate the level of malondialdehyde (MDA), xanthine oxidase (XO), xanthine dehydrogenase (XDH), glutathione content (GSH), superoxide dismutase (SOD), and catalase (CAT).[18],[19],[20],[21],[22],[23]

Histopathological examination

For histopathological study, the tissue samples were taken rapidly from each rat and fixed in 10% formalin. All the samples were dehydrated in ascending grades of ethanol, cleared in butanol, and embedded in parablast. Sections of 5–6 μm thick sections were obtained and stained with the following stains:

  1. Hematoxylin and eosin staining for general histological studies
  2. Masson's trichrome stain for collagen fibers.

Statistical analysis

Results were presented as mean ± standard error (n = 7). Experimental data were analyzed using one-way analysis of variance. Duncan's multiple range test was used to determine the significant differences between means. Statistical analyses were performed using computer program Statistical Package for the Social Sciences (version 22; Chicago, IL, USA).[22]

Differences between means were considered significant at P < 0.05.

  Results Top

The bio-reduction of Ag+ ions was visually confirmed by changing the color of reaction mixture from colorless to brownish-yellow after 3 min of reaction. The brown color increased by increasing the incubation period [Figure 3].
Figure 3: Changing the color of reaction mixture after adding Ulva fasciata aqueous extracts to silver nitrate (colorless)

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Ultraviolet-visible spectroscopy analysis

The bio-synthesis of AgNPs was confirmed by ultraviolet (UV)-visible spectrophotometer analysis. The results obtained that the absorption spectrum of reaction mixture at different wavelengths ranging between 400 and 500 nm revealed a peak at 430 nm [Figure 4].
Figure 4: Ultraviolet-visible spectra showing absorbance for silver nanoparticle synthesized using Ulva fasciata

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Transmission electron microscope

The result of TEM analysis of AgNPs [Figure 5] showed that UF aqueous extract strongly affected the size and shape of the AgNPs. In addition, the results revealed that AgNPs bio-synthesized by UF have spherical shape and well distributed in solution, and the range of particles size is 9–37 nm.
Figure 5: Transmission electron microscopic image of silver nanoparticles biosynthesized (9–37 nm) by the reduction of silver nitrate ions using Ulva fasciata aqueous extract

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Results of biological study

The results revealed that CCl4-administered rats showed a significant elevation of liver enzyme activity markers: AST, ALT, and GGT as compared to the control, whereas treatment of rats with UF-AgNPs and CCl4 resulted in a significant reduction in those markers compared to CCl4 rats [Table 2].
Table 2: Effect of Ulva fasciata-silver nanoparticles on liver enzymes of rats intoxicated with carbon tetrachloride

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The data in [Table 3] indicate that the serum levels of urea and creatinine were significantly increased in the CCl4-treated rats as compared to the control. Treatment of CCl4-administered rats with UF-AgNPs showed significantly decreased levels of serum urea and creatinine as compared to the CCl4-injected rats [Table 3].
Table 3: Effect of Ulva fasciata.silver nanoparticles on kidney function of rats intoxicated with carbon tetrachloride

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CCl4 intoxication resulted in significant increases in MDA and XO and decreases in GSH level and the activity of XDH, SOD, and CAT of hepatic tissues compared to control rats. Treatment of CCl4-intoxicated rats with UF- AgNPs resulted in significant reduction of MDA and XO activity with remarkable elevation in GSH level and antioxidant enzymes relative to CCl4 group [Table 4].
Table 4: Effect of Ulva fasciata-silver nanoparticles on antioxidant status of rats intoxicated with carbon tetrachloride

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Histopathological examination

Histopathological examination of liver tissues revealed that control rats have normal liver architecture with central vein, and cytoplasm and prominent nucleus and nucleolus were preserved [Figure 6]a. The same observation was observed when the experimental animals were treated by UF-AgNPs [Figure 6]b. However, the liver tissues of CCl4-intoxicated rats were characterized by inflammatory cell collection, scattered inflammation across liver parenchyma, focal necrosis, and swelling up of vascular endothelial cells [Figure 6]c. In CCl4-treated rats with UF-AgNPs, the CCl4 toxicity appeared to be significantly prevented as revealed by the preserved cytoplasm of the hepatic cells. This also caused a marked decrease in the number of inflammatory cells [Figure 6]d.
Figure 6: Histological structure of a rat liver (H and E, ×100). (a) Control rats with normal liver lobular architecture, well brought out central vein and prominent nucleus and nucleolus; (b) rat treated with Ulva fasciata-silver nanoparticles showing the normal appearance

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  Discussion Top

The green alga UF is composed of important nutritional components with high therapeutic value. It can be used for biosynthesis of AgNPs.[24],[25] The results indicated that the color change of the reaction mixture from colorless to brownish-yellow was noticed obviously after 3 min of reaction and the intensity of brown color increased by the time. The formation of brown color can be considered as a sign of reduction of Ag+ to AgNPs by UF aqueous extract.[26],[27] Sajidha Parveen and Lakshmi [28] concluded that the reduction time of AgNO3 by red algae (Amphiroa fragilissima) was visually evident from the color change (brownish yellow) of reaction mixtures within 20 min. It has been reported that the appearances of brown color in the reaction may be due to excitation of surface plasmon resonance (SPR) and reduction of AgNO3.[26],[29]

UV-visible spectrophotometer analysis recorded that the SPR of AgNPs bio-synthesized by UF aqueous extract produced a maximum peak at 430 nm. A study had reported that the UV-visible spectroscopy of AgNPs from Murraya koenigii, Zea mays, and phycoerythrin produced an absorption peak at 420–440 nm and thus confirmed the formation of NPs.[30] Other studies concluded and that the frequency and width of the SPR depend on the size and shape of the metal NPs as well as on the dielectric constant of the metal itself and the surrounding medium.[31],[32],[33]

Our results of TEM showed that the micrograph of AgNPs by UF aqueous extract has spherical shaped, well distribution in solution with particles size ranged from 9 to 37 nm. It has been suggested that the formation, shape, size, and distribution of NPs depends on physiochemical properties, such as temperature, time, pH, optical, and concentration of the substrate.[34],[35],[36] The studies done by Abirami and Kowsalya,[37] Rajesh et al.,[38] and Owaid [39] found that the AgNPs synthesis by UF has spherical shape and an average size ranging from 28 to 41 nm. Sangeetha and Saravanan [40] and Hamouda et al.[41] reported that the average size of AgNPs synthesized by Ulvalactuca was 20 nm and spherical in shape. The bioactive constituents of UF can act as both reducing and capping agents that form stable and shape-controlled AgNPs in the solution.[6],[42],[43]

This study revealed that the injection of rats with CCl4 resulted in severe liver damage associated with elevation of the serum activity of ALT, AST, GGT, and levels of serum urea and creatinine when compared to the normal group. Toxicity of CCL4 induces change of transition function of liver cells and increase membrane permeability which leads to the leakage of liver enzymes into extracellular space.[9],[44],[45],[46] Studies done by Khan and Siddique [13],[47] and Elsawy et al.[48] showed that elevation in the plasma levels of urea and creatinine induced by CCl4 can be attributed to the damage of nephron structural integrity.

The present investigation demonstrated that CCl4 toxicity induced a significant elevation in the levels of MDA and XO and a significant reduction in GSH level and the activity of XDH, SOD, and CAT of hepatic tissues compared to control rats. CCl4 affects the cytochrome P450 in the liver tissues and produces trichloromethyl radicals that can react with polysaturated fatty acids and leads to the formation of lipid peroxides.[49],[50],[51],[52],[53] In addition, overformation of these radicals disrupts the balance between ROS production and antioxidant defense system associated with the disruption of cellular functions through some events and causes liver damage and necrosis.[13],[54],[55]

Our results indicated that the AgNPs capped with UF may protect against CCl4-induced toxicity in rats by decreasing the activity of liver enzymes (ALT, AST, and GGT), level of urea and creatinine, by reducing level of hepatic MDA and XO activity, and by increasing the GSH level and the activity of XDH, SOD, and CAT compared to CCl4-injected rats. The effect of AgNPs on liver enzymes could be related to the fact that AgNPs have affinity for thiol (-SH) group within the protein molecule causing change in the functional state of proteins and inactivate amino transaminases.[49],[56],[57] The hepatoprotective activity of UF-AgNPs could be attributed to active components of UF aqueous extract such as carotenoids, tocopherols, and polyphenols that have free radical scavenging activity [6] and can protect the liver cells from damage induced by CCl4. Rizk et al.[56] concluded that sulfated polysaccharides of UF can be regarded as potential anti-peroxidative, atheroprotective, hypolipidemic, and antiatherogenic agents and may be used in the protection of ROS-induced oxidative damage, hyperlipidemia, and atherosclerotic complications. In addition, the authors reported that UF polysaccharides alleviate the oxidative stress by its inhibitory effect of lipid peroxidation by reducing the formation of MDA and enhance the antioxidant defense via increasing GSH retention.[56]

  Conclusion Top

Through the results of our study, it has been confirmed that the aqueous extract of UF can be used as an effective and eco-friendly reducing agent for AgNO3 and producing AgNPs with high stability, spherical shape, well distribution in solution, size range between 9 and 37 nm, and absorption peak at 400–500 nm in the UV-visible spectrum. Furthermore, the results concluded that AgNPs capped with UF can be used as a potent antioxidant and a hepatoprotective agent that can significantly attenuate the histopathological alterations induced by CCl4 toxicity in the liver tissues.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

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  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]

  [Table 1], [Table 2], [Table 3], [Table 4]


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