Indian Journal of Animal Research

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Indian Journal of Animal Research, volume 58 issue 3 (march 2024) : 470-477

Effect of a Combination of Citric Acid and Selenium Nanoparticles on Male Rats Nephrotoxicity Caused by Carbon Tetrachloride

Jameel Al-Tamimi1,*, Hossam Ebaid1, Iftekhar Hassan1, Mohamed Habila2, Nawal M. Al Malahi1, Ibrahim M. Alhazza1
1Department of Zoology, College of Science, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia.
2Department of Chemistry, College of Science, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia.
Cite article:- Al-Tamimi Jameel, Ebaid Hossam, Hassan Iftekhar, Habila Mohamed, Malahi Al M. Nawal, Alhazza M. Ibrahim (2024). Effect of a Combination of Citric Acid and Selenium Nanoparticles on Male Rats Nephrotoxicity Caused by Carbon Tetrachloride . Indian Journal of Animal Research. 58(3): 470-477. doi: 10.18805/IJAR.BF-1706.

ABSTRACT

Background: To investigate the therapeutic effects of a combination of citric acid and Se-NPs against carbon tetrachloride (CCl4)-induced renal damage in rats. 

Methods: Twenty-four rats were divided into three groups (n=8 each). Group 1 (control) received the vehicle, while Group 2 received a single dose of 1 ml/kg CCl4 in liquid paraffin (1:1 volume) via intraperitoneal injection. Group 3 was administered a single dose of 1 ml/kg CCl4 in liquid paraffin and then treated twice a week for three weeks with a dose of 2.5 mg/kg Se-NPs. One-way ANOVA and Tukey’s method were used to compare the overall effects of each treatment.

Result: CCL4 elevated MDA levels and decreased GSH levels in group 2 animals compared with those in the control group. Se-NPs significantly restored the oxidative stability in group 3. We found that CCL4 significantly increased its effect on renal function, whereas Se-NPs restored the renal structure affected by CCL4. As a result, Se-NPs can potentially reduce the markers of renal injury caused by CCl4, while also restoring oxidative stability and renal structure and function.

INTRODUCTION

Globally, kidney disease or complications increase the risk of death to people with cardiovascular disease, diabetes, hypertension, age and obesity (Koye et al., 2018). The prevalence of such renal disease ranges between 8% and 16% in patients with the mentioned diseases. Cellular damage may be caused by exposure to various organic molecules, including environmental contaminants and medications (Haghi et al., 2014) that contribute to kidney diseases and nephrotoxicity (Bibu et al., 2011; Sales and Foresto, 2020). Suppose the disease-induced, toxicant or drug-mediated nephrotoxicity is not addressed timely with adequate treatment. In that case, it can lead to severe health compromise, single or multiple organ failure, cancer and even death. Carbon tetrachloride (CCl4) is an intensively researched chemical toxicant and environmental pollutant to study hepatotoxicity and nephrotoxicity in vivo (Baig and Khan, 2023). CCl4 is commonly used as an organic solvent in dry cleaning, production of chloroform, aerosol propellant, fabric-spotting fluid, fire extinguisher fluid and refrigerating agent. However, during its usage in various forms, the compound has been established as a strong hepatoxicant and nephrotoxicant along with suspected carcinogen  (Cohen et al., 2023). Therefore, many investigators are working in this field of research to investigate in regulating its exposure to mankind and environment by administration of herbal active compound or drug (Ahmed et al., 2020; Alhazza et al., 2022; Alhazza et al., 2020; Alhazza et al., 2023; Ebaid et al., 2021; Ebaid et al., 2020; Hassan et al., 2019).
       
The use of nanotechnology for drug delivery may lead to the development of new types of medicines (Sahu et al., 2021). Drug delivery is significantly affected by several biomolecules acting together. Extensive dataset analysis, interpretation methodologies and dataset applications for nanomaterials have improved and facilitated their use in health and environment sectors (Dixit et al., 2022). Selenium nanoparticles (SeNPs) are extensively studied nanoparticles in dealing with various clinical and industrial issues (Ebaid et al., 2021; Goltyaev and Varlamova, 2023). Selenium is essential trace element for the body because it is a constituent of selenoproteins  influencing the activity of glutathione peroxidase, immune cells and many other important metabolic enzymes and proteins. It also protects cells and tissues from free radicals mediated harm by functioning as an antioxidant (Geoffrion et al., 2020). Selenium (Se) is often used as a dietary supplements (Nkengfack et al., 2019; Skalickova et al., 2017). However, depending on the chemical form of selenium, the period of supplementation and human health status, both a shortage and excess of selenium may be harmful to the body (Kieliszek and Bano, 2022). Selenium nanoparticles and citric acid have antioxidant, antibacterial and anticoagulant properties (Alhawiti, 2022).
       
Traditional selenium supplements have low absorption rates and high toxicity (Hosnedlova et al., 2018). The bioavailability of this element increases at the nanoscale, allowing for its regulated release into the body (Hosnedlova et al., 2018; Sadeghian et al., 2012). Numerous studies have found that Se-NPs can be more effective in cancer chemoprevention as possible anticancer agents and drug delivery carriers (Zambonino et al., 2023). Furthermore, its anti-metal toxicity properties are well established (Hassanin et al., 2013). Additionally, the immunostimulatory action of nanoscale selenium has been found to positively affect various physiological activities (AbdEl-Kader et al., 2023). Citric acid, in addition to its antioxidant bioactivity, promotes selenium stability (Abd El-Kader et al., 2023).
       
As CCl4- induced nephrpotoxicity is a serious medical concern, the present study is aimed to investigate whether supplementation with a combination of citric acid and selenium nanoparticles can effectively reduce CCl4- mediated nephrotoxicity in rat animal model. Samples from the treated animals were subjected to basic biochemical analysis that were further confirmed by histological evaluation.

MATERIALS AND METHODS

Preparation of the combination of citric acid and selenium nanoparticles (Se-NPs)
 
As a selenium precursor, selenium dioxide was dissolved in water and thoroughly combined with citric acid by continuous stirring at room temperature for 3 h using a magnetic stirrer. Ascorbic acid (100 mL of 0.1 M solution) was then gently dropped. At 100oC, the reaction mixture was vigorously stirred for 10 hours. After centrifugation, selenium/citric acid nanocomposites were collected and analyzed by scanning electron microscopy (SEM) and energy-dispersive X-ray spectroscopy (EDS) (Khurana et al., 2019; Shahabi et al., 2021).
 
Animals and experimental design
 
Twenty-four healthy male Swiss albino rats weighing 150-170 g (3-4 months old) were obtained from the Zoology Department (King Saud University, Riyad, Saudi Arabia). The rats acclimatized for a week to the laboratory settings in sufficiently large plastic cages before starting of the experiment. The rats were housed in an environment with a light-dark cycle of 12:12 h and a temperature range of 18-22oC, with access to food, water and ad libitum. The Animal Ethics Committee of King Saud University approved this study under ethical clearance number KSU-SE-20-38. Rats were divided into three groups (n=8). Group 1 was treated with vehicle solution (Phosphate Buffered Saline) equivalent in volume to the other treatment groups and served as the control. Group 2 was administered a single intraperitoneal (IP) injection of 1 ml/kg of CCl4 in liquid paraffin (1:1 v/v) (Makni et al., 2011). After a single dose of CCl4, group 3 was given at the dose of 2.5 mg/kg of the combination of citric acid and Se-NPs dissolved in phosphate buffer saline (PBS) as per a schedule of twice a week for three weeks (Ebaid et al., 2021).
 
Blood and kidney samples
 
After anesthesia, blood was drawn by puncturing the heart directly and placing it in tubes without any anticoagulant. The blood was centrifuged at 3000 × g for 10 min and the serum was separated into Eppendorf tubes and stored at -20oC. Serum was used to determine levels of renal function as well as the amount of albumin. The kidneys were removed from sacrificed animals and washed with PBS. They were cut into two parts: one part of the kidney was used for histological study and the other was used to assess lipid peroxidation (MDA) and reduced glutathione (GSH).
 
Renal function and albumin tests
 
Renal function tests (urea and creatinine) and albumin levels were determined in serum samples. They were measured using commercial kits (Salucea Company, Netherlands) according to the manufacturer’s instructions. A UV/visible spectrophotometer (Pharmacia Biotech, Cambridge, England) was used for all biochemical analyses. 
 
Estimation of lipid peroxidation and an assay of reduced glutathione
 
Lipid peroxidation in the kidney was measured following the method described by (Ohkawa et al., 1979) and the results were reported as nanomoles of MDA per mg of protein. Reduced glutathione was measured at 412 nm using the method described by (Moron et al., 1979), with DTNB as the coloring reagent.
 
Histological study
 
Light microscopy was used to examine kidney samples to assess the effect of the treatment. The tissues were embedded in paraffin after fixation in 10% neutral-buffered formalin. Hematoxylin and eosin (H&E) staining was performed on the paraffin slices (H&E). Collagen deposits were stained with Mallory trichrome to separate the slides. Kidney damage was assessed by blind folding using a Leica DMRB/E light microscope (Switzerland). A rating score between (-: no change) and (+++: severe damage) was assigned to each investigated section (Dommels et al., 2007).

Statistical analysis
 
Statistical analysis of the generated data was performed using SPSS software (IBM SPSS Statistics, Version 23). One-way analysis of variance (ANOVA) was used to determine the overall effects of each treatment. This analysis was supplemented by tests between treatments using Tukey’s method for pairwise comparisons. Results are expressed as arithmetic mean (M)±standard deviation (SD), with p<0.05 as statistically significant between the treatment groups.

RESULTS AND DISCUSSION

Structural examination of Se-NPs/citric acid matrix
 
SEM examination of the prepared selenium/citric acid nanocomposite showed the heterogeneous shape of agglomerated needles and spheres with an average diameter of 200 nm (Fig 1). EDS examination showed the surface elements of carbon (64.72%), selenium (30.94%) and oxygen (4.34%), confirming the formation of citric acid in the nanocomposite. The combination of citric acid and selenium has many advantages for drug delivery. Selenium is an essential element that affects several physiological processes in the form of various selenoproteins. A moderate number of elements can prevent health problems by enhancing metabolism and boosting immunity (Hosnedlova et al., 2018; Islam et al., 2023; Sadeghian et al., 2012). Hence, it contributes to a healthy life and increases average health. However, the element in its nanoform sheds its relative toxicity and is considered more appropriate for supplementation as a means of drug delivery or as an adjuvant to conventional medicine (Ferro et al., 2021; Raza et al., 2022).
 

Fig 1: The selenium nanoparticles were characterized by two prominent techniques.


 
Effect of the combination of citric acid and selenium nanoparticles on antioxidant status
 
Malondialdehyde (MDA) is a low-molecular-weight end product formed during the decomposition of some lipid peroxidation products. MDA estimation can be regarded as a diagnostic index for the extent of lipid peroxidation and oxidative injury in tissue lipids. Therefore, the present study considered MDA as a marker of lipid peroxidation induced by CCl4. Group II showed a significant increase in MDA levels by (812.69%) compared to the control group I. However, in group III, the combination of citric acid and Se-NPs significantly restored the MDA level by (24.34%) concerning group II (Fig 2).
 

Fig 2: Bar diagram showing standard oxidative stress parameters [malondialdehyde (MDA) and reduced glutathione (GSH) in samples from different rat groups: group I (control) was treated with vehicle solution only, group II was treated with CCl4 and group III was treated with CCl4+Se NPs.


 
       
Reduced glutathione (GSH) acts as a scavenger and enzyme-catalyzed antioxidant in the oxidative injury of different tissues. Therefore, GSH plays a major role in protecting biological structures and functions. In the present study, reduced glutathione (GSH) was used as a primary parameter to determine the antioxidant status of the kidneys of treated animals. Group II showed a decrease in GSH level of (24.09%) in group I, while the CCl4 + Se NP-treated group III showed a (13.90%) decrease in GSH level compared to group II (Fig 2).
       
Selenium is an essential component of many enzymes, some of which have antioxidant properties. Animals that are deficient in this element are more vulnerable to harm from certain forms of oxidative stress (Sobolev et al., 2018). In this study, we investigated the effects of Se-NPs, a powerful antioxidant, on the rat’s CCl4-induced kidney damage and oxidative stress in an animal model. Our results indicated that Se-NPs exerted an ameliorative effect against CCl4 nephrotoxicity. Our data confirm the formation of citric acid in the nanocomposite. The combination of citric acid and selenium has several advantages. These findings are consistent with those of a study conducted by Alhawiti, who found that citric acid and selenium nanoparticles have antioxidant, antibacterial and anticoagulant properties (Alhawiti, 2022). The combination of selenium and citric acid increases selenium stability and reduces the presence of the selenite form of the element, which is harmful and is associated with increased apoptosis (Fan et al., 2020; Hosnedlova et al., 2018; Nazýroðlu et al., 2017; Qian et al., 2019). Therefore, we planned this study to determine whether this combination could ameliorate CCl4-induced renal toxicity in vivo. The combination of citric acid and Se-NPs replenished the activity of vital antioxidant enzymes and proteins, such as reduced glutathione in CCl4 treated rats with greater efficacy.
 
Effect of the combination of citric acid and selenium nanoparticles on renal functions
 
Urea level is the most indicative marker of renal function. Interestingly, CCl4 in Group II resulted in a significant increase in urea levels by (96.92%) compared to the control. However, the combination of citric acid and the combination of citric acid and Se-NPs in group III was found to demonstrate a decrease in its level by (20.31%) compared to group II (Fig 3). However, the urea concentration in Group III was still significantly higher than that in the control group.
 

Fig 3: Bar diagram showing renal function (urea and creatinine) in serum samples from different rat groups. Group I (control) was treated with vehicle solution only, group II was treated with CCl4 and group III was treated with CCl4+ Se NPs.


       
Creatinine level is an indicator of renal function. The creatinine level increased by (35.63%) in group II after CCl4 injection. The combination of citric acid and Se-NPs decreased its level by (2.71%) in group III rats (Fig 3) compared to that in group II. However, no significant changes were observed in either group (II, III) compared with the control group. Statistical analysis revealed no significant changes in albumin concentrations during this study. However, its level was decreased by only (0.58%) in group II, while the combination of citric acid and Se-NPs enhanced it by (3.15%) in CCl4 treated group III (Fig 4).
 

Fig 4: Bar diagram showing total serum albumin in different rat groups: group I (control) with vehicle solution only, group II treated with CCl4 and group III treated with CCl4+ Se-NPs.


       
The critical parameters of kidney function (urea and creatinine), which were elevated in CCl4 injected rats, tended towards normal values with the supplementation of the combination of citric acid and Se-NPs. Many previous studies have demonstrated a consistent relationship between nephrotoxicity and oxidative stress (Wu et al., 2018). The results of our study on lipid peroxidation and renal function markers showed the same pattern (AlBasher et al., 2020) reported that Se-NPs exhibit antioxidant properties. This study also confirmed that Se-NP supplementation could counter CCl4-induced oxidative stress in vivo.
 
Kidney histology
 
Examination of the histopathological sections revealed that CCl4 induced severe deterioration in renal tissues compared to control rats. Dilated urinary space with partially shrunken glomeruli was observed in the CCl4 group. The combination of citric acid and Se-NPs showed a noticeable improvement in the renal tissues, exhibiting the urinary space and glomeruli structurally comparable to that of the control rats (Fig 5). Histological scores further confirmed that the combination of citric acid and Se-NPs noticeably improved the renal microstructure in the tissue samples in several histological indices; however, inflammatory cells were also observed in the same group (Table 1).
 

Fig 5: Representative microscopic images (H and E staining) at different magnifications for control.


 

Table 1: Histological score of the pathological changes in the renal tissues in rat treated only with CCL4 and those treated with CCL4 and Se-NPs.


       
The kidney is one of the prime targets for xenobiotic and toxic substances because its large share of blood flow gives it the capacity to concentrate these substances (Timbrell and Barile, 2023). The glomerular hypertrophy in CCl4-injected rats might be due to the proliferation of mesangial cells, which secrete more matrix as a defense mechanism. Furthermore, the blood capillaries appeared engorged with red blood cells and the urinary gap was obliterated in the kidney samples, as previously reported for indomethacin and piroxicam injections in rat animal models (Ebaid et al., 2007; Good et al., 2023). Infiltration of inflammatory cells into the intertubular tissues accompanied the tubular injury observed in the present study, possibly to minimize the lesion. Treatment with CCl4 also induced the infiltration of inflammatory cells in the target organ and kidney, similar to the induction of inflammation by indomethacin and piroxicam in rat as animal models (Abd-Alla et al., 2022).
       
Moreover, histological analysis of the tissue sections and their scores confirmed that considerable improvement was observed after the administration of NPs in the CCl4 treated group. Here, the combination of citric acid and Se-NPs were found to lower lipid peroxidation and increase the level of GSH compared to control rats. Our study is in accord of previously reported  by (Ansar et al., 2017) showing supplementation with Se-NPs attenuates hepatotoxicity more strongly than supplementation with Ag-NPs. The combination of citric acid and Se-NPs increases plasma glutathione peroxidase (GPx) activity in vivo (Yanez-Lemus et al., 2022). Therefore, our study is the first to report that combining SeNP with citric acid as nanocomposites are effective in ameliorating the CCl4- induced nephrotoxicity.
       
In addition, they exhibited much lower toxicity when assessed based on the LD50, acute kidney injury and short-term toxicity. The findings of the present study suggest that nanoscale selenium, such as Se-NPs with citric acid, can act as an antioxidant with a significantly reduced risk of toxicity compared with elemental selenium in vivo (Zambonino et al., 2023). The effect of Se-NPs on selenoenzyme upregulation is equivalent to that of selenite and Se-NPs, with a considerable decrease in acute toxicity (Zambonino et al., 2023).

CONCLUSION

In conclusion, this study confirmed that the combination of citric acid and Se-NPs alleviate CCl4-induced renal toxicity and the histological structure of renal tissues. These findings will pave the way for new therapeutic horizons of Se as Se-NPs, either as a means of drug delivery or as an adjuvant to any established drug have nephrotoxicity as a major side effect. The study will benefit to the people who are exposed to CCl4- based industries and consumer items. However, further studies are needed to understand the detailed mechanism involved in exploiting the advantages of Se-NPs with citric acid in biomedical and industrial applications.

ACKNOWLEDGEMENT

This work was supported by the Researchers Supporting Project number (RSP2024R366) of King Saud University, Riyadh, Saudi Arabia.

CONFLICT OF INTEREST

All authors declared that there is no conflict of interest.

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