Science International  Volume 5 Issue 3, 2017

Research Article

Antioxidant and Ameliorative Effects of Zingiber Officinale Against Aluminum Chloride Toxicity
Nabil A. Hasona
Department of Chemistry, Faculty of Science, Beni-Suef University, Beni-Suef, Egypt

Mohammed Q. Ahmed
Department of Pharmacology, College of Medicine, Hail University, Hail, Kingdom of Saudi Arabia

ABSTRACT:
Objective: The present study was performed to assess the antioxidant capacity of different doses of Zingiber officinale extract and its efficacy in alleviating the biochemical alterations induced by aluminum chloride in rabbits. Material and Methods: Twenty-eight male rabbits were allocated into four groups (7 rabbits in each); Group I: Served as normal control, Group II: Treated with aluminum chloride (AlCl3) (150 mg kg–1 b.wt.), Group III: Treated with AlCl3 and Zingiber officinale extract (100 mg kg–1 b.wt.) and Group IV: Treated with AlCl3 and Zingiber officinale extract (200 mg kg–1 b.wt.). Rabbits in groups (III, IV) were orally treated daily with Zingiber officinale extract for 4 weeks. Data was analyzed using SPSS. Results: Aluminum exposure caused a significant elevation of BUN, creatinine, lipid profile, ALT, ALP, TNF-α and amylase activity. All these parameters showed the reverse trend following oral Zingiber officinale treatment. Aluminum exposure showed a significant decrease in hepatic GSH and catalase activity. Treatment with Zingiber officinale extract significantly reversed aluminum effects, in the level of GSH content and hepatic catalase activity. Conclusion: Zingiber officinale is effective in alleviating the oxidative stress and inflammation and is thus effective in improving lipid profile and hepatotoxicity and nephrotoxicity in AlCl3 administration.
 
    How to Cite:
Nabil A. Hasona and Mohammed Q. Ahmed , 2017. Antioxidant and Ameliorative Effects of Zingiber Officinale Against Aluminum Chloride Toxicity. Science International, 5: 96-104
DOI: 10.17311/sciintl.2017.96.104
 


INTRODUCTION

Plant derived products have been used for medicinal purposes for centuries and also being used in our daily food intake. Drugs of plant source are known to play an important role in the controlling of many diseases. Ginger is one of the world’s best known spices. Ginger (Zingiber officinale, Family: Zingiberaceae), an herbal drug, produced in South-East Asia and then became prevalent in many ecological areas. Ginger (Zingiber officinale) is one of the most widely used spices for the seasoning of food worldwide1. The major chemical ingredients of the ginger rhizome are essential volatile oil and non-volatile pungent compounds, such as gingerols, shogaols, paradols and zingerone2. The pharmaceutical importance of ginger is due to the presence of alkaloids, glycosides, resins, volatile oils, gums and tannins etc. The active ingredients usually remain concentrated in the storage organs of the plants3.

Aluminum is a plentiful element in the earth’s layer and is widely distributed throughout the environment. Currently, aluminum salts are included in greasepaints, food handling and packing also used in various nonprescription drugs4. Several authors designate that an excessive and prolonged aluminum exposure directly affects hematological and biochemical parameters, interrupts lipid peroxidation and diminishes the activities of the antioxidant enzymes in plasma and tissues of animals models5. This impairment of the physiological pro-oxidant/antioxidant balance causes oxidative stress.

The serum biochemical profile is a key index that reveals the main organ functions. The liver and kidney are the main organs used for metabolism and excretion. Liver, the vital organ involved in numerous metabolic functions and detoxification of lethal substances, is a frequent target of a number of toxicants. The disruption in the transport function of the hepatocytes as a result of hepatic damage causes the outflow of enzymes from the liver cytosol into the blood due to altered permeability of membrane6.

The kidney is a complex organ for its role as an organ of excretion, reabsorption and general homeostasis, has an extensive blood flow, receiving approximately 1.2 L min–1 and filtering on average 125 mL plasma min–1. The processes of reabsorption and secretion, particularly of organic acids and bases, may, however, lead to the accumulation of toxins within the tubules, making this vital organ more susceptible to toxic insults than other organs7.

The aim of the present study is to appraise the phytochemical characterization of the ethanol extract of ginger and evaluate the antioxidant, anti-inflammatory, hepatoprotective, hypolipidemic and nephroprotective effects against AlCl3 toxicity in rabbits.


MATERIALS AND METHODS

Chemicals: Aluminium chloride anhydrous (AlCl3), M.W. 133.34 was purchased from Aldrich Chemical Company (Milwaukee, WI, USA). All other chemicals and reagents used were of analytical grade.

Plant materials: Ginger (Zingiber Officinale) was purchased from a local market of the herbs in Hail city, KSA.

Preparation of the extract: Ten gram of ginger powder were placed in the round bottle flask; 100 mL of ethanol (70%) were added to the flask. After soaking 12 h the extract was filtered by using Whatman filter paper No. 31 the filtrate so obtained was placed in the oven to facilitate evaporation of ethanol content8. The crude extract was used for further investigation for antioxidant properties.

Phytochemical examination: The Phytochemical screening for the presence of alkaloids, tannins, flavonoids, phlobatannins, anthraquinone, coumarins, carbohydrates and terpenoids were carried out according to the methods of Harborne9 and Trease and Evans10.

Determination of antioxidant activity of ginger extract
Determination of total antioxidant capacity: Total antioxidant capacity of extract was assayed by the phosphomolybdenum method as described by Prieto et al.11.

Determination of reducing power: The reducing power of extract was determined by the method of Oyaizu12.

Experimental animals: Male white rabbits (Initial weight of 1.00±0.27 kg) were used. All animals received humane care in compliance with the guidelines of the Ethics Committee of the Experimental Animal Care Society, College of Medicine, University of Hail, Saudi Arabia. Animals were individually kept in stainless steel cages. Feed and water were provided ad libitum. Rabbits were fed with pellets consisted of Alfalfa pellets 35%, maize broke 15%, barley 15%, white sorghum 10%, sunflower white 5%, sunflower black 5%, wheat 10% and safflower 5%.

Design of the experiment: After one week of acclimatization period, 28 mature male rabbits were randomly divided into four equal groups of seven rabbits each. Group I: Served as normal control. Group II: Administrated with aluminum chloride (AlCl3) (150 mg kg–1 b.wt.) were given by intraperitoneal injection13. Group III: administrated with AlCl3 (150 mg kg–1 b.wt.) by intraperitoneal injection and ginger extract (100 mg kg–1 b.wt.) by oral gavage. Group IV: administrated with AlCl3 (150 mg kg–1 b.wt.) by intraperitoneal injection and ginger extract (200mg kg–1 b.wt.) by oral gavage. Rabbits in groups (3, 4) were orally treated daily with ginger extract for 4 weeks. The doses of ginger and AlCl3 were calculated according to the animal’s body weight on the week before dosing.

By the end of the experimental periods (4 weeks), the rabbits were sacrificed at fasting state. The blood samples were collected and allowed to coagulate at room temperature and centrifuged at 3000 rpm for 10 min. The clear, non-haemolysed supernatant sera were quickly separated and stored at -20°C for subsequent biochemical analysis.

Liver tissues were quickly excised, weighed and homogenized in a saline solution (0.9%) and centrifuged at 3000 rpm for 15 min and the supernatant were stored at -20°C for the assay of biochemical parameters related to oxidative stress.

The determination of hepatic catalase activity was assayed as described by Cohen et al .14 and hepatic content of reduced GSH was assayed by the spectrophotometric technique according to Sedlack and Lindsay–1 b.wt.15.

The following biochemical tests were performed, serum ALT and ALP activities by using clinical test kits (UDI/KSA); serum BUN according to Patton and Crouch16 and serum creatinine level as per the method of Henry17. Serum totalcholesterol, triglyceride and HDL-cholesterol were assayed according to Allain et al.18, Jacobs and Van Denmark19 and Gordon and Gordon20, respectively, by using clinical test kits (UDI/KSA). Serum LDL-cholesterol and vLDL-cholesterol levels were calculated according to the following formula:

LDL-cholesterol = TC-(TG/5)-HDL-cholesterol21

And:

VLDL-C =TG/5, respectively22

Serum TNF-α was determined by using specific ELISA kit (R and D system) following the manufacturer’s instructions.

Statistical analysis: The Statistical Package for the Social Sciences (SPSS for WINDOWS, version 18.0; SPSS Inc, Chicago) was used for the statistical analyses. Comparative analyses were conducted by using the general linear models procedure (SPSS Inc). Values of p>0.05 were considered statistically insignificant, while values of p<0.05 were considered statistically significant, values of p<0.01 were considered statistically highly significant and p<0.001 were considered statistically very highly significant.


RESULTS

Preliminary phytochemical examination: The crude extract of ginger was examined for the most common phytochemical ingredients of medicinal plants for which hepatoprotective activity of other plants has been ascribed. These included saponins, tannins, flavonols, glycosides, terpenoids, alkaloids, reducing sugars, steroids, proteins, fats and polyphenols. The results showed that the most abundant phytochemicals were tannins, alkaloids, phenols, vitamins, flavonoids and terpenoids as shown in Table 1.

Total antioxidant activity and reducing power: The total antioxidant activity is based on reduction of molybdate [VI] to molybdate [V] at acid pH and formation of a green phosphate complex, which can be quantified spectrophotometrically at 695 nm. In the current study, as shown in Fig. 1, total antioxidant capacity of ginger extracts was demonstrated. The results revealed that the antioxidant activity of the ginger extracts increased with increasing concentration of the ginger extract.

On the other hand, the reducing power assays. Increased absorbance of the reaction mixture indicates increased reducing power. Figure 2 shows the dose response for the reducing power of the extract of ginger. The reducing power values were found to be correlated with the concentration of each extract.

Biochemical analysis: As shown in Fig. 3 AlCl3 -administered rabbits showed significantly (p<0.001) elevation in serum ALT and ALP activities as compared to normal control group.

Table 1: Phytochemical screening of ethanolic ginger extract

Figure 1: Total antioxidant capacity of ginger extract

Figure 2: Total reduction capacity of ginger extract

Whereas, a significant decrease (p<0.001) in the serum ALT and ALP activities after treatment by either dose of ginger extract when compared with AlCl3 treated control group.

Also, as shown in Fig. 3 AlCl3 administered rabbits showed markedly (p<0.001) increased in the level of TNF-α when compared with control group. Treatment of AlCl3 intoxicated rabbits with either dose of ginger extract (100 or 200 mg mL–1) markedly (p<0.001) decrease the level of TNF- α as compared to AlCl3 control group.

On the other hand, the serum creatinine and BUN levels in the AlCl3 treated control group showed a significant (p<0.001) increase when compared to the normal control one. The oral administration of ginger extract with either dose produced a marked (p<0.001) improvement in the altered serum creatinine and BUN levels of the AlCl3 intoxicated group Fig. 4.

Data summarized in Table 2 show the effect of AlCl3 administration and treatment with ginger extract on lipid profile. The administration of AlCl3 produced marked elevation of lipid profile as showed by the significant (p<0.001) elevation in serum total cholesterol, triglycerides, vLDL- cholesterol and LDL-cholesterol levels.

Figure 3(a-c): Effect of ginger extract on serum ALT and ALP activities and TNF-α level

Concurrent oral administration of either dose of ginger extract significantly decreased the elevated levels of serum total cholesterol, triglycerides, vLDL-cholesterol and LDL-cholesterol levels when compared with the AlCl3 control group. In contrast, a significant (p<0.001) decline in the level of HDL- cholesterol was observed in AlCl3-treated group as compared to normal control one. On the other hand, there was a significant (p<0.001) increase in HDL-cholesterol in ginger treated rabbits when compared to AlCl3- treated group Table 2.

On the contrary, AlCl3 intoxicated rabbits showed significantly (p<0.001) decrease in the hepatic content of GSH and catalase activity as compared to normal control group. On the other hand, ginger extract treatment with high dose (200 mg mL–1) showed a significant (p<0.01) elevation in hepatic catalase activity and a significant (p<0.01) improvement in hepatic content of GSH when compared with AlCl3 control one Fig. 5.

Table 2: Effect of ginger extract (GE) on serum levels of lipid profile

Figure 4(a-b): Effect of ginger extract on serum BUN and creatinine levels


DISCUSSION

The exploration of medicinal properties of various plants is paying attention, since the last couple of decades due to their forceful pharmacological activities, appropriateness, economic feasibility and low toxicity. Recently, there has been an upgrading of finding natural antioxidants, from plant materials to replace synthetic antioxidants because the previous ones are accepted as green medicine to be safe for health controlling whereas, the latter ones are quite unsafe and their toxicity is a matter of concern23. Natural antioxidants belonging to the higher plants especially the typical compounds, such as vitamins, carotenoids and phenolics reveal antioxidant activity and they lessen disease-related chronic health problems.

Figure 5(a-b): Effect of ginger extract on hepatic catalase activity and hepatic reduced glutathione content in AlCl3-induced toxicity

It has been denounced that there is an inverse affiliation between antioxidative status and incidence of human diseases such as malignancy, caducity, neurodegenerative disease and atherosclerosis24.

In the current study, Phytochemical screening of ethanolic ginger extract showed the presence of alkaloids, phlobotannins, flavonoids, carbohydrates, tannins, coumarins and terpenoids and absence of anthraquinone Table 1. Similar results were obtained in the study by which showed that the phytochemical screening of ginger shows the presence of carbohydrates, alkaloids, saponins, flavonoids, polyphenols and reducing sugars in both aqueous and petroleum ether extracts25,26. As a rich source, Phytochemical and mineral contents ginger can be considered a potential source of medicinal herb.

Antioxidant activity of ginger extract was assessed by determination of total antioxidant capacity and determination of reducing power. Antioxidant compounds and their activity are highly dependent on concentration of the solvent and type of the solvent27.

Our results revealed that the antioxidant capacity of the ginger extract increased with increasing concentration of the ginger extract. Regarding, the reducing power assay, there are dose response for the reducing power of the ginger extract where increased absorbance of the reaction mixture indicates increased reducing power. Our results are in agreement with Maizura et al.28 and Eleazu et al.29. Moreover, previous studies reported that the reducing power of bioactive compounds is associated with antioxidant activity30.

Transaminases are intracellular enzymes, released into the circulation after injury of hepatocytes31. ALT is the most specific indicator of hepatic injury and hepatocellular necrosis. This liver enzyme catalyzes the transfer of α-amino group alanine to the alpha-ketoglutaric acid32.

Exposure to high concentrations of Al can result in its accumulation in the liver and in turn to alterations in the liver function. The current study provoked significant alterations in the activity of ALT in the blood of AlCl3-treated rabbits which may be a sign of impaired liver function and disorder in the biosynthesis of these enzymes with modulation in the permeability of the liver membrane. These results are in concordance with findings of Geyikoglu et al.33, Ighodaro et al.34 and Attyah and Ismail35.

ALP is a membrane-bound enzyme related to the transport of several metabolites so it is a profound biomarker for liver disease. In the present study, AlCl3 caused a significant elevation in the activity of ALP. This observation is in concordance with the earlier findings of Geyikoglu et al.33and Ighodaro et al.34. On the other hand, oral administration of AlCl3 treated rabbits by ginger extract causes a reduction in the serum ALT and ALP activity. These may be attributed to ginger components which may stabilize hepatocytes plasma membrane and prevent transmission of ALT to the extracellular fluid. This finding is in agreement with results of Thomson et al.36.

The current findings showed that administration of AlCl3 has induced kidney injury and glomerular dysfunction evidenced by the elevated circulating creatinine and blood urea nitrogen levels. These measurements are often regarded as reliable markers of kidney damage37 and indicate the loss of a majority of kidney function38. These elevated assessments are in agreement with the studies of Ahmed et al.32 and Geyikoglu et al.33. Concomitant administration of either dose of ginger extract significantly decreased circulating creatinine and blood urea nitrogen levels. These results are in agreement with the previous studies of Gehan and Amin39 and Abdalla et al.40, who states that presence of polyphenols and flavonoids in the ginger extract might be responsible for the antioxidant nephroprotective activities and the reduction of serum urea and creatinine levels.

AlCl3 administration induced a significant increase in serum level of TNF-α which represents an important mediator of inflammatory tissue damage. Studies presented evidence that nephrotoxicants could provoke an inflammatory response leading to organ injury41. The significantly elevated TNF-α reflects the degree of inflammation. In a dose-dependent manner, concurrent administration of ginger extract produced pronounced decline in serum TNF-α, indicating its anti-inflammatory efficacy. This finding is consistent with that of recent studies on ginger supplementation on anti-inflammatory mediators. Naderi et al.42 found that ginger extract had an anti-inflammatory effect on elderly knee osteoarthritis patients. Active ingredients of ginger extract decreased TNF-α expression by inhibiting I-kappa B alpha phosphorylation, nuclear factor-kappa B (NF-k B) nuclear activation and protein kinase C-alpha translocation.

AlCl3 administration resulted in dyslipidaemic changes, as illustrated by increasing total cholesterol, triglycerides, vLDL-cholesterol and LDL-cholesterol and a decrease in serum level of HDL-cholesterol. Concurrent oral supplementation of either doses of ginger extract significantly decreased serum levels of total cholesterol, triglycerides, vLDL-cholesterol and LDL-cholesterol and increased serum HDL-cholesterol levels. The lipid lowering effect of ginger may come from inhibition of hepatic fatty acid synthesis by lowering key enzymes activities in supplying substrates, thus reducing serum levels of cholesterol and triglyceride. Our finding is in line with a previous report43,44. It was recommended by Hasona et al.45 that presence of phytoconstituents like flavonoid inhibits fat accumulation and ameliorates dyslipidemia and increased antioxidant defense.

Oxidative stress plays a key contributory role in many diseases including liver damage46. The body has anti-oxidative mechanisms to alleviate oxidative molecules, control lipid oxidation and preserve these radicals in balance. When free radicals are produced, the body preserves itself from these radicals by endogenous antioxidants47. Catalase enzyme is known to play an important role in scavenging reactive oxygen species. CAT decreases the H2O2 into water and oxygen to prevent oxidative stress and in maintaining cell homeostasis. Administration of AlCl3 reduced the activity of antioxidant enzyme catalase in the liver tissue. The reduction in the activity of catalase enzyme reflects the reduced synthesis of this enzyme due to higher intracellular concentrations of Al and/or accumulation of free radicals and that in agreement with Newairy et al.44.

The administration of ginger extract with AlCl3 repaired the oxidant/antioxidant balance as reflected by the stimulation of the antioxidants enzyme catalase in the liver. These results are in agreement with Kalaiselvi et al.43 who showed that Ginger has an ability to increase the intracellular activities of catalase and have synergistically conflict oxidative stress by scavenging free radicals and boosting endogenous antioxidant activities. This may be related to its active components which motivate free radical scavenging activities48.

Glutathione is an important biofactor produced in all living cells. It forms an important substrate for GPX, GST and several other enzymes. In addition, GSH plays an important role in hepatic antioxidation and drug metabolism. High intracellular GSH levels lessen damage and stimulate better persistence under conditions of oxidative stress49. Reduced glutathione (GSH) constitutes the first line of defense against free radicals. AlCl3 treatment resulted in a decrease in the hepatic GSH content. These observations are similar to the data reported by Kalaiselvi et al.43.The administration of ginger extract plus AlCl3 the GSH content was increased. These results are in agreement with Kalaiselvi et al.43 and Reddy et al.50.


CONCLUSION

Based on the findings of this study, it was accomplished that ginger extract showed promising antioxidant, anti-inflammatory, hepatoprotective, hypolipidemic and nephroprotective effects against AlCl3 toxicity. The previous ameliorative properties of ginger make it useful as a therapeutic candidate for the treatment of human diseases.


ACKNOWLEDGMENT

The authors are thankful to the Dean of College of Medicine, Hail University, Kingdom of Saudi Arabia for supporting and providing all facilities to carry out this work.


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