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 Table of Contents  
EXPERIMENTAL STUDIES
Year : 2012  |  Volume : 1  |  Issue : 1  |  Page : 23-29  

Effects of cactus pear (Opuntia ficus indica) juice on oxidative stress in diabetic cataract rats


1 Department of Biochemistry and Nutrition, Women's College Ain Shams University, Giza, Egypt
2 Home Economic, Women's College Ain Shams University, Giza, Egypt
3 Department of Biochemistry, Faculty of Agriculture, Cairo University, Giza, Egypt; Department of Medical Biochemistry, College of Medicine and Medical Science, Taif University, KSA
4 Department of Food Science, Faculty of Agriculture, Ain Shams University, Cairo, Egypt
5 Department of Biochemistry and Nutrition, Research Institute of Ophthalmology, Giza, Egypt

Date of Web Publication13-Apr-2012

Correspondence Address:
Anhar M Gomaa
Department of Biochemistry and Nutrition, Research Institute of Ophthalmology, Giza, P.O. Box 12111, Egypt

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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/2278-0521.94980

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  Abstract 

Diabetes mellitus is a heterogeneous metabolic disorder characterized by hyperglycemia. It is often associated with complications, such as cataracts. The purpose of this study was to investigate the effects of cactus pear juice on oxidative stress and cataract formation in alloxan-induced diabetic rats. Rats were divided into six groups, Group 1 untreated as negative control, Group 2 injected with alloxan only to induce diabetes as diabetic cataract positive control, Groups 3,4,5 and 6 injected with alloxan and given orally 1, 2, 3 and 4 ml concentrated cactus juice/rat/day, respectively. After 8 weeks, the animals treated with cactus juice showed a significant decrease in the level of blood glucose and lipid peroxidation in blood and lens, and a significant decrease in the concentration of lens Fas ligand, compared with negative control (group 1). Also, the treated groups showed significant increase in the level of reduced glutathione and the activity of superoxide dismutase and significant decrease in the levels of nitric oxide concentration. Slit lamp examination revealed that supplementation with cactus juice delayed the progression and maturation of cataract in the treated groups compared with positive control (group 2), which developed subcapsular cataract. The best result observed in Group 5, which was given orally 3 ml juice/rat/day. The data in the present study indicate that cactus juice is a rich source of natural antioxidants such as total phenolics, total flavonoids, vitamin C, vitamin E, β-carotene and total carotenoids. It can be concluded that regular consumption of cactus pear juice can protect the body from the oxidative stress and can attenuate the development of cataract as a complication of diabetes by reducing the level of blood sugar.

Keywords: Antioxidants, cactus pear juice, cataract, diabetes, flavonoids, lens, oxidative stress, phenolics, vitamin C


How to cite this article:
Abd El-Razek FH, El-Metwally EM, Shehab GM, Hassan AA, Gomaa AM. Effects of cactus pear (Opuntia ficus indica) juice on oxidative stress in diabetic cataract rats. Saudi J Health Sci 2012;1:23-9

How to cite this URL:
Abd El-Razek FH, El-Metwally EM, Shehab GM, Hassan AA, Gomaa AM. Effects of cactus pear (Opuntia ficus indica) juice on oxidative stress in diabetic cataract rats. Saudi J Health Sci [serial online] 2012 [cited 2019 Jul 21];1:23-9. Available from: http://www.saudijhealthsci.org/text.asp?2012/1/1/23/94980


  Introduction Top


Cataract is one of the complications that diabetic patients are at higher risk of developing. It is characterized by cloudiness or opacity of the eye lens and is the leading cause of blindness worldwide. [1] The association between diabetes and cataract formation has been shown in clinical epidemiological and basic research studies. It is well established that osmotic stress from the accumulation of sorbitol in the ocular lens leads to cataract development. There are numerous publications that describe oxidative stress damage to lens fibers by free radical in diabetics. However, there is no evidence that user these free radicals initiate the process of cataract formation but rather accelerate and aggravate its development. [2],[3]

It has been suggested that glucose autoxidation and nonenzymatic glycation, together termed glycoxidation, are the major contributors to the increase in free radicals in diabetic lens. [4]

Several studies have suggested that intake of antioxidant-rich foods may slow the progression of cataract. [5],[6] The cactus, Opuntia spp. has been used in traditional medicine and as a source of vegetal nutriments in many countries. It has been reported that the extracts of fruits and stems of cactus exhibit hypoglycemic, [7] anti oxidant, [8] anti-tumor, [9] anti-ulcer, [10] anti-allergic [11] and analgesic and anti-inflammatory actions. [12] The nutraceutical benefits of cactus juice and extracts are believed to their contents of a large variety of compounds with anti-ulcerogenic activity and antioxidant properties such as polyphenols, vitamins C and E, β-carotene, glutathione and a mixture of betaxanthin and betacyanin pigments. [13],[14] Moreover, the regular consumption of cactus juice was reported to reduce blood glucose and cholesterol levels. [15] Accordingly, we hypothesized that cactus juice may prevent or delay the progression of cataract formation in alloxan induced diabetic rats.

To our knowledge, no publication has been tested the effects of cactus juice on the delay or the prevention of cataract formation. Thus, in this study, we investigated the beneficial effects of different doses of cactus pear juice on the oxidative stress induced by diabetes and protect or delay from cataract formation in alloxan induced diabetic rats.


  Materials and Methods Top


Plant material and juice preparation

The orange-yellow cactus pear (Opuntia ficus indica) fruits were purchased from a local market in Cairo (Egypt) during summer season 2010. Whole fresh fruits were sorted, washed with tap water, manually peeled then the juice was extracted from the whole edible pulp using a food processor with no addition of water and centrifuged (3000 rpm, 10 min, 4°C) to remove hard fibers and seeds. Aliquots of the supernatant were stored frozen at −20°C for the subsequent chemical analysis. For biological experiment, the juice was concentrated to one fifth the volume by lyophilization then aliquots were kept frozen at −20°C until used.

Chemicals

Folin-Ciocalteu reagent, gallic acid, rutin, ascorbic acid, 2,6-dichlorophenol indophenol reagent, alloxan, sodium carbonate and aluminum chloride were purchased from Sigma-Aldrich Co. Ltd. (St. Louis, MO, USA). The chemical used were of analytical grade. The used kits were purchased from Gama Tried Co. (El-Mohandessen, Cairo).

Experimental design

Diets

Commercial diet 12% protein was prepared for all rats from fine ingredients according to National Research Council. [16] Diet and water were provided ad-libitum through the experimental period (8 weeks).

Animal treatment and samples collection

During the experiment, 36 adult male, Spargue Dawely strain rats obtained from Research Institute of Ophthalmology Giza - Egypt, weighting 135-145 g were used. All animal experiments were carried out in accordance with the internationally accepted guidelines for the care and use of laboratory animals. Rats were kept in a controlled environment (temperature 22±2°C, natural light) and divided into six groups. Group 1 untreated group (negative control), Group 2 were injected with alloxan (130 mg/kg body weight) to induce diabetes (positive control) and Groups 3, 4, 5 and 6 were injected with alloxan to induce diabetes then were given orally 1, 2, 3 and 4 ml concentrated cactus juice/day/rat, respectively.

Freshly prepared alloxan was administered by a single intraperitoneal injection of 130 mg/kg body weight. The diabetic state was confirmed by the measurement of blood glucose concentration 3 days after alloxan injection using blood samples from the eyes. Animals with blood glucose levels of less than 165 mg/dl were excluded. Eyes were examined every week using a slit lamp biomicroscope on dilated pupil to investigate the lenticular opacity. At the end of the experiment, all rats were fasting and blood samples were taken from the eyes under ether anesthesia for biochemical analysis. The eyes were enucleated then the lenses were excised, carefully decapsulated and washed in 0.15 M isotonic sodium chloride solution. Lens homogenate was prepared according to each method. Samples were kept in deep freezer at −20°C until used.

Biochemical analysis

Glucose was determined in serum as described by Howanitz and Howantiz. [17] Reduced glutathione (GSH) was determined in blood and lens according to Beutler et al.[18] Serum and lens superoxide dismutase activity (SOD) was assessed by the method of Marklund and Marklund, [19] and nitric oxide (NO) according to Moshage et al.[20] Lens Fas ligand (FasL) was assessed as described by Tanaka et al.[21] Serum and lens lipid peroxidation as malonaldehyde (MDA) was determined according to the method of Draper and Hadley. [22]

Cactus pear juice analysis

Three separate juice preparations were used for the chemical analysis. Total phenolics content was determined using Folin-Ciocalteu reagent. [23] Gallic acid was used as a standard and the results were expressed as mg gallic acid equivalents (GAE)/100 g of cactus juice. Total flavonoids content were determined by the colorimetric method described previously, [24] using rutin as a standard. The results were expressed as mg rutin equivalents (RE)/100 g of cactus juice. Vitamin C or ascorbic acid content was measured using the 2, 6-dichlorophenol indophenol titrimetric method (AOAC). [25] Vitamin C content was expressed as mg/100 g of cactus juice. Vitamin E content was analyzed by HPLC according to the procedure described by Lee et al.[26] Vitamin E content was expressed as μg/100 g of cactus juice. β-carotene content was measured by HPLC according to the Danish official, [27] the are results expressed as μg/100 g of cactus juice. Total carotenoids content was measured spectrophotometrically as described by Dere et al.[28] The results were expressed as mg/100 g of cactus juice.

Statistical analysis

The obtained results were statistically analyzed according to statistical analysis system SAS User's Guide, (SAS, 1999). LSD at 5% level of significance was used to compare between means according to Snedecor and Cochran. [29]


  Results Top


The cactus peer juice antioxidant compounds

The compounds of cactus peer juice with antioxidant activity such as total phenolics, total flavonoids, vitamin C, vitamin E, β-carotene and total carotenoids were determined. The data in the present study indicate that cactus juice is a rich source of natural antioxidants [Table 1]. The cactus juice exhibited high total phenolic content (228.5±0.97 mg gallic acid equivalents (GAE)/100 g) and total flavonoids (26.95±0.51 mg rutin equivalents (RE)/100 g). The amount of vitamin C and vitamin E assessed in the cactus juice was 14±0.23 mg/100 g and 125±0.76 μg/100 g, respectively. The concentration of β-carotene was 17.54±0.62 μg/100 g, while the total carotenoids concentration was 3.92±0.19 mg/100 g.
Table 1: Vitamin and antioxidant contents of cactus pear juice per 100 g

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The biological effects of cactus juice

The animals treated with alloxan only (group 2; the positive control) showed, compared with Group 1 (negative control), a significant increase in the level of blood glucose and lipid peroxidation in blood and lens, and the concentration of lens FasL, while the level of reduced glutathione (GSH) and the activity of the antioxidant enzyme superoxide dismutase (SOD) concentration decreased significantly [Table 2] and [Table 3]. The level of nitric oxide (NO) was increased in diabetic cataract group when compared to control group [Table 2] and [Table 3].
Table 2: Effect of different levels supplementation of cactus juice on serum glucose, blood reduced glutathione, serum superoxide dismutase, serum nitric oxide and serum lipid peroxidation as malonaldehyde in cataract diabetic rat groups (mean±SD)

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Table 3: Effect of different levels supplementation of cactus juice on lens Fas‑ligand, reduced glutathione, superoxide dismutase, nitric oxide and lipid peroxidation as malonaldehyde in diabetic cataract rat groups (meanąSD)

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The treatment with different doses of cactus pear juice (groups: 3, 4, 5 and 6) significantly decreased serum glucose levels compared with diabetic cataract group (group 2; the positive control). There was no significant change in the glucose level between Groups 3, 4, 5 which treated with alloxan and given orally 1 ml, 2 ml, and 3 ml concentrated juice/day/rat and the negative control group. A significant glucose value observed in Group 6 compared with the negative control (group 1) but still significantly lower than the positive control.

The data in [Table 2] and [Table 3] show that, in both blood and lens the treatment with different doses of cactus pear juice (groups: 3, 4, 5 and 6) significantly decreased lipid peroxidation as malonaldehyde (MDA) compared with diabetic cataract group (group 2) the decrease was also dose dependant with the exception of Group 6, which show a little increase in the value of MDA compared with the other groups (3, 4 and 5). The best results were observed in Group 5 (treated with alloxan and given orally 3 ml concentrated juice/day/rat).

The level of reduced glutathione (GSH) and the activity of superoxide dismutase (SOD) in all treated groups increased significantly compared with diabetic cataract group (group 2) in both blood and lens. Also, the increase in the activity was dose dependant with the exception of Group 6, which show a little decrease in the activity compared with the other treated groups (3, 4 and 5), but still significantly higher than the positive control (group 2) [Table 2] and [Table 3]. The best results were also observed in Group 5 (given 3 ml juice/day/rat).

The results of NO concentration in blood and lens show a significant decrease in all treated groups compared with the positive control (group 2) [Table 2] and [Table 3].

The examination of eyes using a slit lamp biomicroscope on dilated pupil to investigate the lenticular opacity revealed that the juice treatments, delay the formation of cataract.


  Discussion Top


In recent years, an attention is given to the study of natural products and healthy foods, which may counteract the detrimental effects of environmental toxic compounds and prevent multiple human diseases. [30],[31] In addition to the major food constituents, fruits and vegetables contain other components that may have a positive effect on human health. [32] In this line, this study was undertaken to analyze the important components of cactus pear juice and to investigate its effects on oxidative stress in diabetic cataract rats and its protective action against cataract development.

Cataract is the leading cause of blindness worldwide and its surgical treatment is expensive and usually has risks. [1] It has been demonstrated that the rate and progression of cataract is elevated in diabetic patients, who also have higher complication rates from cataract surgery. [33] In recent years, oxidative stress is thought to contribute to diabetes induced cataract and researchers have focused on the impact of oxidative stress on lens transparency and the antioxidant defense against free radicals and reactive oxygen species. [34],[35] It has actually been suggested that cataract in diabetic lenses may be attributed to oxidation. [35] Therefore, finding a way to delay or inhibit the mechanisms leading to the development of cataract is desirable.

Many plants have successfully been used to overcome this problem. Cactus specious is widely used in medicine to treat various diseases including diabetes. Chang et al., [36] suggested that opuntia fruit byproducts may play potential role as a source of health promoting phenolics associated with antioxidant activity.

As shown in [Table 1] the chemical analysis of the cactus pear juice indicated that it contains significant amounts of various antioxidants such as phenolic compounds (228.5±0.97 mg GAE/100 g), flavonoids (26.95±0.51 mg RE/100 g), carotenoids (3.92±0.19 mg/100 g) and vitamins C and E (14±0.23 mg/100 g and 125±0.76 μg/100 g, respectively). These data was in agreement with several studies, which demonstrated that cactus pear yield high values of important nutrients and exhibit antioxidant functions. [13],[37]

According to Wu, et al., [38] most of the antioxidant capacity (AC) associated with fruits is exerted by ascorbic acid and phenolic compounds, and only about 1% of the total AC in fruits and vegetables is due to lipophilic compounds. Recently, Yahia and Mondragon-Jacobo, [39] observed the highest AC in the hydrophilic extracts compared with the lipophilic extracts of ten cultivars and lines of cactus pear fruit (Opuntia spp.). They suggested that betalains, vitamin C and phenolic compounds contributed in higher extent to the AC than other phytochemicals such as carotenoids and tocopherols.

The antioxidant ascorbic acid, flavonoids and phenolic compounds can lower the risk of cataract development. Many studies have shown that ascorbic acid plays an important role in lens biology that can completely protect the lipids from detectable peroxidative damage. [40] Also, it has been demonstrated that flavonoids can prevent or delay the occurrence of cataracts in rat lenses, in diabetic cataracts. [5],[6] Quercetin, a major dietary flavonoid that present in cactus, is an effective inhibitor of H 2 O 2 -induced lens opacification by inhibiting oxidative damage to the lens and inhibiting aldose reductase activity in lenses of diabetic rates as reported by Cornish, et al.[41] This enzyme initiates cataract formation in diabetes, thus we are suggested that flavonoids in cactus pear may have a role in delay or prevent cataract formation.

Likewise, phenolic compounds are very important plant constituents because of their antioxidant activities. Recently, Chang et al., [36] suggested that opuntia fruit byproducts may play potential role as a source of health promoting phenolics associated with antioxidant activity. Furthermore, Xiao et al., [42] found that higher intakes of lutein/zeaxanthin and vitamin E are associated with decreased risk of cataract.

In diabetes mellitus, various ROS can be generated in the lens through many pathways. The elevated glucose in the aqueous humor in the presence of transition metals leads to the production of superoxide radical (O2 _ ) through autoxidation reactions between glucose and oxygen. Glucose may also induce glycation of lens proteins that can generate O2 .- and concurrently accelerate the formation of advanced glycation end-products (AGEs). [43] Moreover, the produced AGEs may, in turn, contribute in the generation of O2 _ and hydrogen peroxide (H 2 O 2 ) in the lens. [44] Furthermore, the flux of glucose through the polyol pathway may contribute to a loss of antioxidants, which is further aggravated by the glycation and inactivation of lens antioxidant enzymes such as the superoxide dismutases. [45]

The data in this study showed reduction of serum glucose for all treated groups compared with positive control. Since the level of blood glucose in diabetic cataract group was 282.38±36.9, decreased in all treated groups as shown in [Table 2]. The reduction in glucose levels may be due to hypoglycemic activity of the cactus juice on diabetic-induced rats. Feugang et al.[46] found that, the combination of insulin and purified extract of cactus reduced blood glucose and glycated hemoglobin levels to normal. Moreover, it has been demonstrated that the hypoglycemic effect of the cactus is useful in the treatment of type 2 diabetes mellitus. Furthermore, Alarcon-Aguilar et al.[47] reported that oral dose of prickly pear cactus extract (1 mg/kg b.w./day) is necessary to control diabetes.

Preventive antioxidant such as (CAT), superoxide dismutase (SOD) are the first line of defense against ROS. Hegde and Varma [48] reported that, GSH is especially abundant in the lens where it plays a vital role as a first line of defense against ROS. It has been demonstrated that lenses from diabetic animals show a loss of GSH that is aggravated by exposure to further oxidative stress. Identically, the dominant superoxide dismutase isoenzyme SOD1 in the lens plays a vital role as a first line of defense against ROS. It has been demonstrated that the loss of this enzyme may result in cell damage and more prone to photochemical cataract. [49] The assessment of GSH and SOD has therefore become an appreciated method for evaluating oxidative damage in the lens. Therefore, in the present study the level of GSH and the activities of SOD antioxidant enzyme, in addition to lipid peroxidation as malonaldehyde (MDA) in blood and lens were studied to explore the effects of cactus fruit juice on oxidative stress. Diabetes was found to induce an increase in the lipid peroxidation indicated by elevated levels of MDA compared to control [Table 2] and [Table 3]. Concurrently, the level of GSH and the activity of SOD were found to be significantly lowered in diabetic rats compared to control [Table 2] and [Table 3]. The regular ingestion of cactus fruit juice restored the level of GSH and the activity of SOD enzyme and reduced the peroxidation of lipids [Table 2] and [Table 3] demonstrating the beneficial roles of the cactus fruit juice. This can be ascribed to the presence of significant amounts of various antioxidants compounds in the cactus fruit juice.

Samuel and Johncy [34] illustrated the prevalence of oxidative stress in diabetes by a highly significant increase in the concentration of MDA in comparison to the control subjects. Moreover, in poorly controlled diabetes mellitus, glucose oxidation through the pentose phosphate pathway leads to an excessive formation of NADPH, which in turn can promote lipid peroxidation. The results of the present study show that, daily supplementation with concentrated cactus pear juice especially at level 3 ml/day for 8 weeks reduces oxidative damage and greatly improves the oxidative stress status in diabetic rats. The experimental evidence includes remarkable reductions, in both serum and lens markers of oxidative damage to lipids, such as MDA.

Apoptosis is identified by FasL/Fas complex. The FasL is formed of a surface protein with trans-membrane domain. Pro-apoptotic markers elevate in the presence of microvascular complications of diabetes. [50] Clinical trials suggest that in human islets, high glucose may modulate the balance of proapoptotic and antiapoptotic proteins toward apoptosis. [51] Brewer et al.[52] concluded that Arizona prickly pear cactus effectively inhibited cell growth in several different immortalized and cancer cell cultures in vitro and suppressed tumor growth.

Our data indicated that, diabetic group have significantly higher level of serum FasL (645±25.0 Pg/ml) when compared to control group (370±20.0 Pg/ml). This may reflect the wide spread cell wall death. Our data suggested that the higher state of apoptosis and hyperglycemia are markers associated with diabetic cataract and also reported that cactus pear may inhibit apoptosis.

In addition to O2 .- and H 2 O 2 , other ROS such as nitric oxide (NO . ) may also be elevated by diabetic conditions. [53] Our results indicated that, diabetic group have significantly higher levels of nitric oxide in the lens compared to the negative control group [Table 3]. Also, the diabetic group showed elevated levels of NO. in the serum compared to the negative control [Table 2]. Our data was in agreement with Ornek et al.[53] who found that the levels of nitric oxide (NO) may, for instance, be increased in the diabetic lens, which may increase peroxynitrite formation. The treatment with different doses of cactus pear juice significantly decreased the levels of NO comparing to diabetic group in both serum and lens [Table 2] and [Table 3]. Concerning to NO level, the decrease could be attribute to the antioxidant activity of the juice contents.

In conclusion, this investigation showed the potential value of opuntia cactus fruit juice as a good source of natural antioxidants, which have a protective action against cataract development. The regular ingestion of concentrated cactus fruit juice especially at level of 3 ml/day for 8 weeks reduced blood sugar level, oxidative damage, and peroxidation of lipids and greatly restored the activity of antioxidant enzymes.

 
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  [Table 1], [Table 2], [Table 3]



 

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