Lipidemic, glycemic and organ protective actions of tea seed oil in rats fed with high fat and high carbohydrate diet

Warinna Pinthong1,*,#, Thamolwan Suanarunsawat2, Watcharaporn Devakul Na Ayutthaya3namra3*

1Biomedical Sciences Graduate Program, Department of Medical Sciences, Faculty of Science, Rangsit University, Thailand

2Physiology Unit, Department of Medical Sciences, Faculty of Science, Rangsit University, Thailand

3Pharmacology and Toxicology Unit, Department of Medical Sciences, Faculty of Science, Rangsit University, Thailand

*,#e-mail:

Abstract

The present study was conducted to investigate the lipidemic, glycemic and organ protective effects of tea seed oil (TSO) in rats fed with high fat and high carbohydrate (HFHC) diet. Three groups of male Wistar rats were used including normal control group, group fed with HFHC diet (cholesterol + lard + fructose) for three months, and HFHC group treated with TSO. At the end of the experiment, serum lipid profile, blood glucose, oral glucose tolerance test (OGTT), serum AST, ALT, LDH, CK-MB, creatinine and BUN were determined. Individual fatty acid contents in TSO were assayed by Gas chromatography. The results showed that oleic acid was the primary fatty acid in TSO (83.36%). HFHC diet increased serum lipid profile and atherogenic index (AI). The high serum levels of lipid profile and AI were decreased in HFHC rats treated with TSO. The elevation of area under the curve of OGTT was alleviated by TSO. TSO also normalized the high serum levels of AST, ALT, LDH, CK-MB, creatinine and BUN. It can be concluded that TSO was able to decrease the high serum levels of lipid profile and high blood glucose level of OGTT in rats fed with HFHC, indicating its therapeutic potency to prevent atherosclerosis and hyperglycemia. It also protects liver, heart and kidney in HFHC. Oleic acid content in TSO might be responsible for these activities.

Keywords: tea seed oil, high fat and high carbohydrate diet, liver function, cardiac function, fructose

Introduction

Hyperlipidemia and hyperglycemia are widely known to be the major risk factor for the development of atherosclerosis, ultimately causes coronary artery disease [1, 2]. The modern life style with high fat and high carbohydrate diet and less physical activity are the significant causes of hyperlipidemia and hyperglycemia. Hyperlipidemia and hyperglycemia have been found to induce oxidative stress in various organs such as liver, heart and kidney [3, 4]. Since synthetic hyperlipidemia and hyperglycemia drugs cause several adverse effects especially liver damage, searching for natural products that have less or no side effects has been increasing. Among many kinds of medicinal plants available in Thailand, Camellia oleifera Abel. oil (tea seed oil, TSO) is promising for hyperlipidemia and hyperglycemia drugs since it has several outstanding properties such as high smoking point, stable, and high nutritional contents, especially Vitamin E, and high unsaturated fat which is useful for human foods [5]. TSO is extensively used as cooking oil in several countries including China and Thailand. Tea seed oil has been shown to lower serum lipid profile [6, 7] and protected vital organs in normal and several stress conditions as reported earlier [8, 9, 10]. However, no experimental study to elucidate its effects on serum lipid profile and blood glucose in subjects fed with high fat and high carbohydrate diet has been reported. Therefore, the present study was conducted to investigate its lipidemic, glycemic and organ protective effects in rats fed with high fat and high carbohydrate diet.

Methodology

1. Animal preparation

Male Wistar rats weighing between 180-220 g from the National Laboratory Animal Centre, Mahidol University, Salaya, Nakornprathom, Thailand were used in the study. The animals were housed in the animal facility of the Faculty of Science, Rangsit University under standard conditions of temperature (25±2°C), 50-60% of humidity and 12 h/12 h light/dark cycles. Food and water were given ad libitum. High fat and high carbohydrate (HFHC) diet was prepared by adding 2 g% cholesterol powder along with 10% lard in normal diet, and 60% fructose powder mixed in drinking water. Body weight and food consumption were recorded weekly in all groups. Three groups of seven rats each were fed on the following diet for three month: group I, normal diet for a control; group II, a high fat and high carbohydrate (HFHC) diet; and group III, HFHC diet treated with TSO was orally administered once a day at the dose of 5.69 g/kg BW/day for the last three months. This dose has been chosen because of its anti-oxidative effect to protect liver against CCl4 [10]. In addition, it is the average dose that showed blood lipid lowering in previous reports [7, 11]. The tea seed oil was bought from the local market.

2. Experimental protocol

2.1 Effect of tea seed oil on blood glucose and oral glucose tolerance tests in rats fed with HFHC diet

After 3 months of normal or HFHC diet feeding, the rats were fasted overnight. Blood was collected from rats’ tail to determine fasting blood glucose (FBG) using automatic glucometer (One Touch Ultra, Lifescan, CA, USA). Oral glucose tolerance test was evaluated by feeding 2 g/kg BW of 50% glucose solution. After glucose loading, blood was collected from the tail to determine blood glucose every 30 min for 120 min and the rats were anesthetized by intraperitoneal injection with zolitil (40 mg/kg BW) plus xylazine (3 mg/kg BW).

2.2 Effect of tea seed oil on serum lipid profile in rats fed with HFHC diet

At the end of the experiment, the rats were fasted overnight, and were anesthetized by intraperitoneal injection with sodium pentobarbiturate (60 mg/kg BW). Blood was collected from abdominal vein. Serum was separated by refrigerated centrifuge at 3000 rpm, 4°C for 5 min for determination of serum lipid profile including total cholesterol (TC), triglyceride (TG), high density lipoprotein cholesterol (HDL-C) and low density lipoprotein cholesterol (LDL-C).

2.3 Organ protective effect of tea seed oil in rats fed with HFHC diet

At the end of the experiment, the rats were fasted overnight, and were anesthetized by intraperitoneal injection with sodium pentobarbiturate (60 mg/kg BW). Blood was collected from abdominal vein. Serum was separated by refrigerated centrifuge at 3000 rpm, 4°C for 5 min. Liver damage was evaluated by determination of serum alanine aminotransferase (ALT), aspartate aminotransferase (AST). Cardiac damage was also assessed by determination of serum lactate dehydrogenase (LDH) and creatine kinase MB subunit (CK-MB). Renal function was evaluated by determination of serum creatinine and blood urea nitrogen (BUN).

2.4 Biochemical Assay

The total serum levels of total cholesterol, triglyceride and HDL-C were assayed by using an enzymatic kit (Gesellschaft für Biochemica und Diagnostica GmbH, Germany). LDL-C was calculated by using the equation: LDL-C = [TC-(HDL-C)]-(triglyceride/5). The serum levels of AST, ALT, LDH, and CK–MB were measured by using an enzymatic kit (Randox Laboratories, UK). Total cholesterol and triglyceride contents in the liver and feces were determined using enzymatic kit.

3. Statistical Analysis

All values were presented as means ± SEM. The results were analyzed by ANOVA. Duncan multiple rank test was performed to determine statistical significance among groups by using SPSS software version 11.5. Significant difference was accepted at p < 0.05.

Results

Table 1 and Figure 1 showed that basal blood glucose was slightly increased in rats fed with HFHC diet but the level was not significantly different from normal rats. TSO treatment slightly decreased basal blood glucose but the level was not significantly different from HFHC rats.

In contrast, area under the curve (AUC) of oral glucose tolerance test (OGTT) was significantly increased in rats fed with HFHC diet as compared to normal rats. The high level of AUC was significantly lowered in HFHC rats treated with TSO (Table 2 and Figure 2).

The serum levels of total cholesterol, triglyceride, HDL-C, LDL-C and atherogenic index (AI) were shown in the Table 3 and Figure 3. Three months of HFHC diet feeding significantly increased serum total cholesterol, triglyceride, LDL-C and AI whereas HDL-C was slightly decreased. TSO treatment significantly decreased the levels of total cholesterol, triglyceride, LDL-C, and atherogenic index (AI) in HFHC rats.

The serum levels of AST, ALT, LDH, CK-MB, creatinine, and BUN were shown in Table 4. Three months of HFHC diet feeding significantly increased serum levels of AST, ALT, LDH, CK-MB, creatinine, and BUN. The high levels of AST, ALT, LDH, CK-MB, and BUN were significantly decreased in HFHC rats treated with TSO.

Discussion and Conclusion

It has been widely known that elevation of hyperlipidemia and hyperglycemia can lead to atherosclerosis; blood supply to the organs gradually diminishes until organ function becomes impaired. Several lines of evidence show that the improvement and incidence of atherosclerosis and coronary artery disease are associated with lowering hyperlipidemia [1, 2] and hyperglycemia [3]. To treat hyperlipidemia and hyperglycemia, extensive interventions are recommended, including diet control and exercise. Hyperlipidemia and hyperglycemia drugs can cause several adverse effects especially liver damage indicating the need to find other safer yet effective alternatives [12, 13]. Therefore, herbal medicines might be an effective, safe, and low-cost therapy. Camellia oleifera Abel. oil (TSO) is very promising due to its therapeutic potency [5]. The present study shows that three months of HFHC diet feeding raised the basal blood glucose but the level was not significantly different from normal rats. TSO treatment slightly decreased basal blood glucose but the level was not significantly different from HFHC rats. In contrast, AUC of OGTT was significantly increased in rats fed with HFHC diet. The substantial increase in the amount of dietary fructose consumption from high intake of sucrose has been linked with a rise in obesity and metabolic disorders. A high flux of fructose to the liver perturbs glucose metabolism and glucose uptake pathways, leads to a significantly enhanced rate of de novo lipogenesis and triglyceride synthesis. Because of its lipogenic properties, excess fructose in the diet can cause glucose and fructose malabsorption, and greater elevations in TG and cholesterol. These metabolic disturbances appear to underlie the induction of insulin resistance or impairment of insulin action commonly observed with high fructose feeding in both humans and animal models and then finally results hyperglycemia [7, 10, 11]. Providing fructose with honey, which is naturally rich in antioxidant substances, prevented both the oxidative stress induced by fructose and the reduction of insulin sensitivity [12]. TSO significantly decreased the high level of AUC in HFHC diet, this implies that TSO was able to stimulate insulin secretion or improves insulin action which then eventually prevents the occurrence of anti-hyperglycemic [13]. Research studies that provide evidence TSO effect of decreased total cholesterol, triglyceride, phospholipid and lipid profile in the liver and heart in human and rat [14, 15]. In the present study, HFHC diet also increased serum lipid profile and atherogenic index (AI). Hyperlipidemia is an important factor in development of atherosclerosis and finally coronary artery disease. HFHC diet caused oxidative stress as shown by marked increment in the levels of thiobarbituric acid reactive substance (TBARS) and reduction of reduced glutathione content, decreased activities of SOD, CAT and GPx in the liver, heart and kidney [16, 17]. TSO treatment attenuated the high serum lipid profile and atherogenic index (AI). This is supported by the increased activities of SOD, CAT and GPx in the liver, heart and kidney. These results suggest that TSO could be effective to alleviate atherosclerosis which eventually prevents the occurrence of coronary artery disease [18]. Free radical-induced lipid peroxidation or oxidative stress has been shown to participate in the pathogenesis of several diseases [19]. In addition, it was shown that activities of antioxidant enzymes increased in both the liver, kidney and cardiac tissues of rats after TSO administration [20, 21]. The liver, heart and kidney are widely known to be the major risk organs for hyperlipidemia and hyperglycemia. In the present study, liver, heart and kidney were damaged as shown by the increased of serum levels of AST, ALT, LDH, CK-MB, creatinine, and BUN in HFHC rats (Table 4). HFHC diet feeding induces lipid peroxidation or oxidative stress to injure the liver, heart and kidney. TSO decreased all these serum marker enzymes. In previous research, TSO showed higher antioxidant enzyme (SOD) activity served as anti-active oxygen species in body tissues. On the other hand, TSO can increase antioxidant enzyme activity [22]. Therefore, TSO may protect the liver, heart and kidney from HFHC diet by which antilipidemic, antiglycemic and antioxidative actions. In previous studies, qualitative analysis of the fatty acid composition of TSO shows that the main fatty acid compositions are relatively stable. It is mainly composed of oleic acid has the effect of lipid-lowering in the blood, reduce lipid peroxidation and increase capacity of antioxidants in the plasma and liver in rat [23, 24]. It has been shown that oleic acid decreased hepatic lipid content whereas increased fecal bile acids excretion without significant change of fecal lipid excretion [25]. In this study, oleic acid (83.36%) was the primary fatty acid in TSO. These results indicate that oleic acid containing in TSO may play important role for these effects.

In summary, consumption of the HFHC diet feeding raised blood glucose, serum lipid profile and AI. The liver, heart and kidney functions were also damaged. TSO was able to decrease the high serum levels of lipid profile and blood glucose in rats fed with HFHC, indicating its therapeutic potency to prevent atherosclerosis and hyperglycemia. TSO also protects liver, heart and kidney. Oleic acid containing in TSO might be responsible for hypolipidemic, hypoglycemic and organ protective activities.

References

1.  Freedman JE. High-fat diets and cardiovascular disease. J Am Col Cardiol 2003;41:1750-1752.

2.  Khoo KL, Tan IT, Liew YM, Deslypere JP, and Janus E. Lipids and coronary heart disease. Asia Arterioscler 2003;169:1-10.

3.  Nathan DM, and Cleary PA. Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications (DCCT/EDIC). Study Research Group, December 2005.

4.  Kwiterovich PO. The effect of dietary fat, antioxidants, and pro-oxidants on blood lipids, lipoproteins, and atherosclerosis. J Am Diet Assoc. 1997;97:S31-S41.

5.  Sahari MA, Ataii D, and Hamedi M. Characteristics of tea seed oil in comparison with sunflower and olive oils and its effect as a natural antioxidant. J Am Oil Chem Soc. 2004;81:585-588.