Comparative study between the effects of some dietary sources and metformin drug on weight reduction in obese rats

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The research aimed at comparative study between brown rice, germinated brown rice, and oat and metformin on overweight reduction in obese rats of lipid profiles (total cholesterol, triglycerides, low density lipoprotein (LDL-c), high density lipoprotein (HDL-c) and very low density lipoprotein (VLDL-c)) and liver function (Aspartate Aminotransferase (AST) and Alanine Aminotransferase (ALT)) in rats.

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Nội dung Text: Comparative study between the effects of some dietary sources and metformin drug on weight reduction in obese rats

Annals of Agricultural Science (2015) 60(2), 381–388 H O S T E D BY Faculty of Agriculture, Ain Shams University Annals of Agricultural Science www.elsevier.com/locate/aoas Comparative study between the eﬀects of some dietary sources and metformin drug on weight reduction in obese rats Zenab M. Mosa a,*, Y.A. El Badry a, Hala S. Fattah b, Eman G. Mohamed a a Nutrition and Food Sciences, Home Economics Dept., Fac. of Specific Education, Ain-Shams University, Egypt b Biochemistry and Nutrition Dept., Fac. of Women, Ain-Shams University, Egypt Received 18 October 2015; accepted 2 November 2015 Available online 30 December 2015 KEYWORDS Abstract The worldwide obesity epidemic has produced profound effects on public health. Grain Obesity; such as rice and oat may offer some protection against the early stage of obesity and the develop- Brown rice; ment of complications. The research aimed at comparative study between brown rice, germinated Oat; brown rice, and oat and metformin on overweight reduction in obese rats of lipid profiles (total Metformin; cholesterol, triglycerides, low density lipoprotein (LDL-c), high density lipoprotein (HDL-c) and Lipid profiles; very low density lipoprotein (VLDL-c)) and liver function (Aspartate Aminotransferase (AST) Liver function and Alanine Aminotransferase (ALT)) in rats. This work was carried out on 60 adult male white albino rats (Sprague-Dawley strain) randomly classified into ten groups. The results indicate that the statistical analysis referred that the positive control group was significantly increased in feed intake, triglycerides, HDL/LDL-cholesterol and VLDL-cholesterol comparing with group (3) (188.43 g and 98 g), (123.8 mg/dL and 117.3 mg/dL), (5.42 mg/dL and 0.439 mg/dL), (24.767 mg/dL and 23.467 mg/dL). On the other hand, group (6) in the relative weight heart, kidney and liver was significantly decreased comparing with positive control group (0.417 g and 0.517 g–0.8 g and 1.15 g–3.51 g and 5.65 g). Data represented showed that the significant increase in positive control groups comparing with group (4) of total lipids and glucose (208 mg/dL and 193.3 mg/dL) and (97.5 mg/dL and 76.5 mg/dL), while the positive control group was significantly increased in total cholesterol, HDL-cholesterol, ALT and AST comparing with group (6) (84.333 mg/dL and 56.333 mg/dL), (18.5 mg/dL and 7.167 mg/dL), (23.16 U/L and 13.5 U/L), and (130.5 U/L and 48.7 U/L). Ó 2015 Production and hosting by Elsevier B.V. on behalf of Faculty of Agriculture, Ain Shams University. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/ licenses/by-nc-nd/4.0/). Introduction * Corresponding author. E-mail address: Dr.Zenab@yahoo.com (Z.M. Mosa). The worldwide obesity epidemic has produced profound Peer review under responsibility of Faculty of Agriculture, Ain-Shams effects on public health. Greater than two-thirds of American University. adults are currently reported to be overweight or obese (Flegal http://dx.doi.org/10.1016/j.aoas.2015.11.001 0570-1783 Ó 2015 Production and hosting by Elsevier B.V. on behalf of Faculty of Agriculture, Ain Shams University. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
382 Z.M. Mosa et al. et al., 2008, 2012). In addition to increasing the incidence of control, a high fat diet; and GBR, a high fat diet plus 0.15% heart disease, stroke, and type 2 diabetes (T2D), epidemiologic GBR methanol extract for 7 weeks. GBR administration sig- studies have linked the risk of several types of cancer to both nificantly decreased body weight gain and lipid accumulation obesity and insulin resistance (Gilbert et al., 2013; Hursting in the liver and epididymal adipose tissue as compared to the et al., 2012). Type 2 diabetes taking metformin (an oral anti- HFD control group. In addition, serum triglycerides (TGs) hyperglycemic drug) were reported to have a reduced risk of and total cholesterol (TC) levels were significantly decreased cancer (Franciosi et al., 2013), sparking a flurry of research by following GBR administration compared with those in investigating metformin as an antineoplastic agent in a variety the HFD control group, whereas the high-density lipoprotein of obesity-associated tumor types (Mahmood et al., 2013; (HDL) cholesterol level increased. GBR administration sup- Quinn et al., 2013). pressed body weight gain and lipid accumulation in the liver Obesity is associated with many deleterious changes of lipid and epididymal adipocytes, and improved serum lipid profiles, metabolism: increased low-density lipoprotein cholesterol in part, by controlling adipogenesis through a reduction in (LDL-c), very low-density lipoprotein cholesterol (VLDL-c), transcriptional factors. These results suggest that GBR is a triacylglycerols (TG) and reduced high density lipoprotein potential agent against obesity. cholesterol (HDL-c) concentrations (Poirier et al., 2006). Obesity and oat is an independent risk factor for the devel- HDL plays an important protective role against atherosclerosis opment of coronary artery disease and also exacerbates other and CVD. The anti-atherogenic properties of HDL include the CHD risk factors such as dyslipidemia, high blood pressure, promotion of cellular cholesterol efflux and reverse cholesterol and elevated blood glucose. Observational studies show that transport (RCT), as well as antioxidant, anti-inflammatory and patients who lose weight show an improvement in coronary anti-coagulant effects (Bergouignan et al., 2010). No significant risk profile. Maintaining healthy weight with oats Epidemio- relation was found between AST and ALT in normal, over- logical and clinical data suggest that fiber can aid in weight weight and obese individual (Das et al., 2014). maintenance and/or the prevention of weight gain and subse- Nevertheless, the use of metformin among overweight and quent obesity (>30% over ideal body weight (Brochu et al., obese non-diabetic children and adolescents is steadily increas- 2000). ing in clinical practice despite the fact that this drug has not Oat bran decreased the total cholesterol level in serum, and been authorized for this indication and that the literature on decreased the cholesterol and TG contents in the liver its efficacy and safety is inconsistent (Bouza and Ruiz, 2013). (Grajeta, 1999). Compared with the other gums, oat effectively Thus, the results of a number of systematic reviews ranged reduced both the serum and hepatic lipids (Oda et al., 1994). from reporting the absence of any significant efficacy The whole-grain oat cereal reduced LDL-c more than the (McKeown et al., 2004) to reporting modest favorable effects low-fiber foods for adults with overweight and obesity (Maki on BMI (Park et al., 2009) that are limited to some adolescents et al., 2010). Oat-derived beta-glucan increased HDLc, while with clinical resistance to insulin or pre-diabetes. Most of them diminished LDLc and non-HDL cholesterol levels in over- agreed that more data are necessary to determine the role of weight individuals with hypercholesterolemia (Reyna- metformin in the management of pediatric obesity (Quinn Villasmil et al., 2007). It was reported that high beta-glucan et al., 2010). contained oat bran and oat gum, reduced postprandial serum Rice is generally consumed after it is refined to remove the glucose and insulin in both the control and type 2 diabetic sub- outer bran and germ portions of the intact grains (i.e. brown jects (Braaten et al., 1994). In streptozotocin-induced diabetic rice, BR) and produce white rice (WR), consisting primarily mice, oat significantly decreased fasting blood glucose, glyco- of the starchy endosperm. The postprandial blood glucose sylated protein, and free fatty acid content, while inhibited responses elicited on consumption of WR or BR are substan- pancreatic apoptosis (Shen et al., 2011). tially different (Foster-Powell et al., 2002). Whole grains have The research aimed at comparative study between brown been shown to be associated with a low fasting insulin level rice, germinated brown rice, and oat, and metformin on over- and a low glycemic response after meal ingestion (McKeown weight reduction in obese rats. et al., 2004). The intake of whole grains, but not of refined grains, has also been reported to be associated with low body weight and adiposity (Tighe et al., 2010; Nettleton et al., 2010). Materials and methods Thus, the intake of whole-grain BR might be beneficial for controlling weight and obesity. Recently, we have reported Materials that BR and g-oryzanol, one of its major components, improve high-fat diet-induced metabolic derangement and attenuate the Chemicals and drugs: preference for dietary fat, by decreasing hypothalamic endo- plasmic reticulum stress (Kozuka et al., 2012). Therefore, we (1) Chemical reagents. All chemical reagents used were hypothesized that BR may be useful for ameliorating obesity purchased from EL Nasr Pharmaceutical chemicals and the metabolic syndrome, a constellation of obesity-based Ind., Cairo, Egypt. They were used without further metabolic abnormalities (glucose intolerance, insulin resis- purification. L-cysteine choline chloride, Thiamine tance, dyslipidemia and hypertension, all well-documented risk HCL, and vitamin B1 (>99%) were purchased from factors of CVD), by regulating eating behavior (Shimabukuro Sigma Aldrich Ind. company. Vitamin K, A and E, et al., 2014). D-Biotin was purchased from Kahira Pharm., Cairo, Ho et al. (2012) showed anti-obesity effect of GBR on high Egypt. Riboflavin, pyridoxine, and folic acid were fat induced-obese mice. The mice were divided into three obtained from Nile pharmaceutical Ind., Company, groups and were administered ND, a normal diet; HFD Cairo, Egypt.
Effects of some dietary sources and metformin drug on weight reduction 383 (2) Metformin 850 mg tablets were purchased from EL parameters. Blood samples were collected from the orbital Nasr Pharmaceutical chemicals. Ind., company, abo sinus veins by heparinized capillary tubes and immediately zabal, calyobia, Egypt. It was given via oral gavage transferred into tube without anticoagulant. Blood was cen- (5 mg/kg) of body weight. trifuged at 3500 rpm after coagulation. Serum samples were (3) Starch, Powdered sucrose, lard, oat and corn oil from dried into Eppendorf tubes (1–5 ml) and kept at 25 °C for local market, Cairo, Egypt. further analysis. After collection of blood sample, animals (4) Brown rice obtained from farmers in Shibin el-Qanater, were scarified by cervical dislocation, Liver and kidney adipose Elqalyoubeyah. tissues were removed, washed by saliva solu hiv, dried, and weighed to determine organ relative weight to the body (g Preparation of Brown Rice (BR): organs/100 g animal live body weight according to Drury Brown rice was purified, washed, ground and sieved then and Wallington (1980). stored at 20 °C. Adiposity index (%): Preparation of Germinated Brown Rice (GBR): The adiposity index was calculated as 100 times the quo- Germinated brown rice (GBR) was carried out as previ- tient of the sum of the epididymis and retroperitoneal fat ously described by Suzuki and maekawa (2000) with a slight deposits (g). modification. Four kilograms of brown rice was soaked in water, and water was changed every 6–7 h. This step was Adiposity index: (total abdominal fat 100/body weight) repeated for 3 consecutive days. The GBR obtained was dried, Hepatosomatic index (%) = (liver weight 100/body grounded and kept in airtight containers at 20 °C till demand. weight) Biological investigation: Thirty six Male albino rats (Sprague–Dawley Strain) weigh- ing approximately 150 ± 20 g were used and obtained from Methods Helwan station for experimental animals Helwan, Cairo, Egypt. Healthy animals were randomized, housed in plastic Biological evaluation cages and maintained in air-conditioned room at 12 h Biological evaluation of the different tested diets was carried light/dark cycle at 20 ± 5 °C in the animal house of research out by determination of food intake (FI), everyday by sub- institute of ophthalmology. They were kept under normal tracting the residual and refusal diet from served diet. healthy conditions and fed on the Basel diet without any treatment for one week for acclimatization. Experimental diet Food intake (g) = diet supply (residual diet + refusal diet) and water were offered ad libitum all over the experimental period. The animals were weighed weekly to monitor the body Diet: weight changes. The fed efficiency ratio (FER) was calculated as described by equation of Guo (2002). 1. Basal diet (BD) Biochemical analysis of serum The experimental diet used in the present study was the bal- Determination of Serum Cholesterol: anced diet prepared according to Reeves et al. (1993). Serum cholesterol was determined according to the method described by Fossati and Principe (1982). 2. High fat diet (HFD) Determination of Serum Triglycerides (TG): Serum TG were determined using the enzymatic colorimet- For induction of obesity, the rats were fed a high fat diet, ric procedure according to the method described by Fossati which was prepared according to Reeves et al. (1993). Diet and Principe (1982). was freshly made every week and stored at 4 °C. Determination of High density lipoprotein cholesterol Experimental design: (HDL-c) and low density lipoprotein cholesterol (LDL-c): Thirty six rats were divided into six groups, six rats each as Determination of HDL-c and LDL-c in serum followed the follows: colorimetric method of Friedewald et al. (1972). Calculation of very low density lipoprotein cholesterol Group (1): (negative control) fed on basal diet. (VLDL-c): Group (2): (positive control) fed on high fat diet. Serum Very low density lipoprotein cholesterol (VLDL-c) Group (3): fed on high fat diet and metformin (5 mg/kg/day). was calculated following the method of Arcoll (1997). Group (4): fed on high fat diet and brown rice (20%). Calculation of the risk factor (LDL-c/HDL-c ratio): Group (5): fed on high fat diet and germinated brown rice The risk ratio of LDL-c/HDL-c was calculated as described (20%). by Notarnicola et al. (2005). Group (6): fed on high fat diet and oat (20%). Determination of Alanine Aminotransferase (ALT) and Aspartate Aminotransferase (AST): The clinical monitoring of the animals was performed to Serum ALT and AST activity was determined according to evaluate body weight, food intake and blood glucose concen- the method described by Reitman and Frankel (1975). tration every week. At the end of the experimental period Determination of Serum Glucose: (10 weeks), rats were fasted overnight and once the time and Glucose was determined in the serum according the method blood samples were taken for the determination of biochemical described by Trinder (1969).
384 Z.M. Mosa et al. Statistical analysis comparing with group (6) which were 167.6 g and 106.6. On the other hand, the body weight gain in group (4) was lower Statistical analysis was performed using computer program; than positive control group which was 30.56% and 32.69%. SPSS (1996). One-way analysis of variance (ANOVA) and The results agreed with those obtained by Thamer (2014). Duncan multiple range were used to illustrate significant Means of relative organs weight in rats suffering from obe- p-value 30% over medical conditions such as type 2 diabetes and coronary heart ideal body weight (Rossner, 1992). While the muscle fats in disease (Van Gaal et al., 2006). Traditionally, the increase in group (5) were lower than those in positive control group obesity is attributed to an increased calorie intake and a con- (1.883 g and 2.7 g). It is a potent anti-hyperglycemic and comitant significant reduction in physical activity and energy insulin-sensitizing drug that works by decreasing hepatic glu- expenditure (Prentice, 2001). coneogenesis, activating insulin receptor tyrosine phosphoryla- The results of Table 1 indicate that the statistical analysis tion (Viollet et al., 2012), decreasing intestinal glucose referred that the positive control group was significantly absorption, and increasing skeletal muscle and adipose tissue increased in feed intake comparing with group (3) which were glucose uptake (del Barco et al., 2011). Moreover, metformin 188.43 g and 98 g. Data of the same table showed that the pos- increases the more active mitochondria-bound hexokinase and itive control group was significantly increased in initial weight actin-bound phosphofructokinase in streptozotocin-induced Table 1 Means of feed intake (g) and body weight gain (%) in rats suffering from obesity fed on metformin, brown rice and oat. Groups Parameter Feed intake Initial weight Final weight Body weight gain% b a c Group (1) 118 174.5 179 2.51d Control ( ve) basal diet Group (2) 188.43b 167.6b 249a 32.69b Control (+ve) high fat diet Group (3) 98c 158.3c 244a 35.128b High fat diet and metformin Group (4) 358a 152.5c 219.6b 30.56c High fat diet and brown rice Group (5) 182.25b 137.2c 211.5b 35.13b High fat diet and germinated brown rice Group (6) 244a 106.6d 268.7a 60.33a High fat diet and oat Numbers followed by the same letter in the same column do not differ significantly by Duncan’s multiple rang test (p > 0.05). Table 2 Means of relative organs weight (g) in rats suffering from obesity fed on metformin, brown rice and oat. Groups Relative weight of organs Heart Kidney Liver Muscles fats Fats Group (1) 0.383c 1.517a 4.033c 0.217d 0.333c Control ( ve) basal diet Group (2) 0.517b 1.15b 5.65a 2.7b 2.433a Control (+ve) high fat diet Group (3) 0.867a 1.55a 8.133a 5.917a 0 High fat diet and metformin Group (4) 0.517b 1.333b 5.183b 2.033b 1.117b High fat diet and brown rice Group (5) 0.683a 0.983c 4.267b 1.883c 1.6b High fat diet and germinated brown rice Group (6) 0.417b 0.8c 3.517d 2.567b 2.167a High fat diet and oat Numbers followed by the same letter in the same column do not differ significantly by Duncan’s multiple rang test (p > 0.05).
Effects of some dietary sources and metformin drug on weight reduction 385 Table 3 Means of plasma total lipids (mg/dL) in rats suffering from obesity fed on metformin, brown rice and oat. Groups Parameter Total lipids Triglycerides Total cholesterol c d Group (1) 186.2 97 88.833a Control ( ve) basal diet Group (2) 208.2b 123.8b 84.333b Control (+ve) high fat diet Group (3) 201.8b 117.3bc 84.333b High fat diet and metformin Group (4) 193.3c 123.7b 68.833c High fat diet and brown rice Group (5) 287.8a 202.8a 84.667b High fat diet and germinated brown rice Group (6) 253a 196a 56.333d High fat diet and oat Numbers followed by the same letter in the same column do not differ significantly by Duncan’s multiple rang test (p > 0.05). Table 4 Means of cholesterol fractions (mg/dL) in rats suffering from obesity fed on metformin, brown rice and oat. Groups Parameter HDL-cholesterol LDL-cholesterol (HDL/LDL)-cholesterol VLDL-cholesterol Group (1) 25a 44.433a 0.596ab 19.4c Control ( ve) basal diet Group (2) 18.5b 41.067a 0.542b 24.767b Control (+ve) high fat diet Group (3) 16.8b 44.033a 0.439b 23.467b High fat diet and metformin Group (4) 17.8b 26.267b 0.723a 24.733b High fat diet and brown rice Group (5) 29.3a 14.767c 0.967a 40.567a High fat diet and germinated brown rice Group (6) 7.167c 11.633c 0.592ab 39.2a High fat diet and oat Numbers followed by the same letter in the same column do not differ significantly by Duncan’s multiple rang test (p > 0.05). diabetic male Swiss mice hearts, enhancing glucose sensitivity insulin secretion in humans (Ito et al., 2005). Dietary pre- of those organs (da Silva et al., 2012). The relative weight of germinated brown rice (PGBR) as well as brown rice (BR) fats in group (4) decreased significantly than that in the posi- had effect on hyperlipidemia and cholesterol metabolism by tive control group (1.117 g and 2.433 g). The reduced liver improving abnormal serum lipoprotein profiles; (VLDL enzymes in the GBR group, however, may have been indicative + LDL)-cholesterol, leading to significant reduction in total of hepatocytes’ protection and/or regeneration. Usuki et al. cholesterol level (Miura et al., 2006). The same table shows (2007) and Katz et al. (2001) showed that Obesity is associated that the total cholesterol in the positive control group was sig- with a great diversity of diseases including non-alcoholic fatty nificantly increased comparing with group (6) (84.333 mg/dL liver disease. Our recent report suggested that oat, rich in beta- and 56.333 mg/dL). Oat could improve obesity, body fat, glucan, had a metabolic-regulating and liver-protecting effect serum parameters and liver lipid metabolism. In high-fat-diet in an animal model. In this study, we performed a clinical trial (HFD)-fed rats, oat effectively reduced body weight and fat, to further confirm the effect of oat. Research on other heart and decreased food efficiency but not appetite. Oat lowered healthy components of oats continues to emerge. serum glucose, free-fatty-acid (FFA), triacylglycerol (TG), The data in Table 3 show that the positive control group cholesterol, and LDL-c/HDL-c elevated by HFD, and dose- was significantly increased in total lipids comparing with group dependently reduced hepatic TG and cholesterol. Thus, Oat (4) (208 mg/dL and 193.3 mg/dL). Forcheron et al. (2009) and could act as adjuvant therapeutics for metabolic disorders Lin et al. (2000) proved that the metformin has improved liver via attenuating obesity, body fat, and improving serum param- TG content in some rodent models of diabetes and NAFLD. eters with metabolic regulation and lipid clearance of liver On the other hand, the triglycerides in group (3) were signifi- (Chiung-Huei et al., 2013). cantly decreased comparing with the positive control group Data present in Table 4 indicated that there was significant (117.3 mg/dL and 123.8 mg/dL). Pre-germinated brown rice increase in positive group comparing to group (6) in the was better than white rice to prevent the rapid increase of HDL-cholesterol and LDL-cholesterol and the values were postprandial blood glucose concentration without increasing 18.5 mg/dL and 7.167 mg/dL, and 41.067 mg/dL and
386 Z.M. Mosa et al. Table 5 Means of glucose (mg/dL) and liver function (U/L) in rats suffering from obesity fed on metformin, brown rice and oat. Groups Parameter Glucose (mg/dL) ALT (U/L) AST (U/L) c c Group (1) 88.5 19.167 109.7c Control ( ve) basal diet Group (2) 97.5b 23.167b 130.5a Control (+ve) high fat diet Group (3) 108.8a 22b 113.3b High fat diet and metformin Group (4) 76.5d 39.3a 113.7b High fat diet and brown rice Group (5) 118.2a 13.7c 91.8c High fat diet and germinated brown rice Group (6) 81.3b 13.5c 48.7d High fat diet and oat Numbers followed by the same letter in the same column do not differ significantly by Duncan’s multiple rang test (p > 0.05). 11.633 mg/dL. Such result was in agreement with that obtained rats. It could develop the retarded liver function and lipid pro- by Miura et al. (2006). Oats were significantly hypocholes- file of through supplemented the meal of oat whereas main- terolemic, lowering total and LDL-cholesterol by 2–23%. Oats taining healthy weight with oats Epidemiological and clinical do not reduce cholesterol by displacing fat and cholesterol data suggest that fiber can aid in weight maintenance and/or intake (Ripsin et al., 1992). On the other hand, the HDL/ the prevention of weight gain and subsequent obesity over LDL-cholesterol and VLDL-cholesterol were significantly ideal body weight. decreased in group (3) comparing to positive control group (0.439 mg/dL and 5.42 mg/dL) and (23.467 mg/dL and 24.767 mg/dL). The diets including pre-germinated brown rice References (PGBR) may be useful to control blood glucose level, improved serum total cholesterol and triglyceride. At equal Arcoll, D., 1997. (National Department of Agriculture, Elsenburg) dietary levels, a˜-oryzanol has greater effect on lowering plasma Provided Invaluable Information. Monsanto Allocated Plots for LDL-cholesterol and rising plasma HDL-cholesterol (Wilson the Study at Bapsfontein. et al., 2007). 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