Key words: Type 2 diabetes mellitus; Resveratrol; Glycosylated hemoglobin; Glimepiride
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1 ORIGINAL ARTICLE Complete title of the manuscript: Efficacy and Safety of Resveratrol as an Adjuvant Therapy in Type 2 Diabetes Mellitus Patients: Result of a Randomized Active Controlled Clinical Study Ojha Rakesh 1*, Kulkarni Pranesh 2, Vyas Bhavin 3 1 PhD Scholar/Research Fellow, 3 Associate Professor Department of Pharmacology, Maliba College of Pharmacy, Uka Tarsadia University, Bardoli, Surat, Gujarat, India, 2 Consulting Physician Vikas Hospital, Rambaug, Kalyan (West), Maharashtra ABSTRCT BACKGROUND: No long term clinical efficacy and safety study of resveratrol as adjuvant therapy along with gold standard therapy has been conducted in type 2 diabetes mellitus (T2DM). The aim of this study was to investigate the efficacy and safety of resveratrol as an adjuvant therapy in newly diagnosed T2DM patients. METHODS: In this randomized active-controlled study, T2DM patients (male/female) aged years were randomized to receive glimepiride 2mg or glimepiride 2mg plus resveratrol 1 gram daily for 12 months. Efficacy variables included change in plasma blood glucose (fasting and postprandial) and glycosylated hemoglobin (HbA1c) from baseline and were followed-up for every 3 months. Treatment-emergent adverse events (TEAEs) were assessed. RESULTS: A total of 60 T2DM patients were analyzed (glimepiride [n=30] and glimepiride plus resveratrol [n=30]). Resveratrol as an adjuvant with glimepiride significantly reduced plasma blood glucose concentration as compared to glimepiride monotherapy during fasting and postprandial conditions (p<0.001). Mean levels of HbA1c were significantly lower in glimepiride plus resveratrol group than glimepiride (p<0.001). Both the study drugs have similar safety profile, and found well tolerable. CONCLUSIONS: Resveratrol plus glimepiride was found to be superior over glimepiride monotherapy in reducing plasma blood glucose concentration (fasting and fed) and significantly improve glycemic control by reducing HbA1c levels in patients with T2DM. Both the study drugs were effective with comparable safety profile. Our study supports the long term clinical efficacy and safety study of resveratrol along with gold standard therapy in T2DM. Key words: Type 2 diabetes mellitus; Resveratrol; Glycosylated hemoglobin; Glimepiride INTRODUCTION Type 2 Diabetes mellitus (T2DM) is a chronic metabolic disorder characterized by increased blood sugar, insulin resistance, and relative lack of insulin. The prevalence of diabetes was 5 percent in urban India whereas 2.8 per cent in rural India. 1 World health organization (WHO) suggests that there were 32 million diabetics in India in 2000 and it is projected that India would have largest number of diabetics (80 million) in the world by Prevalence and economic *Corresponding Author: Dr. Rakesh Ojha Department of Pharmacology, Maliba College of Pharmacy, Uka Tarsadia University, Bardoli, Surat, Gujarat, India Contact No: rakeshojha0712@gmail.com burden related to T2DM have been increasing and are projected to be continued to increase. 3 The oral antihyperglycemic agents for type 2 diabetes included insulin secretion stimulating agents (sulphonylureas and rapid-acting secretagogues), hepatic glucose production reduction agents (biguanides), agents those who delay digestion and absorption of intestinal carbohydrate (alpha-glucosidase inhibitors) and thiazolidinediones groups of agents were improve insulin action. 4,5 The limitations of current therapy are weight gain (eg, sulfonylureas and insulin), and result in weight loss (eg, GLP-1 receptor agonists, pramlintide). 4,5. To manage diabetes mellitus effectively, often combination therapy and adjusting dose of gold standard therapy from low to high is required to prevent mortality. This may results in long term safely issues and 81 Int J Res Med. 2017; 5(4); e ISSN: p ISSN:
2 reduce financial burden to patients and in diabetes treatment and also decrease the their family. The agents that improve financial burden to the patients along with glycemic control along with lowering in good safety profile. Moreover, no long blood lipid levels and blood pressure may term clinical efficacy and safety study of lead to improve in morbidity and mortality Resveratrol in diabetic patient has been is the better options for diabetes treatment. conducted. Based on the above facts, the The combination treatment therapy may proposed clinical study designed to also slow down the natural disease evaluate efficacy and safety of progression and reduces the complications Resveratrol, as adjuvants in patients with associated with the diabetes. To prevent recently diagnosed with type 2 diabetes side effects and financial burden due to mellitus who were stable on anti-diabetic combination therapy and high dose of gold monotherapy. standard therapy, there is need of an METHODS AND MATIREALS effective adjuvant therapy which is free A prospective, randomized, parallel, open from side effects, cost effective and label, comparative, active controlled enhances the efficacy of current gold clinical study was conducted at single standard therapy without the need of study centres in India. From Sep 2014 to switching to aggressive therapy. Also there Aug 2015, 60 patients of either sex of 20- is a need of adjuvant therapy which keeps 65 years who had T2DM and stable us healthy and useful as prophylaxis for monotherapy of glimeperide 2 mg were the patients with risk factor of enrolled. Patients with type 1 diabetes, cardiovascular disease. Resveratrol is a pregnant women, lactating mothers, plant based anti-hyperglycemic agent of history of severe heart disease, hepatic stilbenoid type of natural phenol, and a disease and renal dysfunction, willing to phytoalexin produced naturally by several use other antioxidant supplementation plants 6. The action of resveratrol was rather than resveratrol, grapes allergy and demonstrated in in animal models of regular alcoholics were excluded.. During diabetic rats which resulted in reduced the screening visit on the day before blood glucose level and glycosylated surgery, medical history was obtained; hemoglobin (HbA1C) levels, reflected in physical examination and laboratory sustained reduction of glycaemia This investigations were performed. indicates that the possible use of Medications considered necessary for the resveratrol in combination with current patient and which does not interact with anti-diabetic therapies as adjuvant therapy the study medication were allowed. All would be effective in preventing and patients were explained the procedure treating diabetes. Short term clinical use of clearly and written informed consent from Resveratrol 1 gram/daily (500 mg BD) each participant was obtained before their was found to be effective in decreasing participation in the study. The protocol fasting blood glucose level when was approved by Safety, Health and compared to Placebo after 45 days 11. welfare Ethics committee, registered under Another 4 week pilot clinical study (in 10 DCGI (Reg no: ECR/632/Inst/MH/2014). subjects) revealed no change in fasting The study was conducted in compliance blood glucose and, lipid level after with the Ethical principles of Declaration treatment with resveratrol (1g, 1.5g and of Helsinki; Good Clinical Practices 2g/daily). This study suggested that guidelines issued by the Central Drugs resveratrol improves insulin sensitivity and Standard Control Organization (CDSCO), post-meal plasma glucose reduction in Ministry of Health, Government of India; impaired glucose tolerance patients 12. We Ethical guidelines for biomedical research hypothesized that Resveratrol could be on human participants, Indian Council of one of the adjuvant therapy along with Medical Research (ICMR), New Delhi; gold standard antidiabetic medication, and International conference on which may led to significantly improve harmonisation of technical requirements the effectiveness of gold stardard therapy for registration of pharmaceuticals for 82 Int J Res Med. 2017; 5(4); e ISSN: p ISSN:
3 human use guideline for Good Clinical test was used to find p value. Unpaired t Practices. The trial was registered with / Man Whitney test was used to analyze Clinical Trial Registry-India (CTRI) the quantitative data for between group before initiation of study. Enrolled patients comparisons. Within group comparison were randomized in 1:1 in 2 groups as per was performed using paired t test or the computer generated sheet. The patients Wilcoxan test for quantitative data based randomized in interventional group (test on the distribution of data. Missing data group) were received glimepiride 2mg was handled using Mean substitution or once daily along with oral Resveratrol 500 Last observation carried forward (LOCF) mg twice a day (a total of 1 g/daily). The method. Chi-square test /fisher exact test patients randomized to control group were was used to compare the categorical or received only glimepiride 2mg once daily. qualitative data of both the treatment The treatment duration was 12 months for groups. Normality tests (KS and SW test) both the groups. Compliance to study were used to detect distribution of data for drugs was assed using pill count method at numerical data. P value of less than 0.05 each assessment visit after dispending was considered as statistical significant study drugs to patients. Both systolic and difference. diastolic blood pressure (BP) was assessed RESULTS twice with 2 minutes apart after a 5-minute There was no patient dropout from each rest in the sitting position, using an group during the study period. At the end auscultatory method of measurement with of the study, total 30 patients in each group a properly calibrated and validated (control and intervention group) completed mercury sphygmomanometer. Heart rate the study and subjected in statistical was measured for one minute in the two analysis. A consort diagram is presented minute interval between BP showing the flow of participants through measurements. Body temperature was the study (Figure 1). measured by thermometer. Blood glucose Before the start of study drug treatment (at level (fasting and 2 hour post meal) and baseline), blood glucose levels (fasting and hemoglobin A1c (HbA1C) were measured post prandial) were comparable in both the at baseline (before the start of study treatment group. There was gradual treatment), end of 3 month, 6 month, 9 reduction in fasting and post prandial month and 12 month in both the treatment blood glucose levels over a period of 12 groups. All blood tests were performed at months hours in both the treatment groups the same laboratory at any time point as observed from the reduction trend in the (baseline, 3 month, 6 month, 9 month and blood glucose levels from baseline. In both 12 month) for every enrolled patient in the treatment groups, reduction in blood order to avoid the laboratory to laboratory glucose levels (fasting and post prandial) variation in the results. was statistically significant when Statistical Analysis: Based on a power of compared to baseline (within group 80% and a type I error rate of alpha= 0.05 comparison). Between groups comparison (2-tailed), a sample size of at least 50 showed that reduction in blood glucose patients per group was required to detect a levels (fasting and post prandial) was clinically significant difference of 32 significant greater in test group at 3 mg/dl in the change in blood glucose level months, 6, 9 and 12 months when (with an SD of ) between both the compared to control (p<0.005 at each time groups. Considering dropout rate of 15 %, point) [Table 2]. total sample size will be approx. 60 There was significant improvement in patients (60 patients in each group). blood glucose levels in both the treatment Categorical data was presented as absolute groups from baseline. However, number/percentage of patients while improvement in blood glucose level at 3 quantitative data was presented as mean ± months, 6, 9 and 12 months from baseline SD. Depending on the distribution of data was significantly greater in test group as appropriate parametric or non-parametric compared to control group. The difference 83 Int J Res Med. 2017; 5(4); e ISSN: p ISSN:
4 between both the treatments for the change prandial) from baseline was statistically in blood glucose level (fasting and post significant (Table 3). Figure 1: Flow of participants through the study Assessed for eligibility (n = 75) Allocation Enrollment Randomized (n = 60) Allocated to Glimepiride 2mg (n = 30) Received allocated intervention (n =30) Excluded (n =14) Not meeting inclusion criteria (n = 14) Allocated to Glimepiride 2mg + Resveratrol 500 mg BD (n = 30) Received allocated intervention (n =30) Follow up Lost to follow up and Discontinued intervention (n =0) Lost to follow up Discontinued intervention (n =0) Analysis Analyzed (n = 30) Excluded from analysis Analyzed (n = 30) Excluded from analysis Demographic and clinical characteristic of patients of both the treatment groups were comparable (Table 1). At the baseline, there was no significant difference between the two groups regarding age, gender, bodyweight, duration of disease, smoking, HbA1c and plasma blood glucose levels (fasting and 2 hour post meal). The prevalence of diabetes mellitus in the family was also comparable in both the treatment groups (Table 1). Table 1: Demographic and baseline clinical characteristics Patient characteristic Control Test P value Demography Gender (Male/Female) 19/11 17/13 >0.05 Age (year) 37.6 ± ± 3.18 >0.05 Height (Cm) ± ± 7.36 >0.05 Weight (Kg) 74.4 ± ± 7.23 >0.05 Smoking Yes No 3 2 >0.05 Duration of disease (months) 2.5± ± 0.9 >0.05 Family history of diabetes Yes No 3 2 >0.05 Table 2: Blood glucose levels (fasting and post prandial) at baseline and over the period of 12 month after study drug treatments Parameters Control Test 84 Int J Res Med. 2017; 5(4); e ISSN: p ISSN: P value Baseline Fasting ± ± >0.05 Post Prandial ± ± 9.31 >0.05 End of 3 months Fasting ± 7.11* ± 3.73* <0.05 Post Prandial ± 12.27* ± 7.56* <0.05 End of 6 months Fasting ± 5.30* ± 4.40* < ± Post Prandial ± 5.14* < * End of 9 months Fasting ± 3.41* ± 5.99* <0.05 Post Prandial ± 8.57* ± 5.63* <0.05 End of 12 months Fasting ± 2.65* ± 3.76* <0.05 Post Prandial ± 4.37* ± 6.31* <0.05 Control= Glimepiride 2mg; Test= Glimepiride 2mg + Resveratrol 500 mg twice daily. Values are expressed as Mean± Standard deviation. *p<0.05 from baseline by paired t test (within group
5 comparison). Between groups comparison was done using Un-paired t test. Table 3: Change in blood glucose levels (fasting and post prandial) from baseline to 3 months, 6, 9 and 12 after study drug treatments Parameters Control Test P value End of 3 months Fasting ± 9.53* -36.4± 17.75* <0.05 Post Prandial ± 10.70* -32.3± 11.41* <0.05 End of 6 months Fasting ± 13.23* -42.8± 18.57* <0.05 Post Prandial -23.0± 10.57* -38.9± 11.18* <0.05 End of 9 months Fasting -34.7± 13.67* -48.0± 19.75* <0.05 Post Prandial -29.0± 11.24* -44.3± 12.31* <0.05 End of 12 months Table 4: Change in hemoglobina1c (HbA1c) at baseline and over the period of 12 month after study drug treatments Fasting -36.6± 12.08* -49.7± 16.66* <0.05 Post Prandial -30.8± 15.56* ± 11.49* <0.05 Control= Glimepiride 2mg; Test= Glimepiride 2mg + Resveratrol 500 mg twice daily. Values are expressed as Mean± Standard deviation. *p<0.05 from baseline by paired t test (within group comparison). Between groups comparison was done using Un-paired t test At baseline, HbA1c levels among both the treatment groups were comparable. There was gradual reduction in HbA1c over a period of 12 months hours in both the treatment groups as observed from the reduction trend in the HbA1c from baseline. In both the treatment groups, reduction in HbA1c was statistically significant when compared to baseline (within group comparison). Between groups comparison showed that reduction in HbA1c was significant greater in test group at 3 months, 6, 9 and 12 months when compared to control (p<0.005 at each time point) [Table 4]. There was significant improvement in HbA1c levels in both the treatment groups from baseline. However, improvement in HbA1c level at 3 months, 6, 9 and 12 months from baseline was significantly greater in test group as compared to control group. The difference between both the treatments for the change in HbA1c from baseline was statistically significant (Table 4). Parameters Control Test P value Baseline HbA1c 8.2 ± ± 0.46 >0.05 End of 3 months HbA1c 7.3 ± 0.44* 6.6 ± 0.47* <0.05 Change in HbA1c -0.9 ± 0.53* -1.7 ± 0.69* <0.05 End of 6 months HbA1c 6.6 ± 0.40* 6.0 ± 0.31* <0.05 Change in HbA1c -1.6 ± 0.57* -2.3 ± 0.56* <0.05 End of 9 months HbA1c 6.1 ± 0.39* 5.5 ± 0.41* <0.05 Change in HbA1c -2.1 ± 0.61* -2.8 ± 0.57* <0.05 End of 12 months HbA1c 5.9 ± 0.43* 5.4 ± 0.37* <0.05 Change in HbA1c -2.3 ± 0.65* -2.9 ± 0.55* <0.05 Control= Glimepiride 2mg; Test= Glimepiride 2mg + Resveratrol 500 mg twice daily. Values are expressed as Mean± Standard deviation. *p<0.05 from baseline by paired t test (within group comparison). Between groups comparison was done using Un-paired t test. DISCUSSION In this prospective, randomized, parallel, open label, comparative, active controlled, single center clinical study, resveratrol as adjuvant significantly decrease fasting and fed blood glucose level in patients with T2DM. Also Resveratrol significantly decrease HbA1c in patients with T2DM. Resveratrol as adjuvant therapy having acceptable safety profile, and the most common adverse event is gastrointestinal disturbance. Our study suggested that the addition of resveratrol to gold standard therapy of anti-diabetic class of drug significantly improve the efficacy of gold standard therapy, possibly due to synergistic action. The potential effect of resveratrol in management of hyperglycemia has been established in preclinical setting. In rodent model, resveratrol exhibits significant antidiabetic potential by attenuating hyperglycemia, enhancing insulin secretion and antioxidant competence in pancreatic betacells of diabetic rats 7. Resveratrol decreases blood glucose in animals with hyperglycemia. This effect seems to predominantly result from increased intracellular transport of glucose. Studies 85 Int J Res Med. 2017; 5(4); e ISSN: p ISSN:
6 gold standard therapy as adjuvant therapy in clinical setting. CONCLUSION Resveratrol as an adjuvant therapy was found to be well tolerated and effective in T2DM. Both the study drugs have comparable safety profile and found well tolerable. Resveratrol plus glimepiride was found to be superior over glimepiride monotherapy in reducing plasma blood glucose concentration (fasting and fed) and significantly improve glycemic control by reducing HbA1c levels in patients with T2DM. REFERENCES 1. Mohan V, Sandeep S, Deepa R, Shah B, Varghese C. Epidemiology of type 2 diabetes: Indian scenario. Indian J Med Res. 2007; 125(3): Rakesh PM, Shashank RJ, Padmavathy SM, Nalini SS. Prevalence and pattern of diabetic dyslipidemia in Indian type 2 diabetic patients Diabetes & Metabolic Syndrome: Clinical Research & Reviews. 2010; 4: McAdam MC. Economic implications of type 2 diabetes management. Am J Manag Care. 2013;19(8 Suppl):S Rana Ibrahim. Diabetes mellitus type II: review of oral treatment options. International Journal of Pharmacy and Pharmaceutical Sciences. 2010; 2 (Suppl 1): Athena PT. Type 2 Diabetes: Limitations of Current Therapies. of animals with insulin resistance indicate that resveratrol may also improve insulin action 8. Our finding is consistent with the previous reports that resveratrol combined with metformin act synergistically on AMP-activated protein kinase-dependent pathways, leading to increased insulin sensitivity, which may reduce the therapeutic doses of metformin necessary in the treatment of diabetes 9. In rodent model, resveratrol potentiates improving glycemic control, glucose uptake, as well as protecting against pancreatic β-cell failure in a spontaneous type 2 diabetes 10. Moreover, our study results were also consistent with the previous clinical reports, short term clinical use of resveratrol 1 gram/daily (500 mg BD) was found to be effective in decreasing fasting blood sugar level and correct imbalance in lipid level when compared to Placebo after 45 days 11. Another 4 week clinical study (in 10 subjects) suggested that there was no change in fasting blood sugar and, lipid level after administration of resveratrol (1g, 1.5g and 2g/daily). However, study suggested that resveratrol improves insulin sensitivity and post-meal plasma glucose in subjects with impaired glucose tolerance 12. Glycated hemoglobin (HbA1c) levels in blood are one of key marker to know glycemic control 11. In our study, resveratrol significantly decrease hemoglobina1c in patients with T2DM. We also observed that resveratrol as adjuvant therapy was found to be effective in improving glycemic control in type 2 diabetes mellitus. Results of our study showed the combination of resveratrol and gold standard therapy of anti-diabetic class of drug significantly improve glycemic control by decreasing HbA1c as compared to the monotherapy, this was possibly due to synergistic action. The potential effect of resveratrol on HbA1c has been established in pre-clinical setting 10. Our study results with respect to resveratrol were consistent with previous report 11, 12. Our study support the long term clinical efficacy and safety study of resveratrol along with gold standard therapy in diabetic patient, and suggested synergistic effect of resveratrol when given along with Available at: ntlive/supplements/0907con_diabetes_ Philis.pdf [Accessed on 20-Aug-2016]. 6. R. N. Mishra. Resveratrol-The New Rasayan (Anti-aging) Drug. Current Research in Medicine and Medical Sciences. 2011; 1 (1): Palsamy P, Subramanian S. Ameliorative potential of resveratrol on proinflammatory cytokines, hyperglycemia mediated oxidative stress, and pancreatic beta-cell dysfunction in streptozotocinnicotinamide-induced diabetic rats. J Cell Physiol. 2010; 224(2): Int J Res Med. 2017; 5(4); e ISSN: p ISSN:
7 8. Szkudelski T, Szkudelska K Antidiabetic 11. Movahed A, Nabipour I, Lieben Louis effects of resveratrol. Ann N Y X, Thandapilly SJ, Yu L, Acad Sci. 2011; 1215: Kalantarhormozi M, et al. 9. Do GM, Jung UJ, Park HJ, Kwon EY, Antihyperglycemic effects of short Jeon SM, McGregor RA, et al. term resveratrol supplementation in Resveratrol ameliorates diabetes-related type 2 diabetic patients. Evid Based metabolic changes via activation of Complement Alternat Med. 2013; AMP-activated protein kinase and its 2013: downstream targets in db/db mice. Mol 12. Crandall JP, Oram V, Trandafirescu G, Nutr Food Res. 2012; 56(8): Reid M, Kishore P, Hawkins M, et al. 10. Bruckbauer A, Zemel MB. Synergistic Pilot study of resveratrol in older effects of metformin, resveratrol, and adults with impaired glucose tolerance. hydroxymethylbutyrate on insulin J Gerontol A Biol Sci Med Sci. sensitivity. Diabetes Metab Syndr 2012;67(12): Obes. 2013; 6: Int J Res Med. 2017; 5(4); e ISSN: p ISSN:
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