Lipids and cardiovascular/metabolic health

Effects of Avena nuda L. on metabolic control and cardiovascular disease risk among Chinese patients with diabetes and meeting metabolic syndrome criteria: secondary analysis of a randomized clinical trial

Abstract

Background/objectives:

Most patients with Type 2 diabetes mellitus(DM) also have metabolic syndrome (MetS), which is associated with an increased risk of coronary heart disease prevalence. Limited information is available on the effect and effective doses of oat intake with a structured dietary intervention in metabolic control and cardiovascular disease (CVD) risk prevention with the population who has Type 2 DM and meets the MetS criteria.

Subjects/methods:

A total of 260 Type 2 DM patients meeting MetS National Cholesterol Education Program Adult Treatment Panel III criteria were selected from 445 patients between 50 and 65 years of age, and they participated in a single-blinded, 30-day centralized management of a dietary program in China. Participants in the program were randomly assigned into one of the four groups: usual care group (control group, only basic health advice), diet group (systematic diet plans and intensive education), 50 g-organic naked oat with whole germ group (ONOG) and 100 g-organic naked oat with whole germ group (daily ONOG replacement boiled into porridge based on diet group). The primary outcomes were the relative changes in glycosylated hemoglobin (HbA1c) and insulin resistance after a 30-day intervention among the four groups.

Results:

HbA1c decreased significantly with the increase in interventions (Ptrend<0.05). Similar results were also obtained in plasma glucose, serum lipid and hypersensitive C-reactive protein (hs-CRP). For the 100 g-ONOG group but not 50 g-ONOG group, HbA1c and hs-CRP reduced significantly by 0.51% and 1.29 mg/l (P<0.05, vs diet group), respectively. The 100 g-ONOG group showed a reduction by 0.22 U*mol/l2 in insulin resistance, compared with the 50 g-ONOG group (P=0.039).

Conclusions:

Compared with diet alone or no diet, 50–100 g/day ONOG supplement to structured dietary intervention, at a dose of 100 g/day especially, contributes to the Type 2 DM patients meeting MetS criteria in their metabolic control and CVD risk prevention, with external factors being controlled.

Introduction

Type 2 diabetes mellitus (DM) and its cardiovascular complications are global health problems and an economic burden.1, 2, 3 Several studies show that more than half of the population with Type 2 DM, who meet the National Cholesterol Education Program (NCEP) Adult Treatment Panel (ATP) III definition of metabolic syndrome (MetS), have an increased risk of coronary heart disease prevalence.4, 5

A lot of evidence indicates that medical nutrition therapy is highly recommended for the management of Type 2 DM and the improvement on diabetic outcomes.6, 7 As an important dietary factor of medical nutrition therapy, whole-grain intake has got special attention for its high effectiveness on Type 2 DM and other metabolic diseases. Several epidemiologic and experimental studies, as well as systematic reviews, concluded that the consumption of whole grains was inversely associated with the risk of Type 2 DM, MetS and cardiovascular disease (CVD).8, 9, 10, 11 About 3–6 servings (48–96 g) of whole grains per day, that is, at least half of the daily recommended grain intake, are suggested by the Dietary Guidelines for Americans (2010).12 The replacement of 50−100 g/day of refined carbohydrates with equivalent coarse grains is equally helpful to the elderly, according to the recommendation of the Dietary Guidelines for Elderly Chinese (2010).13 However, limited information from clinical trials is available on the effective doses of the whole-grain consumption for Type 2 DM or MetS. In addition, few studies have evaluated the effect of whole-grain consumption on metabolic control and CVD risk prevention in a population with Type 2 DM and meeting MetS criteria.

Oat is an excellent choice among various whole grains because of the advantages in its composition.14 The common oat (Avena sativa L.) and its products such as oatmeal, oat fiber-enriched bread and oat crisp, are a major source of whole-grain intake in western countries. The nutritional composition and therapeutic potentials of common oat have been widely studied.15, 16, 17, 18, 19, 20 However, naked oat (A nuda L.) is the main kind of oats in China and it is different from common oat in terms of its type, origin, environment and processing plant. The composition and health effect of naked oat, however, still remain undetermined and thus questionable.

To develop a protocol of medical nutrition therapy (including whole-grain intake) on Type 2 DM for clinical application, a randomized, single-blinded, multiarm parallel trial was carried out for adults with Type 2 DM at a single study center in Baotou, Inner Mongolia Autonomous Region, China (Trial registration: NCT01495052 at ClinicalTrials.gov). Meanwhile, another objective of this randomized controlled trial was to investigate the effects of naked oat on Type 2 DM and its complications by further analysis. Therefore, the secondary data analysis aimed to evaluate not only the effect and effective doses of naked oat but also the integrative effects of naked oat with a structured dietary intervention in the Type 2 DM patients meeting the MetS criteria. The result of the analysis could provide some evidence for the medical nutrition therapy strategy and the CVD prevention to this population.

Subjects and Methods

Study population

A subgroup of 260 patients meeting MetS criteria (according to the National Cholesterol Education Program Adult Treatment Panel III criteria21) was selected from 445 patients between 50 and 65 years of age and with Type 2 DM (based on the WHO criteria), who took part in a 30-day centralized management of dietary program in the primary Baotou study. The eligible participants experienced at least two of the following circumstances: (1) high blood pressure (systolic blood pressure 130 or diastolic blood pressure85 mm Hg); (2) triglycerides (TGs)150 mg/dl (1.7 mmol/l); (3) high-density lipoprotein cholesterol (HDL-c)<40 mg/dl (1.03 mmol/l) in male participants and <50 mg/dl (1.29 mmol/l) in female participants; (4) central obesity (waist circumference >102 cm in male participants and >88 cm in female participants). Individuals who were pregnant, breastfeeding, under glucocorticoid treatment, or had severe renal or hepatic complications, had pancreatic disease or malignancy in the 3 months before the commencement of the study or had other factors that may be potentially negative to the trial were excluded. Written and oral information of the protocol was announced before the screening, and informed consents were obtained from each participant.

Study design

The study was approved by China–Japan Friendship Hospital of Ministry of Health of People’s Republic of China and was consistent with both the Declaration of Helsinki of 1975 as revised in 1983 and the guidelines of the center’s institutional review board. The offered dietary program was designed to investigate the integrative effects of organic naked oat with whole germ (ONOG), combined with a structured dietary intervention (systematic diet plans and intensive nutritional education included) in patients with Type 2 DM, under the centralized management. All participants were arranged to live in hotels and had dinner together at restaurants under the supervision of trained workers. During the study, they were requested to continue with their habits of physical activity and medication and were encouraged to keep a record of any signs of illness or deviations from the protocol. Food intakes and compliance of every participant were recorded by trained investigators each day. The technicians involved in the analyses and the statistician in charge of the preliminary assessment of the outcomes were blinded to the allocation.

After a 1-week run-in period, the participants were randomized by a computer-generated random number table. The 260 patients within the subgroup were assigned to one of the four groups as follows:

The usual care group (n=63, age 58.4±5.9 years of age, 49.2% male participants) was used as a control group and received no intervention except basic health advice at the beginning and the end of the study. The Chinese buffet meals were provided to this group for the patients to consume according to their own eating habit. Estimated by the participants’ diet record of 30 days in the trial, the mean total energy intake of this subgroup was 2453±594 kcal/day; the percentages of energy from carbohydrate, fat and protein were 44±10%, 37±8% and 19±5%, respectively; the dietary fiber was 22±4g/day.

The diet group (n=61, age 59.3±6.6 years of age, 45.9% male participants) received structured dietary intervention including intensive nutrition education and systematic plans of diets. The nutritional lessons were given six times a week by trained dietitians. The contents covered the knowledge of nutrition and Type 2 DM. The diets were composed of food commonly eaten in China, as determined in the China Food Composition 2004,22 the Dietary Guidelines for Chinese Resident23 and the China Medical Nutrition Therapy Guideline for Diabetes 2010.24 A 7-day menu rotation was used for three meals per day (the sample menu is provided as an online Supplementary Information). Daily intake of energy and nutrients by male and female participants is shown in Table 1. One day’s average serving provided 60% of total energy as carbohydrate, 22% as fat, 18% as protein and 30 g of dietary fiber. All meals were supervised. Food intakes and compliance of every participant were recorded everyday by trained investigators.

Table 1 Composition of the study diets for the treatment groups (one day’s serving)

The participants in the 50 g-ONOG group (n=65, age 59.4±6.1 years of age, 41.5% male participants) received structured dietary intervention, and they had been introduced to a daily homenergic substitute, which replaced the customarily used staple foods (including the products of rice, wheat flour, black rice, corn meal or foxtail millet) with 50 g ONOG (Inner Mongolia Sanzhuliang Natural Oats Industry Corporation, Baotao, China). The ONOG given were primary products peeled from naked oat crops, which were grown in drylands in the northwest of China by automatic planting (Patent Publication Number: CN101264459). They met the organic standards and retained all three necessary ingredients and beneficial nutrients of the whole grains. The nutrient composition of 100 g ONOG was 1623 kJ energy, 13.7 g protein, 63.5 g carbohydrates, 7.6 g fat, 8.7 g fiber, of which 5.0 g was beta (β)-glucan, and no heavy metals and pesticide were detected. The product was boiled into a porridge and provided as breakfast and supper every day. One day’s average serving provided 59% of total energy as carbohydrate, 23% as fat, 18% as protein and 33 g of dietary fiber per day.

Similarly, the participants in the 100 g-ONOG group (n=71, age 60.3±6.0 years of age, 36.6% male participants) received structured dietary intervention, and the daily homenergic substitute of customarily used staple foods was 100 g ONOG. One day’s average serving provided 57% of total energy as carbohydrate, 24% as fat, 19% as protein and 36 g of dietary fiber.

Outcome measures

Physical examinations were carried out at baseline as well as at the end of the 30-day intervention. Weight, height, waist circumference, hip circumference and blood pressure were measured accordingly. Venous blood samples were obtained for the following measurement: fasting plasma glucose (FPG), 2-h postprandial plasma glucose (PG) after eating 100 g steamed bread equaling 75 g oral glucose, total TGs, total cholesterol (TC) and HDL-c, which were measured by the enzymic method; low-density lipoprotein cholesterol (LDL-c), which was calculated; glycosylated hemoglobin (HbA1c), which was measured by the high-performance liquid chromatography method; hypersensitive C-reactive protein (hs-CRP), which was measured by the particle-enhanced immunoturbidimetic assay; fasting insulin, which was measured by the radioimmunoassay; and insulin resistance, which was calculated by the homeostasis model of assessment-insulin resistance with the formula, HOMA-IR=Fasting serum insulin (μU/ml) × FPG (mmol/l)/22.5.11, 25, 26, 27 Safety parameters including physical examination, complete blood count, blood biochemical examination, routine urine tests, liver and renal function (serum alanine transaminase, aspartic transaminase, blood urea nitrogen and serum creatinine), electrocardiogram and abdominal color ultrasonography were also examined.

Participants were required to refrain from medication and food for at least 12 h before the blood collection. All examinations were undertaken by the same certified clinic staff (Inner Mongolia Medical College, Third Hospital) at the same laboratory. Standardized questionnaires were used to obtain self-reported information including socioeconomic, demorgraphic, cultural and biological aspects. The primary outcomes of the randomized controlled trial were the relative changes in HbA1c and insulin resistance after the 30-day intervention.

Statistics

Descriptive statistics include the mean (standard deviation, s.d.) or the median (interquartile range) for continuous variables and the number (percentage) for categorical variables. Equality and normality of variance were checked before any further analysis, and variables with a skewed distribution were log10 transformed. To assess treatment differences, the paired Student’s t test and the Wilcoxon test were used for within-group comparisons; the χ2-Test and the analysis of variance test were used for between-group comparisons. Changes in outcomes were calculated as values at the end of the intervention period minus those of baseline. To adjust for the baseline values of the outcomes and potential confounding variables, a calculation of the multivariable linear regression and an analysis of covariance model (generalized linear model) were carried out. The analysis of covariance model was composed of terms for age, sex, body mass index (BMI) and the corresponding baseline variable value. Results were considered statistically significant at P<0.05 with all P-values two sided. We estimated a s.d. of 2.7mmol/l in HbA1c. The true sample size in the second analysis was 260 (63, 61, 65 and 71 in the usual care, diet, 50-ONOG and 100-ONOG groups, respectively), which provided an 80% power with a 5% α (two-tailed) to detect a difference of 0.98 s.d. in HbA1c between the groups, allowing for 10% of data missing. All data were analyzed on an intention-to-treat basis without imputation with SPSS for WINDOWS 17·0 (SPSS Inc, Chicago, IL, USA).

Results

Seventeen of 260 subjects dropped out because of personal reasons (usual care group: 4, diet group: 4, 50 g-ONOG group: 3 and 100 g-ONOG group: 6). The χ2-Test showed no significant difference in drop-out rates between the groups. In addition, no significant difference was found between the four groups with respect to the main baseline characteristics of patients (Table 2).

Table 2 Baseline characteristics of the study subjects according to groupa

Thirty-day changes in variables from baseline for each group are indicated in Table 3. After the 30-day intervention, weight, BMI, HbA1c, FPG and TC decreased significantly in the usual care group, whereas serum lipids, blood glucose, HbA1c, insulin resistance, weight, BMI, waist circumference and hs-CRP decreased in the other three groups. However, the changes in insulin resistance, LDL-c and hs-CRP in the diet group and those in insulin resistance and TG in the 50 g-ONOG group were not statistically significant.

Table 3 Changes in metabolic variables during the studya

As the interventions increased gradually from the usual care group to the 100 g-ONOG group, HbA1c significantly decreased (Ptrend<0.001) after 30 days. Similar trends were observed in PG, TC, LDL-c (Ptrend<0.001), FPG, TG and hs-CRP (Ptrend=0.001, 0.021 and 0.045, respectively). Among the three treatment groups, FPG was reduced as the oat intake increased (Ptrend=0.038). The circumstances were also observed in TC (Ptrend=0.003) and LDL-c (Ptrend=0.004).

Compared with the usual care group, all three treatment groups showed a reduction in HbA1c, FPG, PG, TC, HDL-c and LDL-c (P<0.05, except for LDL-c in the diet group); insulin resistence, TG, weight, BMI, waist circumference and hs-CRP only reduced significantly in the 100 g-ONOG group (P<0.05, vs usual care group).

Compared with the diet group, relative changes in HbA1c, FPG and PG levels did not differ significantly between the 50 g-ONOG group and the diet group (P=0.054, 0.147 and 0.146, respectively), whereas the 100 g-ONOG replacement seemed to yield more significant changes on the three variables above (P=0.046, 0.022 and 0.020, compared with the diet group, respectively). Relative change in TC in the 50 g-ONOG group was 0.24 mmol/l less (P=0.029), and change in the 100 g-ONOG group was 0.36 mmol/l less (P=0.001) compared with the diet group. Similarly, LDL-c was 0.19 mmol/l less (P=0.020) in the 50 g-ONOG group and 0.28 mmol/l (P=0.001) less in the 100 g-ONOG group, compared with the diet group. The relative decrease in hs-CRP concentration was greater in the 100 g-ONOG group (1.29 mg/l, P=0.048) than those in the 50 g-ONOG group (0.51 mg/l, P=0.784), in comparison with the diet group.

Furthermore, compared with the 50 g-ONOG group, the 100 g-ONOG group showed a reduction of 0.22 μU × mol/l2 in insulin resistance (P=0.039) and 0.40 mmol/l in TGs (P=0.026).

Products were well tolerated by the participants. No serious adverse events were reported during the trial. Adverse events reported were generally hypoglycemia and mild gastrointestinal symptoms including diarrhea, gastrointestinal discomfort and constipation. Hypoglycemia usually occurred early during the study and was transient. The differences in the adverse events and safety parameters between the groups were insignificant.

Discussion

Hyperglycemia control and LDL-c level reduction are two of the primary aims for therapy of MetS.28 Meanwhile, glycemia control has beneficial effects on reducing the risk of diabetic complications, including heart disease.29 Moreover, LDL-C and CRP are important predictors in cardiovascular risk assessment.30 Therefore, the present findings, which showed linear decreasing trends in changes in the plasma glucose, serum lipid and hs-CRP levels with a gradual increase in interventions and ONOG intake, support the assumption that 50–100 g/day ONOG intake combined with a structured dietary intervention has more potential effects than dietary intervention alone or no dietary intervention on MetS factors and Type 2 DM control and on CVD prevention.

Compared with the control group, the dietary intervention groups (excluding ONOG) indicated the hypoglycemic and lipid-lowering effects in our study could possibly be ascribed to two points. First, a controlled diet plan was provided for Type 2 DM patients with relatively low energy, low fat and high fiber (563 kcal/day, 15% and 10 g/day less than the average intake in the usual care group for male participants, respectively; 178 kcal/day, 15% and 6 g/day less for female participants, respectively).23 Second, health education on Type 2 DM could help the participants improve their attitudes and thus stick to the plan easily.

On the basis of the advantages of the diet group, ONOG intake was added to the above dietary intervention for exploring additional effects of the naked oat. Concerning glycemia control in the Type 2 DM patients meeting the MetS criteria, 100 g ONOG (containing 5.0 g/day oat β-glucan) plus structured dietary intervention of 30 days resulted in significant improvements on HbA1c, FPG and PG, compared with the diet alone. The insulin resistance also reduced significantly when the ONOG intake dose was 100 g/day, compared with that when the dose was 50 g/day (P<0.05). A number of previous studies had investigated the relationship between oat products and Type 2 DM. It was revealed that the oat fiber had beneficial effects on glucose control31, 32 and it provided a relatively low glycemic response.33, 34 One cross-over study with a small sample size demonstrated a positive association between oat-bran-concentrated bread products with 9 g/day soluble fiber intake and blood glucose control in Type 2 DM;35 whereas in another 8-week parallel-control trial, 3.5 g/day common oat β-glucan in soup showed no significant improvements in FPG (P=0.45) and HbA1c (P=0.38),17 which could be attributed to its lower baseline of glucose metabolic variables, the different types of oats, β-glucan supplement alone and a lower β-glucan intake, compared with our study.

As for lipid control, the ONOG intake, at a dose of 50 g/day (containing 2.5 g/day oat β-glucan) and 100 g/day, had better effects on the reductions of TC and LDL-c than diet alone for the Type 2 DM patients meeting the MetS criteria. Furthermore, the improvement trend was more prominent at a dose of 100 g/day. Some previous studies had shown the capacity of oats in the treatment of dyslipidemia. As predicted, our results on cholesterol-lowering effects of oat products were consistent with most trials and reviews.14, 19, 36 However, several studies did not support this conclusion, such as a 5-week trial37 of oat β-glucan (4.0 g/day) consumption with a ready-meal soup in healthy subjects and another 3-month trial38 of water-soluble fiber (8.0 g/day) from oat bran intake within hyperlipidemic participants. Similar to the outcome of glycemia control, the difference between the studies above and the present one may be caused by some common reasons: oats used in different experiments were varied; the past products for partcipants’ intake were only part of the oats or extracts from the oats, instead of the whole grains. In addition, similar mild reductions in HDL-c levels were showed in all the three treatment groups. According to the previous document,39 the side effect of a low-cholesterol and saturated-fat diet was one possible reason for HDL-c reduction in our study.

The ONOG product used in the present study was peeled to maintain most ingredients and beneficial nutrients of the whole-oat grains, while keeping the acceptable modest hardness for eating. The doses of ONOG, 50 and 100 g/day, in the study were in line with the recommendation of whole-grain intake or coarse cereals for adults or for the elderly made by the Dietary Guidelines.12, 13 The boiled oat porridge offered to the participants had well palatability and would be a suitable choice of whole grains for Chinese; avoiding some negative palatability of β-glucan supplementation at high doses.17 Among the diet plus or not plus ONOG groups, for the isocaloric replacement between ONOG and the customarily used staple foods, the total energy were identical and the macronutrient composition was slightly changed except dietary fiber, which increased by an average of 3 g/day and 6 g/day for 50 g/day and 100 g/day ONOG replacement, respectively. This increasing fiber intake might partly explain for the additional effects of ONOG in our study.7 As had been mentioned before, the oat ingredients and products contained dietary fiber or oat β-glucan equal or more than that by ONOG intake in our study; however, the lipid-lowering effects were not significant in some studies.37, 38 Despite some factors such as the medium, viscosity, solubility and molecular weight of β-glucan40 might partly explain these controversial results, the entire package-element synergism effects of whole grains should also be taken into account. In previous studies, oat β-glucan and secondary oat products such as oatmeal, oat bran and flour following western dietary habits17, 37, 38 were the main forms of oat intake, which might cause a greater loss in nutrition at the milling step.41 As one of the whole-grain family members, ONOG had favorable chemical composition including water-soluble dietary fiber, protein, unsaturated fatty acids and antioxidants, which might contribute together better on improving health than those of the equivalence β-glucan alone extracted from common oat. Besides, compared with the most of previous trials with free-living subjects,17, 35, 37, 38 one highlight of our study design was the centralized management of subjects’ daily life, which enhanced the homogenization among groups and compliance of the study.

The trends of hs-CRP changing among the three treatment groups were similar to those of the glucose and lipid metabolism variables, which hinted the effect of the decreasing CVD risk by 100 g/day ONOG intake. This result was in agreement with a study about the association between a whole-grain-enriched diet and CVD in patients with MetS.11 In addition, weight and BMI decreased in 100 g/day ONOG intake as partly replacement of the staple food. The reduction was significant when compared with no dietary intervention but not significant when compared with diet alone. There results were mainly in agreement with the previous studies. In three 12-week trials, the effect on weight loss of energy-restricted and low-fiber foods was not obviously enhanced by the supplementation of whole-grain ready-to-eat oat cereal (3 g/day oat β-glucan), oat β-glucan (5–9 g/day) or whole-grain-enriched hypocaloric diet within adults who were overweight, obese or who met the MetS criteria, respectively.11, 19, 42 However, other studies reported the reduction in the percentage of body fat in the abdominal region for whole-grain supplement,11 which needs further investigation.

The limitations of this study must be recognized. Our study could not prevent the information bias during the single-blinded trial due to the lack of suitable placebo for ONOG porridge up to now. Meanwhile, although the centralized management had an important role in sticking to the diet, the results reveal that an ideal model and more clinical practice are needed to allow the interventions to be extrapolated to normal diets in real life.

In conclusion, the results from the secondary data analysis suggest that when external factors are controlled systematically, structured dietary intervention combined with ONOG intake of no less than 50 g/day, particularly at a dose of 100 g/day, shows greater potential in improving glycemia and lipid profile control and even a positive CVD outcome in patients with Type 2 DM and meeting the MetS criteria, compared with dietary intervention alone or no dietary intervention. Future studies including comparison of the effectiveness and mechanisms between A sativa L. and A nuda L. on Type 2 DM and MetS control shall be carried out.

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Acknowledgements

We thank the Beijing Nutrition Society and the Inner Mongolia Medical College, Third Hospital for their help with the study. We also thank the members of our volunteer team, Zhi Sun, Bin Cai, Fang Li, Guangling Hu, Hao Yu, Jianqin Chen, Junguo He, Meihong Yang, Peng Song, Peng Zhang, Xiping Xu, Yao Meng, Meiyan Liu, Yuxia Jin, Ying Li, Yaohui Jiang, Ya Zhang and Zhibin Sun for their excellent job with the study. We thank Yimin Zhu, Yongliang Zhang, Shuhua Zhao and Chuan Fan, Dewei Liang for editing the manuscript for English. This study was funded by Inner Mongolia Sanzhuliang Natural Oats Industry Corporation. The trial is registered at ClinicalTrials.gov, number NCT01495052. The sponsor of the study had no role in the study design, data collection, data analysis, data interpretation or writing of the report.

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Correspondence to Y Li.

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Author contributions

The authors’ responsibilities were described as follows: XM participated in the research design, conducted the research, performed the statistical analysis and wrote the manuscript; YL designed the research and had primary responsibility for final content. All authors participated in data acquisition and study supervision. All authors approved the final version of the report.

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Ma, X., Gu, J., Zhang, Z. et al. Effects of Avena nuda L. on metabolic control and cardiovascular disease risk among Chinese patients with diabetes and meeting metabolic syndrome criteria: secondary analysis of a randomized clinical trial. Eur J Clin Nutr 67, 1291–1297 (2013). https://doi.org/10.1038/ejcn.2013.201

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Keywords

  • cardiovascular disease
  • cereals
  • diabetes mellitus, Type 2
  • Metabolic syndrome X

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