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original article
                                                                                                                              Diabetes, Obesity and Metabolism 12: 204–209, 2010.
                                                                                                                                                  © 2010 Blackwell Publishing Ltd




           A low carbohydrate Mediterranean diet improves
           cardiovascular risk factors and diabetes control among
original
article




           overweight patients with type 2 diabetes mellitus: a 1-year
           prospective randomized intervention study
           A. Elhayany1,2,5 , A. Lustman2,3 , R. Abel2 , J. Attal-Singer4,5 & S. Vinker2,3
           1 CEO, Meir Medical Center, Kfar Saba, Israel
           2 Department of Family Medicine, Central District Clalit Health Services, Rishon Le Zion, Israel
           3 Department of Family Medicine, Tel Aviv University, Tel Aviv, Israel
           4 Endocrinology Institute, Rabin Medical Center, Beilinson Campus, Petah Tikva, Israel
           5 Department of Family Medicine, The Sackler School of Medicine, Tel Aviv University, Tel Aviv, Israel




           Background: The appropriate dietary intervention for overweight persons with type 2 diabetes mellitus (DM2) is unclear. Trials comparing
           the effectiveness of diets are frequently limited by short follow-up times and high dropout rates.
           Aim: The effects of a low carbohydrate Mediterranean (LCM), a traditional Mediterranean (TM), and the 2003 American Diabetic Association
           (ADA) diet were compared, on health parameters during a 12-month period.
           Methods: In this 12-month trial, 259 overweight diabetic patients (mean age 55 years, mean body mass index 31.4 kg/m2 ) were randomly
           assigned to one of the three diets. The primary end-points were reduction of fasting plasma glucose, HbA1c and triglyceride (TG) levels.
           Results: 194 patients out of 259 (74.9%) completed follow-up. After 12 months, the mean weight loss for all patients was 8.3 kg: 7.7 kg for
           ADA, 7.4 kg for TM and 10.1 kg for LCM diets. The reduction in HbA1c was significantly greater in the LCM diet than in the ADA diet (−2.0 and
           −1.6%, respectively, p < 0.022). HDL cholesterol increased (0.1 mmol/l ± 0.02) only on the LCM (p < 0.002). The reduction in serum TG was
           greater in the LCM (−1.3 mmol/l) and TM (−1.5 mmol/l) than in the ADA (−0.7 mmol/l), p = 0.001.
           Conclusions: An intensive 12-month dietary intervention in a community-based setting was effective in improving most modifiable
           cardiovascular risk factors in all the dietary groups. Only the LCM improved HDL levels and was superior to both the ADA and TM in improving
           glycaemic control.
           Keywords: cardiovascular risk, diabetes mellitus, dietary intervention, Mediterranean diet

           Date submitted 16 April 2009; date of first decision 29 July 2009; date of final acceptance 07 August 2009




           Introduction                                                                               The recommendations focus on the quantity of carbohydrates
                                                                                                      consumed, but not on the source or type of carbohydrate.
           The prevalence of diabetes among the Israeli population in
                                                                                                         Diets based on carbohydrates with a low glycaemic
           2000 was 3.4% [1]. According to the Centers for Disease
                                                                                                      index (LGI) have been found to improve HbA1c levels
           Control and Prevention (CDC), the prevalence of diabetes
                                                                                                      and reduce insulin resistance, as well as lower cholesterol,
           in the USA in 2004 was 5.1% [2]. Weight reduction in
                                                                                                      triglyceride (TG) and very low-density lipoprotein cholesterol
           overweight patients with type 2 diabetes mellitus (DM2)
                                                                                                      concentrations [8]. However, the relative importance of
           has been proven to be effective in diabetes treatment [3,4].
                                                                                                      glycaemic index and of glycaemic load as well as the relative
           Proper dietary intervention can restore insulin sensitivity and
           prevent disease progression and complications [5,6]. However,                              advantages of higher fat diets and the type of dietary fat vs.
           recommendations differ as to which diet is more effective                                  diets with high carbohydrate content are debated [9–11]. The
           in achieving weight loss and glycaemic control and reducing                                lack of consensus is largely due to the relatively small number
           cardiovascular risk factors.                                                               of participants in some studies and the difficulties with patient
              In 2004, the American Diabetic Association (ADA)                                        follow-up over long periods particularly in community-based
           recommended that carbohydrates and monounsaturated fats                                    studies.
           (MUFA) together should provide 60–70% of energy intake [7].                                   Previous studies [12–15] have suggested that a diet enriched
                                                                                                      in MUFA elevates blood levels of high-density lipoprotein
                                                                                                      cholesterol (HDL-C), reduces low-density lipoprotein choles-
           Correspondence to: Asher Elhayany, Meir Medical Center, 59 Tchernichovsky Street, Kfar
           Saba 44821, Israel.
                                                                                                      terol (LDL-C) and TGs in DM2 and has a positive effect on
           E-mail: elasher@clalit.org.il                                                              cardiovascular disease risk factors [16,17].
DIABETES, OBESITY AND METABOLISM                                                                 original article
   Given the unclear data, and the lack of community-based            diets included only LGI carbohydrates whereas the ADA
long-term clinical trials, our group conducted a large                diet included mixed glycaemic index carbohydrates. TM
community-centered interventional study comparing three               and ADA included the same percentages of carbohydrates
types of isocaloric diets in overweight DM2 patients.                 (50–55%), fat (30%) and protein (15–20%); LCM included
   We compared the 2003 ADA diet (50–55% carbohydrates,               35% carbohydrates and 45% fat (50% MUFA). Participants
30% fats and 20% proteins) with a traditional Mediterranean           were counselled to eat 4–6 meals/day according to their
(TM) diet (50–55% LGI carbohydrates, 30% fats–high                    lifestyle.
in monounsaturated fat content, 15–20% proteins) and
a low carbohydrate Mediterranean (LCM) diet (35% LGI                  Dietary Questionnaires
carbohydrates, 45% fats–high in monounsaturated fat content,
15–20% proteins). The main outcome measures were                      Participants completed a 24-h food recall questionnaire, a
glycaemic control and biomarkers for cardiovascular risk.             validated food frequency questionnaire (FFQ) and a physical
                                                                      activity questionnaire that included quality of life measures, at
                                                                      baseline, 3 and 6 months [19,20]. Before the study, the dietitians
Methods                                                               participated in a training workshop to ensure standardization
The study population has been described elsewhere [18].               in questionnaire administration.
Briefly, 259 eligible patients with DM2 were enrolled between
March 2003 and April 2004. Eligible patients were recruited
                                                                      Outcome Measures
from 10 urban primary care clinics in Israel’s central region
using the electronic medical records of Clalit Health Services, a     Clinical Measurements
Health Maintenance Organization.                                      Weight, height, waist and hip circumferences were measured
   Inclusion criteria were: (i) age 30–65 years; (ii) DM2             at every visit. Blood pressure was obtained monthly as a mean
diagnosed within 1–10 years; (iii) body mass index (BMI)              of three readings.
27–34 kg/m2 ; (iv) last HbA1c measurement 7–10%; (v) last
plasma TG level 1.8–4.5 mmol/l; (vi) last serum creatinine
<123.2 μmol/l; and (vii) no change in diabetes medication for         Laboratory Measurements
at least 3 months before entering the study.                          All tests were performed in the Clalit Health Services Central
   Exclusion criteria were: (i) proliferative diabetic retinopathy;   District laboratory. Fasting blood glucose, plasma insulin levels,
(ii) current insulin treatment; (iii) active oncologic or             HbA1c, total cholesterol, HDL-C, TGs, liver enzymes, serum
psychiatric disease; and (iv) uncontrolled hypothyroidism or          creatinine and urea were measured at baseline and every
hyperthyroidism.                                                      3 months.
   We identified 2486 patients with DM2, 1063 (42.8%) of
whom met the inclusion criteria and 644 (60.6%) of those were
willing to participate. Before the study entry, patients were         Statistical Analysis
asked to repeat laboratory tests and to undergo fundoscopy:           To compare the differences between diets and changes from
244 patients did not comply and an additional 141 were                baseline, t-test, one way ANOVA, chi-square or Fisher’s exact
excluded as a result of new findings, thus 259 patients were           tests were used as appropriate. To evaluate the effect of the
enrolled (figure 1).                                                   diets and examine the changes over time, as well as the
                                                                      interaction between diet and time, we examined the repeated
Intervention                                                          measures using generalized linear models. Measurements taken
                                                                      at baseline, 3, 6, 9 and 12 months were used in the analyses,
Prior to randomization, the 259 eligible patients entered a 2-
                                                                      and TG levels were examined after log transformation. Post
week maintenance period. During this time, the patients were
                                                                      hoc Scheffe test was used to identify the statistically different
asked to continue their usual diet and keep a food intake diary.
                                                                      diets. All p values were two-sided; p < 0.05 was considered
The patients were then randomly assigned to one of three
                                                                      statistically significant. All analyses were conducted using SPSS-
isocaloric diets: TM, LCM or ADA.
                                                                      PC version 15.
   Patients were followed up by the same dietitian every 2
weeks for 1 year. All dieticians followed a structured protocol
for the 24 scheduled meetings and treated patients from each          Results
of the three diet groups. All patients were advised to engage in
30–45 min of aerobic activity at least 3 days a week.                 Of the 259 patients enrolled in the study, 85 were randomly
                                                                      assigned to the ADA diet, 89 to TM, and 85 to the LCM
                                                                      diet. There were no significant differences at baseline in
Dietary Intervention                                                  demographic, clinical or laboratory measurements among
Table A1 (Appendix) outlines the composition of each diet.            the three groups (table 1). Cumulative dropouts were 43,
The daily recommended intake of calories, protein, sodium             56 and 65 patients at 3, 6 and 9 months respectively. The
(up to 3000 mg), potassium (more than 3000 mg), calcium               discontinuation rates in the three diet groups were similar
(approximately 1300 mg) and magnesium (more than 800 mg)              (figure 1). The 80 individuals who did not complete the 12-
were similar in the three diet programs. The TM and LCM               month follow-up had, at baseline, statistically significant higher



Volume 12 No. 3 March 2010                                                                  doi:10.1111/j.1463-1326.2009.01151.x 205
original article                                                                             DIABETES, OBESITY AND METABOLISM



                                                      Assessed for eligibility
                                                             n =2486


                                                             Enrollment              Not meeting inclusion criteria
                                                                                     n =1423
                                                                                     Refused to participate n=419
                                                       Agreed to participate         Other reasons (unable to contact,
                                                         and randomized              moved, changed to another HMO)
                                                              n=259                  n=385
                                                                                     Total exclusions n=2227

                                                          ENROLLMENT




                                ADA diet n=85             TM diet n=89                      LCM diet n=85


                                                             FOLLOW-UP


                                Lost to follow-up       Lost to follow-up                 Lost to follow-up
                              Up to 3 months n=15      Up to 3 months n=13               Up to 3 months n=14
                              Up to 6 months n= 11     Up to 6 months n= 8               Up to 6 months n= 6
                               6 to 12 months n= 4     6 to 12 months n= 5               6 to 12 months n= 4
                                     Due to:                 Due to:                          Due to:
                             Noncompliance n= 10      Noncompliance n= 11               Noncompliance n=13
                             Changed residence n=2      Unrelated health                Changed residence n=3
                             Domestic problems n=3        problems n=5                  Domestic problems n=4
                                 Unrelated health           Other n=1                     Unrelated health
                                 problems n=7         Incomplete 12-month                  problems n=2
                                    Other n=2          follow up data n=9                    Other n=2
                              Incomplete 12-month
                               follow up data n=6


                                                     Completed 12-month follow-up


                                     n=55                     n=63                                 n=61



Figure 1. Flow chart of the study population.


fasting plasma glucose, total cholesterol and LDL-C levels than           blood lipids and HOMA decreased in all three groups, while
patients who completed the study. No differences were observed            fasting insulin levels increased over time. Differences between
in HbA1c, weight, waist circumference, systolic and diastolic             diets were found for HbA1c, TGs and HDL-C as well as for
blood pressures, HDL-C and TG levels.                                     LDL-C. The reduction in HbA1c was significantly greater for
   To determine patient adherence to the recommended diets,               patients on the LCM than for patients on the ADA diet. The
we evaluated the results of the FFQ administered at 6 months.             decrease in TGs was greater for the LCM and TM than for
The mean reported energy intake was similar in the three diets            the ADA group (p = 0.001). Patients on the LCM achieved a
(2221.6 calories ± 1086.6). There was a statistically significant          significant increase in HDL-C levels compared to the ADA, but
trend in the percentage of polyunsaturated fat intake of total            did not differ significantly from those on the TM diet. LDL-C
energy, from highest (12.9%) in LCM, to 11.5% in TM, and                  levels were reduced for all three diets after a year; we found that
lowest in ADA 11.2% (p = 0.002). The same significant trend                the decrease was greatest in LCM, but not significantly greater
was observed for monounsaturated fat intake (14.6, 12.8, and              than the TM diet.
12.6% for LCM, TM, and ADA, respectively, p < 0.001). The                    Additional analysis was performed including the 80
opposite trend was observed for the percentage of carbohydrate            individuals without 12-month data using the latest available of
intake, being highest in the ADA, and lowest in the LCM                   3-, 6- or 9-month follow-up data. The results were comparable
diet (45.4, 45.2, 41.9 for ADA, TM and LCM, respectively,                 to the analysis of those who completed the study.
p = 0.011).

Clinical Measurements                                                     Discussion
At the end of the 12-month study period, weight, BMI and waist            In recent years, low carbohydrate diets have been shown to
circumference were reduced in all the dietary interventions with          be effective in improving glycaemic control and body weight
no significant difference between the groups (table 2). HbA1c,             in type 2 diabetes [21–24] as well as weight loss in obese



206 Elhayany et al.                                                                                                Volume 12 No. 3 March 2010
DIABETES, OBESITY AND METABOLISM                                                                             original article
Table 1. Baseline characteristics of the patients in the three diet groups       in part by increased consumption of dietary fat in the LCM
                                                                                 group [29], however, the non-significant differences in caloric
                        Diet [data presented as mean (±s.d.)]                    intake between groups may have contributed to this weight
                        ADA            TM            LCM                         loss.
Characteristics         (n = 55)       (n = 63)      (n = 61)       p-value         The LCM reduced the LDL levels by an extra 8% when
Male/female (n)         27/28        35/28       31/30              0.764
                                                                                 compared to the ADA and TM, which themselves each reduced
Age (year)           56.0 (6.1)   57.4 (6.1)  55.5 (6.5)            0.229        LDL by 20% (LCM reduced 24.8%, TM 20.9% and ADA
Years since DM        5.1 (2.6)    6.2 (9.9)   5.5 (3.8)            0.229        13.8%). This finding is of particular note, as other studies using
  diagnosis                                                                      high MUFA diets have not shown significant reductions in LDL
Weight (kg)          87.9 (13.7) 85.5 (10.6) 86.7 (14.3)            0.544        [16]. These studies had a follow-up between 4 and 6 weeks. It
BMI                  31.8 (3.3)   31.1 (2.8)  31.4 (2.8)            0.483        is possible that the reduction of LDL in high MUFA diets takes
Waist circumference 113.4 (10.0) 111.1 (9.1) 112.7 (9.6)            0.401
  (cm)
                                                                                 considerably longer to manifest than 4–6 weeks and therefore
HbA1c (%)             8.3 (0.8)    8.3 (1.0)   8.3 (1.0)            0.980        in these earlier studies the full effect of the MUFA diet was not
Fasting plasma       10.3 (1.7)   10.1 (1.8)  10.5 (2.0)            0.454        recorded.
  glucose (mmol/l)                                                                  In our study, LCM was the only diet that led to an increase
Fasting plasma       12.7 (6.2)   12.1 (6.5)  13.5 (5.7)            0.476        in HDL-C levels (12%). Although the ADA recommends
  insulin (μU/ml)                                                                reducing fat calories to less than 30% of the total daily caloric
HOMA                  5.8 (3.3)    5.0 (2.9)   5.9 (4.0)            0.549
                                                                                 intake, several recent studies underlined the superiority of diets
Total cholesterol     5.4 (0.9)    5.5 (0.8)   5.4 (0.9)            0.848
  (mmol/l)                                                                       containing higher amounts of MUFA. Garg et al. [30] found
HDL-C (mmol/l)        1.1 (0.2)    1.1 (0.2)   1.1 (0.2)            0.732        a 7–13% increase in HDL-C levels when comparing a diet
LDL-C (mmol/l)        3.0 (0.9)    3.2 (0.8)   3.1 (0.8)            0.769        rich in MUFA with a diet rich in carbohydrates in diabetic
Triglycerides         3.1 (0.8)    3.0 (0.7)   3.2 (0.8)            0.792        patients. These findings together with our study suggest that a
  (mmol/l)                                                                       low carbohydrate, high MUFA diet might be the best method
                                                                                 to increase HDL-C, while still reducing LDL.
patients [25–27]. Based on this increasing evidence, in 2008                        Previous studies were unable to clarify the effect of a high
the ADA included a low carbohydrate diet as a possible                           MUFA diet on HbA1c. In our study, both TM and LCM diets
intervention.                                                                    induced a greater decrease in HbA1c than did the ADA. As
   We found that an intensive community-based dietary                            both Mediterranean diets were based on LGI carbohydrates,
intervention reduced cardiovascular risk factors in overweight                   while the reference diet included mixed glycaemic index
patients with DM2 for all three diets. The LCM group had                         carbohydrates, this study supports the suggested protective
improved cardiovascular risk factors compared to either the                      effects of LGI carbohydrates on glycaemic control in patients
ADA or the TM groups.                                                            with DM2.
   The weight loss in the LCM group at 1 year was greater                           Consumption of MUFA is thought to improve insulin
than in the other dietary intervention groups, although the                      sensitivity [31–33], an effect that may explain the favourable
difference was not significant. Similar results have been found                   effect of the Mediterranean diet on glucose and HbA1c levels.
among moderately obese adults [28]. This may be explained                        Furthermore, both the Mediterranean and low carbohydrate

Table 2. Results from generalized linear model analysis describing changes in clinical and laboratory measurements between baseline and 12-month
follow-up examinations


                                    ADA (n = 55)                   TM (n = 63)                LCM (n = 61)
                                    Baseline       12-month        Baseline      12-month     Baseline       12-month    Change over    p value
Variables                           (± s.d.)       (± s.d.)        (± s.d.)      (± s.d.)     (± s.d.)       (± s.d.)    time p value   between diets
Weight (kg)                         87.8   (13.7) 80.2 (13.2) 85.5 (10.6) 78.1 (9.9)    86.7 (14.3) 77.8 (13.1)          <0.001          0.557
BMI                                 31.8   (3.2)  29.0 (3.3)   31.1 (2.8)  28.5 (2.9)   31.4 (2.8)  28.1 (2.8)           <0.001          0.359
Waist circumference (cm)           113.1   (9.7) 104.0 (10.2) 110.9 (8.9) 101.6 (8.0) 112.6 (9.7) 102.2 (10.2)           <0.001          0.388
Fasting plasma glucose (mmol/l)    10.26   (1.69) 7.19 (1.85) 10.07 (1.80) 6.57 (1.34) 10.47 (2.00) 6.18 (0.84)          <0.001          0.087
HbA1c (%)                            8.3   (0.8)   6.7 (0.9)    8.3 (1.0)   6.5 (0.8)    8.3 (1.0)   6.3 (1.4)           <0.001          0.021∗,†
Total cholesterol (mmol/l)          5.36   (0.89) 4.50 (0.71) 5.46 (0.85) 4.50 (0.69) 5.38 (0.97) 4.50 (0.85)            <0.001          0.204
LDL-C (mmol/l)                      3.05   (0.87) 2.68 (0.83) 3.18 (0.76) 2.63 (0.67) 3.07 (0.81) 2.46 (0.72)            <0.001          0.036∗
HDL-C (mmol/l)                      1.05   (0.22) 1.00 (0.19) 1.09 (0.17) 1.09 (0.21) 1.08 (0.23) 1.21 (0.21)            <0.001         <0.001∗‡
Triglycerides (mmol/l)              3.14   (0.81) 2.26 (1.12) 3.04 (0.68) 1.58 (0.33) 3.18 (0.78) 1.66 (0.36)            <0.001         <0.001∗,†
Fasting insulin (μU/ml)             12.8   (6.7)  13.7 (5.3)   11.2 (6.6)  12.4 (6.2)   12.6 (8.4)  14.9 (5.7)            0.007          0.183
HOMA                                5.85   (3.32) 4.32 (2.07) 4.96 (2.95) 3.69 (1.90) 5.94 (4.00) 4.20 (1.80)            <0.001          0.238
∗ LCM different than ADA.
†
  TM different than ADA.
‡
  LCM different than TM.



Volume 12 No. 3 March 2010                                                                               doi:10.1111/j.1463-1326.2009.01151.x 207
original article                                                                                         DIABETES, OBESITY AND METABOLISM


diets have been shown to reduce postprandial hyperglycaemia,                         9. Hung T, Sievenpiper JL, Marchie A, Kendall CWC, Jenkins DJA. Fat versus
which likely lowers LDL and TGs [34].                                                   carbohydrate in insulin resistance, obesity, diabetes and cardiovascular
   Some limitations in our study must be underlined.                                    disease. Curr Opin Clin Nutr Metab Care 2003; 6: 165–176.
Potentially eligible patients refused to repeat fundoscopy and                      10. Hu FB, van Dam RM, Liu S. Diet and risk of type II diabetes: the role of
blood tests and therefore, were not enrolled. The dropout                               types of fat and carbohydrates. Diabetologia 2001; 44: 805–817.
rate was relatively high at 31% (80/259), although this was                         11. Sargrad KR, Mozzoli M. Effect of high protein vs high carbohydrate intake
in keeping with other nutritional studies [35]. Patients were                           on insulin sensitivity, body weight, hemoglobin A1c, and blood pressure
in independent living conditions without close supervision of                           in patients with type 2 diabetes mellitus. J Am Diet Assoc 2005; 105:
their food intake. However, food questionnaires showed a good                           573–580.
adherence to the assigned diet and patients were followed up                        12. Garg A, Bonamone A, Grundy SM, Zhang ZJ, Unger RH. Comparison of a
every 2 weeks in an urban primary care clinic.                                          high-carbohydrate diet with a high-monounsaturated-fat diet in patients
   In conclusion, we found that nutritional therapy in a                                with non-insulin-dependent diabetes mellitus. N Engl J Med 1988; 319:
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was effective in reducing BMI, HbA1c, LDL and TG levels for                         13. Campbell LV, Marmot PM, Dyer JA, Borkman M, Storlien LH. The high-
all three of the dietary interventions. A low carbohydrate                              monounsaturated fat as a practical alternative for NIDDM. Diabetes Care
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Mediterranean diet also increased HDL-C levels and was
superior in reducing LDL, TG and HbA1c levels compared                              14. Toobert DJ, Glasgow RE, Strycker LA et al. Biologic and quality-of-life
to ADA and standard Mediterranean diets. It would appear                                outcomes from the Mediterranean lifestyle program. Diabetes Care 2003;
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                                                                                        mellitus: a meta-analysis. Am J Clin Nutr 1998; 67: 577S–582S.
                                                                                    16. Rodriguez-Villar C, Perez-Heras A, Mercade I, Casals E, Ros E. Comparison
Acknowledgements                                                                        of a high-carbohydrate and a high- monounsaturated fat, olive oil-rich
                                                                                        diet on the susceptibility of LDL to oxidative modification in subjects with
This study was registered in Clinical Trials.gov Protocol
                                                                                        type 2 diabetes mellitus. Diabet Med 2004; 21: 142–149.
Registration System: IDNCT00520182. The authors would like
                                                                                    17. Esposito K, Marfella R, Ciotola M et al. Effect of a mediterranean-style diet
to thank S. Daniel Abraham International Center for Health and
                                                                                        on endothelial dysfunction and markers of vascular inflammation in the
Nutrition, Ben Gurion University, for assisting in study design
                                                                                        metabolic syndrome: a randomized trial. JAMA 2004; 292: 1440–1446.
and statistical analysis, Faye Schreiber for editorial assistance
                                                                                    18. Shahar DR, Abel R, Elhayani A, Vardi H, Fraser D. Does calcium intake
and Nava Yelin for helping in statistical analysis.
                                                                                        enhance weight loss among overweight diabetic patients? Diabetes Care
                                                                                        2007; 30: 485–489.
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    diabetes mellitus. N Engl J Med 2000; 342: 1392–1398.                               Association. Diabetes Care 2008; 31: S61–S78.




208 Elhayany et al.                                                                                                            Volume 12 No. 3 March 2010
DIABETES, OBESITY AND METABOLISM                                                                                 original article
28. Shai I, Schwarzfuchs D, Henkin Y et al. Dietary intervention random-          35. Jenkins DJ, Kendall CW, McKeown-Eyssen G et al. Effect of a low-glycemic
    ized controlled trial (DIRECT) group. Weight loss with a low-                     index or a high-cereal fiber diet on type 2 diabetes: a randomized trial.
    carbohydrate, Mediterranean, or low-fat diet. N Engl J Med 2008; 17:              JAMA 2008; 300: 2742–2753.
    229–241.
29. Tucker LA, Thomas KS. Increasing total fiber intake reduces risk of weight     Appendix
    and fat gains in women. J Nutr 2009; 139: 576–581.
30. Garg A, Bantle JP, Henry RR, et al. Effects of varying carbohydrate content   Table A1. Composition of diets
    of diet in patients with NIDDM. JAMA 1994; 271: 1421–1428.
31. Esposito K, Marfella R, Ciotola M et al. Effect of a Mediterranean-style        Diet                                 ADA            TM            LCM
    diet on endothelial dysfunction and markers of vascular inflammation             Carbohydrates∗ (% of TCI)            50             50            35
    in the metabolic syndrome: a randomized trial. JAMA 2004; 292:                    Fibre (g)                          15             30            30
    1440–1446.                                                                      Fat∗ (% of TCI)                      30             30            45
32. Schwenke DC. Insulin resistance, low-fat diets, and low-carbohydrate              MUFA (% of fat)                    10             10            23
    diets: time to test new menus. Curr Opin Lipidol 2005; 16: 55–60.                 PUFA (% of fat)                    12             12            15
                                                                                      SFA                                 7              7             7
33. Lara-Castro C, Garvey WT. Diet, insulin resistance, and obesity: zoning in
                                                                                    Protein∗ (% of TCI)                  20             20            20
    on data for Atkins dieters living in South Beach. J Clin Endocrinol Metab
                                                                                    Calories/kg body weight              20             20            20
    2004; 89: 4197–4205.
34. Gheewala NM. Dietary strategies for improving post-prandial glucose,          MUFA, monounsaturated fats; PUFA, polyunsaturated fats; SFA, saturated
    lipids, inflammation, and cardiovascular health. J Am Coll Cardiol 2008;       fats.
                                                                                  ∗
    51: 249–255.                                                                    Carbohydrates, fat and proteins are 100% of total caloric intake (TCI).




Volume 12 No. 3 March 2010                                                                                 doi:10.1111/j.1463-1326.2009.01151.x 209

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A low carbohydrate mediterranean diet improves cardiovascular risk factors and diabetes control among overweight patients

  • 1. original article Diabetes, Obesity and Metabolism 12: 204–209, 2010. © 2010 Blackwell Publishing Ltd A low carbohydrate Mediterranean diet improves cardiovascular risk factors and diabetes control among original article overweight patients with type 2 diabetes mellitus: a 1-year prospective randomized intervention study A. Elhayany1,2,5 , A. Lustman2,3 , R. Abel2 , J. Attal-Singer4,5 & S. Vinker2,3 1 CEO, Meir Medical Center, Kfar Saba, Israel 2 Department of Family Medicine, Central District Clalit Health Services, Rishon Le Zion, Israel 3 Department of Family Medicine, Tel Aviv University, Tel Aviv, Israel 4 Endocrinology Institute, Rabin Medical Center, Beilinson Campus, Petah Tikva, Israel 5 Department of Family Medicine, The Sackler School of Medicine, Tel Aviv University, Tel Aviv, Israel Background: The appropriate dietary intervention for overweight persons with type 2 diabetes mellitus (DM2) is unclear. Trials comparing the effectiveness of diets are frequently limited by short follow-up times and high dropout rates. Aim: The effects of a low carbohydrate Mediterranean (LCM), a traditional Mediterranean (TM), and the 2003 American Diabetic Association (ADA) diet were compared, on health parameters during a 12-month period. Methods: In this 12-month trial, 259 overweight diabetic patients (mean age 55 years, mean body mass index 31.4 kg/m2 ) were randomly assigned to one of the three diets. The primary end-points were reduction of fasting plasma glucose, HbA1c and triglyceride (TG) levels. Results: 194 patients out of 259 (74.9%) completed follow-up. After 12 months, the mean weight loss for all patients was 8.3 kg: 7.7 kg for ADA, 7.4 kg for TM and 10.1 kg for LCM diets. The reduction in HbA1c was significantly greater in the LCM diet than in the ADA diet (−2.0 and −1.6%, respectively, p < 0.022). HDL cholesterol increased (0.1 mmol/l ± 0.02) only on the LCM (p < 0.002). The reduction in serum TG was greater in the LCM (−1.3 mmol/l) and TM (−1.5 mmol/l) than in the ADA (−0.7 mmol/l), p = 0.001. Conclusions: An intensive 12-month dietary intervention in a community-based setting was effective in improving most modifiable cardiovascular risk factors in all the dietary groups. Only the LCM improved HDL levels and was superior to both the ADA and TM in improving glycaemic control. Keywords: cardiovascular risk, diabetes mellitus, dietary intervention, Mediterranean diet Date submitted 16 April 2009; date of first decision 29 July 2009; date of final acceptance 07 August 2009 Introduction The recommendations focus on the quantity of carbohydrates consumed, but not on the source or type of carbohydrate. The prevalence of diabetes among the Israeli population in Diets based on carbohydrates with a low glycaemic 2000 was 3.4% [1]. According to the Centers for Disease index (LGI) have been found to improve HbA1c levels Control and Prevention (CDC), the prevalence of diabetes and reduce insulin resistance, as well as lower cholesterol, in the USA in 2004 was 5.1% [2]. Weight reduction in triglyceride (TG) and very low-density lipoprotein cholesterol overweight patients with type 2 diabetes mellitus (DM2) concentrations [8]. However, the relative importance of has been proven to be effective in diabetes treatment [3,4]. glycaemic index and of glycaemic load as well as the relative Proper dietary intervention can restore insulin sensitivity and prevent disease progression and complications [5,6]. However, advantages of higher fat diets and the type of dietary fat vs. recommendations differ as to which diet is more effective diets with high carbohydrate content are debated [9–11]. The in achieving weight loss and glycaemic control and reducing lack of consensus is largely due to the relatively small number cardiovascular risk factors. of participants in some studies and the difficulties with patient In 2004, the American Diabetic Association (ADA) follow-up over long periods particularly in community-based recommended that carbohydrates and monounsaturated fats studies. (MUFA) together should provide 60–70% of energy intake [7]. Previous studies [12–15] have suggested that a diet enriched in MUFA elevates blood levels of high-density lipoprotein cholesterol (HDL-C), reduces low-density lipoprotein choles- Correspondence to: Asher Elhayany, Meir Medical Center, 59 Tchernichovsky Street, Kfar Saba 44821, Israel. terol (LDL-C) and TGs in DM2 and has a positive effect on E-mail: elasher@clalit.org.il cardiovascular disease risk factors [16,17].
  • 2. DIABETES, OBESITY AND METABOLISM original article Given the unclear data, and the lack of community-based diets included only LGI carbohydrates whereas the ADA long-term clinical trials, our group conducted a large diet included mixed glycaemic index carbohydrates. TM community-centered interventional study comparing three and ADA included the same percentages of carbohydrates types of isocaloric diets in overweight DM2 patients. (50–55%), fat (30%) and protein (15–20%); LCM included We compared the 2003 ADA diet (50–55% carbohydrates, 35% carbohydrates and 45% fat (50% MUFA). Participants 30% fats and 20% proteins) with a traditional Mediterranean were counselled to eat 4–6 meals/day according to their (TM) diet (50–55% LGI carbohydrates, 30% fats–high lifestyle. in monounsaturated fat content, 15–20% proteins) and a low carbohydrate Mediterranean (LCM) diet (35% LGI Dietary Questionnaires carbohydrates, 45% fats–high in monounsaturated fat content, 15–20% proteins). The main outcome measures were Participants completed a 24-h food recall questionnaire, a glycaemic control and biomarkers for cardiovascular risk. validated food frequency questionnaire (FFQ) and a physical activity questionnaire that included quality of life measures, at baseline, 3 and 6 months [19,20]. Before the study, the dietitians Methods participated in a training workshop to ensure standardization The study population has been described elsewhere [18]. in questionnaire administration. Briefly, 259 eligible patients with DM2 were enrolled between March 2003 and April 2004. Eligible patients were recruited Outcome Measures from 10 urban primary care clinics in Israel’s central region using the electronic medical records of Clalit Health Services, a Clinical Measurements Health Maintenance Organization. Weight, height, waist and hip circumferences were measured Inclusion criteria were: (i) age 30–65 years; (ii) DM2 at every visit. Blood pressure was obtained monthly as a mean diagnosed within 1–10 years; (iii) body mass index (BMI) of three readings. 27–34 kg/m2 ; (iv) last HbA1c measurement 7–10%; (v) last plasma TG level 1.8–4.5 mmol/l; (vi) last serum creatinine <123.2 μmol/l; and (vii) no change in diabetes medication for Laboratory Measurements at least 3 months before entering the study. All tests were performed in the Clalit Health Services Central Exclusion criteria were: (i) proliferative diabetic retinopathy; District laboratory. Fasting blood glucose, plasma insulin levels, (ii) current insulin treatment; (iii) active oncologic or HbA1c, total cholesterol, HDL-C, TGs, liver enzymes, serum psychiatric disease; and (iv) uncontrolled hypothyroidism or creatinine and urea were measured at baseline and every hyperthyroidism. 3 months. We identified 2486 patients with DM2, 1063 (42.8%) of whom met the inclusion criteria and 644 (60.6%) of those were willing to participate. Before the study entry, patients were Statistical Analysis asked to repeat laboratory tests and to undergo fundoscopy: To compare the differences between diets and changes from 244 patients did not comply and an additional 141 were baseline, t-test, one way ANOVA, chi-square or Fisher’s exact excluded as a result of new findings, thus 259 patients were tests were used as appropriate. To evaluate the effect of the enrolled (figure 1). diets and examine the changes over time, as well as the interaction between diet and time, we examined the repeated Intervention measures using generalized linear models. Measurements taken at baseline, 3, 6, 9 and 12 months were used in the analyses, Prior to randomization, the 259 eligible patients entered a 2- and TG levels were examined after log transformation. Post week maintenance period. During this time, the patients were hoc Scheffe test was used to identify the statistically different asked to continue their usual diet and keep a food intake diary. diets. All p values were two-sided; p < 0.05 was considered The patients were then randomly assigned to one of three statistically significant. All analyses were conducted using SPSS- isocaloric diets: TM, LCM or ADA. PC version 15. Patients were followed up by the same dietitian every 2 weeks for 1 year. All dieticians followed a structured protocol for the 24 scheduled meetings and treated patients from each Results of the three diet groups. All patients were advised to engage in 30–45 min of aerobic activity at least 3 days a week. Of the 259 patients enrolled in the study, 85 were randomly assigned to the ADA diet, 89 to TM, and 85 to the LCM diet. There were no significant differences at baseline in Dietary Intervention demographic, clinical or laboratory measurements among Table A1 (Appendix) outlines the composition of each diet. the three groups (table 1). Cumulative dropouts were 43, The daily recommended intake of calories, protein, sodium 56 and 65 patients at 3, 6 and 9 months respectively. The (up to 3000 mg), potassium (more than 3000 mg), calcium discontinuation rates in the three diet groups were similar (approximately 1300 mg) and magnesium (more than 800 mg) (figure 1). The 80 individuals who did not complete the 12- were similar in the three diet programs. The TM and LCM month follow-up had, at baseline, statistically significant higher Volume 12 No. 3 March 2010 doi:10.1111/j.1463-1326.2009.01151.x 205
  • 3. original article DIABETES, OBESITY AND METABOLISM Assessed for eligibility n =2486 Enrollment Not meeting inclusion criteria n =1423 Refused to participate n=419 Agreed to participate Other reasons (unable to contact, and randomized moved, changed to another HMO) n=259 n=385 Total exclusions n=2227 ENROLLMENT ADA diet n=85 TM diet n=89 LCM diet n=85 FOLLOW-UP Lost to follow-up Lost to follow-up Lost to follow-up Up to 3 months n=15 Up to 3 months n=13 Up to 3 months n=14 Up to 6 months n= 11 Up to 6 months n= 8 Up to 6 months n= 6 6 to 12 months n= 4 6 to 12 months n= 5 6 to 12 months n= 4 Due to: Due to: Due to: Noncompliance n= 10 Noncompliance n= 11 Noncompliance n=13 Changed residence n=2 Unrelated health Changed residence n=3 Domestic problems n=3 problems n=5 Domestic problems n=4 Unrelated health Other n=1 Unrelated health problems n=7 Incomplete 12-month problems n=2 Other n=2 follow up data n=9 Other n=2 Incomplete 12-month follow up data n=6 Completed 12-month follow-up n=55 n=63 n=61 Figure 1. Flow chart of the study population. fasting plasma glucose, total cholesterol and LDL-C levels than blood lipids and HOMA decreased in all three groups, while patients who completed the study. No differences were observed fasting insulin levels increased over time. Differences between in HbA1c, weight, waist circumference, systolic and diastolic diets were found for HbA1c, TGs and HDL-C as well as for blood pressures, HDL-C and TG levels. LDL-C. The reduction in HbA1c was significantly greater for To determine patient adherence to the recommended diets, patients on the LCM than for patients on the ADA diet. The we evaluated the results of the FFQ administered at 6 months. decrease in TGs was greater for the LCM and TM than for The mean reported energy intake was similar in the three diets the ADA group (p = 0.001). Patients on the LCM achieved a (2221.6 calories ± 1086.6). There was a statistically significant significant increase in HDL-C levels compared to the ADA, but trend in the percentage of polyunsaturated fat intake of total did not differ significantly from those on the TM diet. LDL-C energy, from highest (12.9%) in LCM, to 11.5% in TM, and levels were reduced for all three diets after a year; we found that lowest in ADA 11.2% (p = 0.002). The same significant trend the decrease was greatest in LCM, but not significantly greater was observed for monounsaturated fat intake (14.6, 12.8, and than the TM diet. 12.6% for LCM, TM, and ADA, respectively, p < 0.001). The Additional analysis was performed including the 80 opposite trend was observed for the percentage of carbohydrate individuals without 12-month data using the latest available of intake, being highest in the ADA, and lowest in the LCM 3-, 6- or 9-month follow-up data. The results were comparable diet (45.4, 45.2, 41.9 for ADA, TM and LCM, respectively, to the analysis of those who completed the study. p = 0.011). Clinical Measurements Discussion At the end of the 12-month study period, weight, BMI and waist In recent years, low carbohydrate diets have been shown to circumference were reduced in all the dietary interventions with be effective in improving glycaemic control and body weight no significant difference between the groups (table 2). HbA1c, in type 2 diabetes [21–24] as well as weight loss in obese 206 Elhayany et al. Volume 12 No. 3 March 2010
  • 4. DIABETES, OBESITY AND METABOLISM original article Table 1. Baseline characteristics of the patients in the three diet groups in part by increased consumption of dietary fat in the LCM group [29], however, the non-significant differences in caloric Diet [data presented as mean (±s.d.)] intake between groups may have contributed to this weight ADA TM LCM loss. Characteristics (n = 55) (n = 63) (n = 61) p-value The LCM reduced the LDL levels by an extra 8% when Male/female (n) 27/28 35/28 31/30 0.764 compared to the ADA and TM, which themselves each reduced Age (year) 56.0 (6.1) 57.4 (6.1) 55.5 (6.5) 0.229 LDL by 20% (LCM reduced 24.8%, TM 20.9% and ADA Years since DM 5.1 (2.6) 6.2 (9.9) 5.5 (3.8) 0.229 13.8%). This finding is of particular note, as other studies using diagnosis high MUFA diets have not shown significant reductions in LDL Weight (kg) 87.9 (13.7) 85.5 (10.6) 86.7 (14.3) 0.544 [16]. These studies had a follow-up between 4 and 6 weeks. It BMI 31.8 (3.3) 31.1 (2.8) 31.4 (2.8) 0.483 is possible that the reduction of LDL in high MUFA diets takes Waist circumference 113.4 (10.0) 111.1 (9.1) 112.7 (9.6) 0.401 (cm) considerably longer to manifest than 4–6 weeks and therefore HbA1c (%) 8.3 (0.8) 8.3 (1.0) 8.3 (1.0) 0.980 in these earlier studies the full effect of the MUFA diet was not Fasting plasma 10.3 (1.7) 10.1 (1.8) 10.5 (2.0) 0.454 recorded. glucose (mmol/l) In our study, LCM was the only diet that led to an increase Fasting plasma 12.7 (6.2) 12.1 (6.5) 13.5 (5.7) 0.476 in HDL-C levels (12%). Although the ADA recommends insulin (μU/ml) reducing fat calories to less than 30% of the total daily caloric HOMA 5.8 (3.3) 5.0 (2.9) 5.9 (4.0) 0.549 intake, several recent studies underlined the superiority of diets Total cholesterol 5.4 (0.9) 5.5 (0.8) 5.4 (0.9) 0.848 (mmol/l) containing higher amounts of MUFA. Garg et al. [30] found HDL-C (mmol/l) 1.1 (0.2) 1.1 (0.2) 1.1 (0.2) 0.732 a 7–13% increase in HDL-C levels when comparing a diet LDL-C (mmol/l) 3.0 (0.9) 3.2 (0.8) 3.1 (0.8) 0.769 rich in MUFA with a diet rich in carbohydrates in diabetic Triglycerides 3.1 (0.8) 3.0 (0.7) 3.2 (0.8) 0.792 patients. These findings together with our study suggest that a (mmol/l) low carbohydrate, high MUFA diet might be the best method to increase HDL-C, while still reducing LDL. patients [25–27]. Based on this increasing evidence, in 2008 Previous studies were unable to clarify the effect of a high the ADA included a low carbohydrate diet as a possible MUFA diet on HbA1c. In our study, both TM and LCM diets intervention. induced a greater decrease in HbA1c than did the ADA. As We found that an intensive community-based dietary both Mediterranean diets were based on LGI carbohydrates, intervention reduced cardiovascular risk factors in overweight while the reference diet included mixed glycaemic index patients with DM2 for all three diets. The LCM group had carbohydrates, this study supports the suggested protective improved cardiovascular risk factors compared to either the effects of LGI carbohydrates on glycaemic control in patients ADA or the TM groups. with DM2. The weight loss in the LCM group at 1 year was greater Consumption of MUFA is thought to improve insulin than in the other dietary intervention groups, although the sensitivity [31–33], an effect that may explain the favourable difference was not significant. Similar results have been found effect of the Mediterranean diet on glucose and HbA1c levels. among moderately obese adults [28]. This may be explained Furthermore, both the Mediterranean and low carbohydrate Table 2. Results from generalized linear model analysis describing changes in clinical and laboratory measurements between baseline and 12-month follow-up examinations ADA (n = 55) TM (n = 63) LCM (n = 61) Baseline 12-month Baseline 12-month Baseline 12-month Change over p value Variables (± s.d.) (± s.d.) (± s.d.) (± s.d.) (± s.d.) (± s.d.) time p value between diets Weight (kg) 87.8 (13.7) 80.2 (13.2) 85.5 (10.6) 78.1 (9.9) 86.7 (14.3) 77.8 (13.1) <0.001 0.557 BMI 31.8 (3.2) 29.0 (3.3) 31.1 (2.8) 28.5 (2.9) 31.4 (2.8) 28.1 (2.8) <0.001 0.359 Waist circumference (cm) 113.1 (9.7) 104.0 (10.2) 110.9 (8.9) 101.6 (8.0) 112.6 (9.7) 102.2 (10.2) <0.001 0.388 Fasting plasma glucose (mmol/l) 10.26 (1.69) 7.19 (1.85) 10.07 (1.80) 6.57 (1.34) 10.47 (2.00) 6.18 (0.84) <0.001 0.087 HbA1c (%) 8.3 (0.8) 6.7 (0.9) 8.3 (1.0) 6.5 (0.8) 8.3 (1.0) 6.3 (1.4) <0.001 0.021∗,† Total cholesterol (mmol/l) 5.36 (0.89) 4.50 (0.71) 5.46 (0.85) 4.50 (0.69) 5.38 (0.97) 4.50 (0.85) <0.001 0.204 LDL-C (mmol/l) 3.05 (0.87) 2.68 (0.83) 3.18 (0.76) 2.63 (0.67) 3.07 (0.81) 2.46 (0.72) <0.001 0.036∗ HDL-C (mmol/l) 1.05 (0.22) 1.00 (0.19) 1.09 (0.17) 1.09 (0.21) 1.08 (0.23) 1.21 (0.21) <0.001 <0.001∗‡ Triglycerides (mmol/l) 3.14 (0.81) 2.26 (1.12) 3.04 (0.68) 1.58 (0.33) 3.18 (0.78) 1.66 (0.36) <0.001 <0.001∗,† Fasting insulin (μU/ml) 12.8 (6.7) 13.7 (5.3) 11.2 (6.6) 12.4 (6.2) 12.6 (8.4) 14.9 (5.7) 0.007 0.183 HOMA 5.85 (3.32) 4.32 (2.07) 4.96 (2.95) 3.69 (1.90) 5.94 (4.00) 4.20 (1.80) <0.001 0.238 ∗ LCM different than ADA. † TM different than ADA. ‡ LCM different than TM. Volume 12 No. 3 March 2010 doi:10.1111/j.1463-1326.2009.01151.x 207
  • 5. original article DIABETES, OBESITY AND METABOLISM diets have been shown to reduce postprandial hyperglycaemia, 9. Hung T, Sievenpiper JL, Marchie A, Kendall CWC, Jenkins DJA. Fat versus which likely lowers LDL and TGs [34]. carbohydrate in insulin resistance, obesity, diabetes and cardiovascular Some limitations in our study must be underlined. disease. Curr Opin Clin Nutr Metab Care 2003; 6: 165–176. Potentially eligible patients refused to repeat fundoscopy and 10. Hu FB, van Dam RM, Liu S. Diet and risk of type II diabetes: the role of blood tests and therefore, were not enrolled. The dropout types of fat and carbohydrates. Diabetologia 2001; 44: 805–817. rate was relatively high at 31% (80/259), although this was 11. Sargrad KR, Mozzoli M. Effect of high protein vs high carbohydrate intake in keeping with other nutritional studies [35]. Patients were on insulin sensitivity, body weight, hemoglobin A1c, and blood pressure in independent living conditions without close supervision of in patients with type 2 diabetes mellitus. J Am Diet Assoc 2005; 105: their food intake. However, food questionnaires showed a good 573–580. adherence to the assigned diet and patients were followed up 12. Garg A, Bonamone A, Grundy SM, Zhang ZJ, Unger RH. Comparison of a every 2 weeks in an urban primary care clinic. high-carbohydrate diet with a high-monounsaturated-fat diet in patients In conclusion, we found that nutritional therapy in a with non-insulin-dependent diabetes mellitus. N Engl J Med 1988; 319: 829–834. community-based population of overweight DM2 patients was effective in reducing BMI, HbA1c, LDL and TG levels for 13. Campbell LV, Marmot PM, Dyer JA, Borkman M, Storlien LH. The high- all three of the dietary interventions. A low carbohydrate monounsaturated fat as a practical alternative for NIDDM. Diabetes Care 1994; 17: 177–182. Mediterranean diet also increased HDL-C levels and was superior in reducing LDL, TG and HbA1c levels compared 14. Toobert DJ, Glasgow RE, Strycker LA et al. Biologic and quality-of-life to ADA and standard Mediterranean diets. It would appear outcomes from the Mediterranean lifestyle program. Diabetes Care 2003; 26: 2288–2293. that the low carbohydrate Mediterranean diet should be recommended for overweight diabetic patients. 15. Garg A. High-monounsaturated-fat diets for patients with diabetes mellitus: a meta-analysis. Am J Clin Nutr 1998; 67: 577S–582S. 16. Rodriguez-Villar C, Perez-Heras A, Mercade I, Casals E, Ros E. Comparison Acknowledgements of a high-carbohydrate and a high- monounsaturated fat, olive oil-rich diet on the susceptibility of LDL to oxidative modification in subjects with This study was registered in Clinical Trials.gov Protocol type 2 diabetes mellitus. Diabet Med 2004; 21: 142–149. Registration System: IDNCT00520182. The authors would like 17. Esposito K, Marfella R, Ciotola M et al. Effect of a mediterranean-style diet to thank S. Daniel Abraham International Center for Health and on endothelial dysfunction and markers of vascular inflammation in the Nutrition, Ben Gurion University, for assisting in study design metabolic syndrome: a randomized trial. JAMA 2004; 292: 1440–1446. and statistical analysis, Faye Schreiber for editorial assistance 18. Shahar DR, Abel R, Elhayani A, Vardi H, Fraser D. Does calcium intake and Nava Yelin for helping in statistical analysis. enhance weight loss among overweight diabetic patients? Diabetes Care 2007; 30: 485–489. References 19. Shahar DR, Shai I, Vardi H, Brener-Azrad A, Fraser D. Development of a 1. The Israeli Ministry of Health Statistics. Selected health for all indicators semi quantitative food frequency questionnaire (FFQ) to assess dietary 2003. Morbidity, disability and hospital discharges. Available from URL: intake of multiethnic populations. 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  • 6. DIABETES, OBESITY AND METABOLISM original article 28. Shai I, Schwarzfuchs D, Henkin Y et al. Dietary intervention random- 35. Jenkins DJ, Kendall CW, McKeown-Eyssen G et al. Effect of a low-glycemic ized controlled trial (DIRECT) group. Weight loss with a low- index or a high-cereal fiber diet on type 2 diabetes: a randomized trial. carbohydrate, Mediterranean, or low-fat diet. N Engl J Med 2008; 17: JAMA 2008; 300: 2742–2753. 229–241. 29. Tucker LA, Thomas KS. Increasing total fiber intake reduces risk of weight Appendix and fat gains in women. J Nutr 2009; 139: 576–581. 30. Garg A, Bantle JP, Henry RR, et al. Effects of varying carbohydrate content Table A1. Composition of diets of diet in patients with NIDDM. JAMA 1994; 271: 1421–1428. 31. Esposito K, Marfella R, Ciotola M et al. Effect of a Mediterranean-style Diet ADA TM LCM diet on endothelial dysfunction and markers of vascular inflammation Carbohydrates∗ (% of TCI) 50 50 35 in the metabolic syndrome: a randomized trial. JAMA 2004; 292: Fibre (g) 15 30 30 1440–1446. Fat∗ (% of TCI) 30 30 45 32. Schwenke DC. Insulin resistance, low-fat diets, and low-carbohydrate MUFA (% of fat) 10 10 23 diets: time to test new menus. Curr Opin Lipidol 2005; 16: 55–60. PUFA (% of fat) 12 12 15 SFA 7 7 7 33. Lara-Castro C, Garvey WT. Diet, insulin resistance, and obesity: zoning in Protein∗ (% of TCI) 20 20 20 on data for Atkins dieters living in South Beach. J Clin Endocrinol Metab Calories/kg body weight 20 20 20 2004; 89: 4197–4205. 34. Gheewala NM. Dietary strategies for improving post-prandial glucose, MUFA, monounsaturated fats; PUFA, polyunsaturated fats; SFA, saturated lipids, inflammation, and cardiovascular health. J Am Coll Cardiol 2008; fats. ∗ 51: 249–255. Carbohydrates, fat and proteins are 100% of total caloric intake (TCI). Volume 12 No. 3 March 2010 doi:10.1111/j.1463-1326.2009.01151.x 209