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

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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.
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original article DIABETES, OBESITY AND METABOLISM
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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
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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
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and statistical analysis, Faye Schreiber for editorial assistance
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and Nava Yelin for helping in statistical analysis.
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