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Diabetologia. Author manuscript; available in PMC Jul 4, 2010.
Published in final edited form as:
PMCID: PMC2896567
NIHMSID: NIHMS213763
Adults with type 1 diabetes eat a high fat, atherogenic diet which is associated with coronary artery calcium
JK Snell-Bergeon,1 C Chartier-Logan,1 DM Maahs,1 LG Ogden,2 JE Hokanson,2 GL Kinney,1 RH Eckel,3 J Ehrlich,3 and M Rewers1
1 Barbara Davis Center for Childhood Diabetes, University of Colorado Denver Anschutz Medical Campus, Aurora, CO
2 Colorado School of Public Health, University of Colorado Denver Anschutz Medical Campus, Aurora, CO
3 Department of Medicine, University of Colorado Denver Anschutz Medical Campus, Aurora, CO
Address correspondence to: Janet K. Snell-Bergeon Barbara Davis Center for Childhood Diabetes University of Colorado Denver P.O. Box 6511, Mail Stop A-140 Aurora, CO 80045 Phone: 303-724-6762 FAX: 303-724-5998 Janet.Snell-Bergeon/at/uchsc.edu
Aims/Hypotheses
Coronary heart disease (CHD) is the leading cause of mortality among people with type 1 diabetes. Diet is an important lifestyle factor related to CHD. The aim of this study was to examine how diet and adherence to dietary guidelines differ between adults with and without type 1 diabetes, and their correlation with CHD risk factors and coronary artery calcium (CAC).
Methods
571 people with type 1 diabetes and 696 controls 19 to 56 years old who were asymptomatic for CHD were studied. CAC was measured by electron beam CT.
Results
Adults with type 1 diabetes reported a diet higher in fat, saturated fat, and protein but lower in carbohydrates than controls. Less than half those with type 1 diabetes met dietary guidelines for fat and carbohydrate intake, and only 16% restricted saturated fat to <10% of daily calories. Adults with type 1 diabetes were significantly less likely to meet dietary guidelines than controls. Fat and saturated fat intake were positively correlated but carbohydrate intake was negatively correlated with CHD risk factors and hemoglobin A1c (HbA1c). A high fat diet and higher protein intake were associated with greater odds of CAC, while higher carbohydrate intake was associated with reduced odds of CAC.
Conclusions/Interpretation
Adults with type 1 diabetes reported consuming higher than recommended fat and saturated fat. Fat intake was associated with increased CHD risk factors, worse glycaemic control, and CAC. An atherogenic diet may contribute to the risk of CHD in adults with type 1 diabetes.
Keywords: Type 1 Diabetes Mellitus, coronary heart disease, dietary intake, fat intake, carbohydrate intake
Heart disease has been the leading cause of death in the United States for almost 80 years [1]. People with type 1 diabetes are at increased risk for developing coronary heart disease (CHD), with CHD mortality rates among adults with diabetes two to four times higher than the rates for adults without diabetes [2]. While most CHD mortality among adults can be attributed to type 1 diabetes [3], little is known about how well adults in the United States with type 1 diabetes meet dietary guidelines, and the influence of dietary intake on CHD risk in type 1 diabetes is not fully understood. The American Heart Association (AHA) has recognized diet and lifestyle are important, modifiable factors influencing CHD risk and are critical components of CHD prevention efforts [4].
Guidelines for medical nutrition therapy have been published by the American Diabetes Association (ADA) for patients with diabetes [5]. The dietary goals for patients with type 1 diabetes are largely in agreement with the dietary guidelines from the Institute of Medicine (IOM), which apply to healthy adults [6]. These include avoiding a low carbohydrate diet and consuming 45-65% of total calories in the form of carbohydrate; consuming 10-35% of total calories in the form of protein; and consuming 20-35% of total calories in the form of fat. For patients with diabetes, both the ADA and American Heart Association (AHA) [7] recommend limiting saturated fat to < 7% of total calories, while the AHA recommends limiting saturated fat to <10% of total calories in the larger population. Among patients with kidney disease, protein should be limited to 0.8 g/kg to prevent nephropathy [8]. As achieving glycaemic control (HbA1c < 7%) is an important ADA goal for patients with type 1 diabetes, the need to balance sufficient carbohydrate intake with avoidance of post-prandial hyperglycaemia is important, and can potentially be addressed by taking into account the glycaemic index (GI) of carbohydrates in the diet [5].
A recent report from the SEARCH for diabetes in youth study found that adherence to dietary guidelines was poor among children and adolescents with type 1 diabetes [9]. The Norwegian Childhood Diabetes and Quality Project found that children and adolescents with type 1 diabetes had a high frequency of atherogenic risk factors [10], and a high intake of energy from saturated fat and a low intake of fiber[11]. Another study in adolescents found that those with type 1 diabetes were heavier, ate more saturated fat, and ate less fruit and vegetables compared to those without diabetes [12].
Studies of dietary intake among adults with type 1 diabetes are sparse. The Diabetes and Nutrition Complications Trial in Spain found that adherence to American Diabetes Association (ADA) recommendations among adults with type 1 diabetes was low for fat and carbohydrate, although fat consumption was not associated with diabetes complications [13]. On the other hand, an Australian study reported lower fat and saturated fat intake among adults with type 1 diabetes compared to non-diabetic controls, and no association between dietary intake and glycaemic control in subjects with type 1 diabetes [8].
CHD is a chronic disease which develops over the course of decades, beginning as early as the teen years and progressing from fatty streaks to raised lesions and then complex lesions [14]. The detection of atherosclerosis in the preclinical stages is critical to furthering our understanding of risk factors which affect the early development and progression of disease. Coronary artery calcium (CAC) detected by electron beam computed tomography is a proxy measure for overall plaque burden[15-17], and the presence of CAC is a strong predictor of CHD events [18;19].
The purpose of this study was to examine dietary habits among adults with type 1 diabetes compared to adults without diabetes, and the association between diet, CHD risk factors and subclinical atherosclerosis.
Study Participants
The data presented in this report were collected as part of the baseline examination of the Coronary Artery Calcification in Type 1 Diabetes (CACTI) study. The study enrolled 1,416 individuals between 19-56 years of age, with no known history of CHD: 652 subjects with type 1 diabetes and 764 nondiabetic control subjects. Participants with type 1 diabetes had long-standing disease (mean duration 23 years, range 4-52 years), were insulin dependent within a year of diagnosis, and were diagnosed prior to age 30 or had positive antibodies or a clinical course consistent with type 1 diabetes.
Dietary Intake
Study participants who completed the baseline screening visit were asked to fill out a validated [20] self-administered food frequency questionnaire (Harvard, 1988). 1306 study participants completed the food frequency questionnaire. Per the guidelines suggested by Walter Willett [21] for excluding individuals with implausible reported energy intake, 40 participants were excluded due to reported caloric intake that was very low (< 500 calories per day if female or < 800 calories per day if male), or very high (3500 or higher if female, 4000 or higher if male), leaving 571 participants with type 1 diabetes and 696 controls in this analysis.
Cardiovascular Risk Factors
Participants completed a baseline examination between March 2000 and April 2002. Anthropometric measurements were obtained, including height, weight, minimum waist circumference (measured at the smallest point between the 10th rib and the iliac crest, over bare skin, in duplicate), and hip circumference (measured at the maximum circumference of the buttocks, in duplicate). Body mass index (BMI) was calculated in kg/m2. Resting systolic blood pressure (SBP) and fifth-phase diastolic blood pressure (DBP) were measured three times while the patients were seated, following a 5-minute rest, and the second and third measurements were averaged. Hypertension was defined as a blood pressure ≥ 140/90, or current antihypertensive treatment. Participants completed standardized questionnaires, including medical history, Rose angina, medication inventory, insulin dose record, physical activity, alcohol and tobacco use, and family medical history.
Following a 12-hour fast, participants came to the clinic in the morning for blood collection, as previously described. Lipids (total cholesterol, HDL-cholesterol, LDL-cholesterol, and triglycerides and calculated non-HDL [total cholesterol minus HDL-cholesterol]), fasting glucose and HbA1c were measured. Albumin excretion rate (AER) was calculated from urinary albumin measured on two timed overnight urine samples, and the results from the two nights were averaged. Abdominal fat at the lumbar 4-5 region was quantified by CT, and intra-abdominal fat (IAF) and subcutaneous fat volumes were determined. Estimated glucose disposal rate (EGDR) was calculated according to the formula published by the Pittsburgh Epidemiology of Diabetes Complications Study and derived from euglycaemic hyperinsulinemic clamps performed in 24 patients with type 1 diabetes: EGDR = 24.31 – 12.22*(waist/hip ratio) – 3.29*(hypertension) – 0.568*(HbA1c) [22].
CAC measurement by EBCT
Two sets of high resolution, noncontrast, contiguous 3-mm tomographic images were acquired at 100-ms exposure on an Imatron C-150XLP EBCT scanner (Imatron, San Francisco, CA) as previously described [23]. The two sets of scans were acquired within 5 minutes, and CAC scores were averaged.
Statistical Analysis
Variables were examined for normality, and non-normally distributed variables (triglycerides, visceral fat and subcutaneous fat) were log transformed. Differences in risk factors between men and women with type 1 diabetes and without diabetes were examined using a t-test. A Chi-Square test for goodness of fit was used to determine if categorical risk factors differed between patients with type 1 diabetes and non-diabetic participants.
Correlations between dietary macro- and micro-nutrients and CHD risk factors were examined using Pearson correlation coefficients. Logistic regression analysis was used to examine the relationship between presence of coronary artery calcium (0 vs. any coronary artery calcium) and dietary macro- and micro-nutrients.
Each dietary factor's association with presence of CAC was examined in a logistic regression model adjusted for age, sex, total daily kilocalories of intake and diabetes status (Model 1), and then potential mediators of the relationship between dietary factors and presence of CAC were examined by individually adding them to Model 1.
Informed consent
All study participants provided informed consent, and the study protocol was approved by the Colorado Multiple Institutional Review Board.
Characteristics of study participants are shown in Table 1. Study participants with type 1 diabetes were significantly younger than participants without diabetes, both among men and women. Only 18% of men and 22% of women met the ADA's goal of a HbA1c <7%. Men with type 1 diabetes had less intra-abdominal fat (IAF), a smaller average waist circumference, lower total and LDL-cholesterol, lower triacylglycerol, and higher HDL-cholesterol than men without diabetes. Similarly, women with type 1 diabetes had less IAF, lower total and LDL-cholesterol, lower triacylglycerol and higher HDL-cholesterol than women without diabetes. Physical activity levels did not differ by diabetes status among either men or women, but AER and CAC were significantly increased among participants with type 1 diabetes.
Table 1
Table 1
Characteristics of Study Participants by Gender and Diabetes Status
Daily intake in kilocalories per kg body weight did not differ in men by diabetes status, but women without diabetes reported a higher daily intake of kilocalories per kg body weight than women with type 1 diabetes. However, both men and women with type 1 diabetes reported consuming less of their daily calories as carbohydrate (CHO), and more as fat and protein than non-diabetic individuals. In addition, saturated fat intake as a percentage of daily calories was significantly higher in both men and women with type 1 diabetes than in men and women without diabetes. Glycaemic index (GI), which is the ratio of a food's influence on blood sugar levels (2 hour glucose area under the curve) compared to glucose and multiplied by 100, was similar in all groups. However, glycaemic load, which is the carbohydrate content in grams multiplied by the GI and then divided by 100, was significantly lower in both men and women with type 1 diabetes compared to control men and women.
Figure 1 shows adherence to dietary guidelines (ADA, AHA, and DRI) in the cohort, by diabetes and gender. Significantly fewer individuals with type 1 diabetes met the DRI goal for total fat intake (20-35% of daily intake) than controls, and fewer people with type 1 diabetes met the goal for saturated fat intake of < 10% of daily calories. Fewer adults with type 1 diabetes than controls met the goal of obtaining 45-65% of daily caloric intake from CHO, but nearly all participants met the recommended goals for protein intake (10-35% of daily intake). Adherence to guidelines for intake of folate, Vitamin E calcium and fiber did not differ by diabetes status. All women met the daily recommended intake of Vitamin C, while control men had significantly lower adherence to Vitamin C guidelines than men with type 1 diabetes. Less than half of study participants met calcium guidelines, with calcium intake lowest among control men and significantly lower than in men with type 1 diabetes. Fiber intake did not differ by diabetes status, but only 6% of men in both groups met fiber guidelines, while 30% of women with type 1 diabetes and 31% of women without diabetes met the fiber guidelines.
Figure 1
Figure 1
Percentage of study participants meeting dietary goals for macro- and micro-nutrients by gender and diabetes status (white bars: Male T1D; light gray bars: Male non-diabetic; dark gray bars: Female T1D; black bars: Female non-diabetic)
We then examined whether the dietary composition was correlated with CHD risk factors, including total cholesterol, LDL- and HDL-cholesterol, triacylglycerol, non-HDL cholesterol, Apolipoprotein B, HbA1c, BMI, IAF volume, waist circumference and EGDR. As shown in Table 2, the percentage of calories from fat, the percentage of calories from saturated fat, and the percentage of calories from monounsaturated fatty acids (MUFA) were all significantly positively correlated with total and LDL-cholesterol, non-HDL cholesterol, Apolipoprotein-B, HbA1c, BMI, IAF, waist circumference and DBP, and negatively correlated with EGDR. The percentage of calories from trans fat and the percentage of calories from polyunsaturated fatty acids (PUFA) were also significantly positively correlated with LDL-cholesterol, non-HDL cholesterol, Apolipoprotein-B, BMI, IAF, waist circumference, and DBP, and negatively correlated with EGDR. A higher average dietary glycaemic index was associated with lower HDL-cholesterol and EGDR, and higher triacylglycerol, non-HDL cholesterol, Apolipoprotein-B, IAF, SBP and DBP. On the other hand, increased carbohydrate intake was significantly negatively correlated with total, LDL- and HDL-cholesterol, non-HDL cholesterol, Apolipoprotein-B, HbA1c, BMI, IAF, waist circumference and DBP, and significantly positively associated with EGDR.
Table 2
Table 2
Pearson Partial Correlation Coefficients for Dietary % Intake of Fats and Carbohydrates, Adjusted for Age, Sex, calories per day and type 1 diabetes
Univariate associations between variables of interest and CAC were explored (Table 3), and all covariates were significantly associated with the presence of CAC except for intake of protein and glycaemic index. The relationship between dietary composition and presence of CAC was then examined in logistic regression models, shown in Table 4. Model 1 was adjusted for age, sex, total kcal intake per day and diabetes status, and interaction terms for diabetes status and each dietary variable were included but non-significant (p>0.10) and therefore were dropped. A high fat diet (>35% fat), saturated fat as a percentage of calories, and protein intake as a percentage of calories were associated with increased odds of CAC when adjusted for Model 1, and when further adjusted for triacylglycerol and HbA1c. Protein intake remained associated with the presence of CAC when adjustment was made for HDL- and LDL-cholesterol, hypertension, physical activity, and EGDR, and a high fat diet remained significantly associated with CAC when adjusted for HbA1c and AER. The percentage of calories from carbohydrate was associated with decreased odds of CAC when adjusted for Model 1 (age, sex, total kcal intake per day, diabetes status), and remained significantly associated with reduced odds of CAC when further adjusted for lipids, hypertension, physical activity, HbA1c, and AER. Associations between high fat diet, saturated fat, carbohydrate and protein intake and CAC were all attenuated when adjustment was made for BMI. Glycaemic index was not associated with CAC in any of the models. A fully adjusted model (excluding EGDR and non-HDL cholesterol as these variables are a linear combination of other variables) revealed that the relationships between dietary variables and CAC were not significant when adjusted for all other variables of interest.
Table 3
Table 3
Univariate associations of covariates with coronary artery calcium
Table 4
Table 4
Odds Ratios and 95% Confidence intervals for Association of Dietary Macronutrients and Coronary Artery Calcium
Finally, in order to explore inter-relationships between dietary components, a forward selection logistic regression model was fitted, with age, diabetes status, high fat diet, protein intake, carbohydrate intake, and glycaemic index forced into the model (Model 5). Additional variables which entered the model were triacylglycerol, BMI, and EGDR, and an interaction term for protein intake and diabetes status. Protein intake was significantly associated with presence of CAC only among participants with type 1 diabetes when adjusted for other dietary variables.
In the present study we found that adults with longstanding type 1 diabetes consume a diet that differs significantly from their non-diabetic spouses and friends and community controls, despite dietary guidelines that are the same for both groups for dietary macronutrients. Adults with type 1 diabetes reported eating more fat and saturated fat and less carbohydrate than the participants without diabetes. In particular, few men and women with type 1 diabetes met the guidelines to restrict saturated fat intake to less than 10% of daily intake, and almost none met the more stringent guideline for intake of saturated fat less than 7% of daily calories which applies to people with elevated LDL-cholesterol, CHD or CHD risk equivalent. Less than half of men and women with type 1 diabetes met the recommendations for total fat intake (20-35% of daily intake). Male and female controls, who were recruited from spouses and friends of participants with type 1 diabetes as well as the community, had significantly higher adherence to the guidelines from the AHA and IOM, which apply to both adults with and without diabetes. Fiber intake was low among all participants, particularly males.
This study has some important limitations. The dietary intake data are self-reported, and there is the possibility of bias or misclassification, especially since patients with type 1 diabetes may be more accustomed to answering questions regarding their diet. In addition, diet questionnaires were not completed by some of the study participants and 40 diet questionnaires were excluded from the analysis due to excessively low or high reported caloric intake. These 40 study participants who were excluded did not differ significantly from those included in the analysis in terms of age, percent of daily calories consumed as fat, carbohydrate, protein, or saturated fat, CHD risk factors, or distribution by sex and diabetes. An additional consideration is that 33% of controls (232/696) in the study were the spouse or live-in partner of a patient with type 1 diabetes. Couples who live together may eat a diet that is more similar and share other lifestyle risk factors for CHD than independent individuals, which may cause our study to underestimate differences in dietary habits between adults with and without type 1 diabetes.
The results from our study add to those of the SEARCH study [9], demonstrating that both adolescents and adults with type 1 diabetes in the United States eat more fat and saturated fat than recommended by the ADA and AHA, with correspondingly lower carbohydrate intake. Our results demonstrating poor dietary compliance are also consistent with reports from studies in Spain and Italy. Reported total fat and cholesterol was excessive among 209 adults with variable (4 months – 41 year) duration of type 1 diabetes in Italy, although patients had lower overall energy intake as well as lower absolute intake of carbohydrate, fat and saturated fat than healthy controls [24]. Adherence to ADA nutritional guidelines were also found to be suboptimal among 93 adults with type 1 diabetes in the Diabetes Nutrition and Complications Trial in Spain [13].
On the other hand, our results contrast with those of a study conducted in Australia where diet was compared between 56 adults with newly diagnosed type 1 diabetes and 47 people without diabetes and no difference was found in intake of fat, saturated fat, carbohydrate or protein [8]. Overall, the diet among adults in Australia was lower in fat and higher in protein than in our study population, and the discrepancy with the current study could be due to cultural differences in diet, differing medical care, or the recent onset of type 1 diabetes in their study group compared to the long-standing duration in the present study.
In our study, higher fat intake was associated with worse glycaemic control, higher total and LDL-cholesterol, increased adiposity and hypertension. In addition, total fat intake, saturated fat intake and GI of the diet were inversely associated with insulin sensitivity, while carbohydrate intake was positively correlated with insulin sensitivity. Our results are consistent with the improvement in insulin sensitivity reported among patients with type 1 diabetes following 3 months of a low fat diet [25].
In addition, in this cohort dietary fat intake above the recommended level was associated with the presence of CAC, although this association was no longer significant when adjustment was made for other known CHD risk factors, including HDL- and LDL-cholesterol, hypertension, BMI, physical activity and insulin sensitivity. This suggests that the association between higher dietary fat intake and CAC is mediated through increased lipids and other CHD risk factors, and that there is not an independent effect of fat intake on CHD development. A higher protein intake was associated with the presence of CAC as well, and this association was only attenuated by adjustment for BMI and AER, suggesting that a high protein diet may contribute to subclinical atherosclerosis through obesity and renal disease, and this is consistent with the ADA guidelines stating that adults with type 1 diabetes who are at high risk for renal disease should limit protein intake [5]. When adjusted for other dietary variables, protein intake was only significantly associated with CAC among adults with type 1 diabetes, further supporting a role of high protein intake in the pathophysiology of both renal and cardiovascular disease in these patients. A higher carbohydrate diet was associated with reduced odds of having CAC, even when adjusted for lipids, hypertension, and physical activity, but this association was no longer significant when adjusted for BMI and EGDR. Of note, adjustment for HbA1c did not attenuate the associations between a high fat diet, saturated fat, carbohydrate or protein intake and CAC, suggesting that the effects of diet are independent of glycaemic control.
Adults with type 1 diabetes are at increased risk for the development of CHD, and diet is an important, modifiable risk factor for CHD. Excess intake of fat and saturated fat among adults in this study was associated with increased CHD risk factors, including higher total and LDL-cholesterol, obesity, and poorer glycaemic control. In addition, a high fat diet was associated with the presence of CAC, a marker of subclinical atherosclerosis. Some patients with type 1 diabetes may limit their carbohydrate intake in order to achieve better glycaemic control or to avoid additional insulin dosing; however, in this study the percentage of daily calories from carbohydrate correlated negatively with HbA1c. These results suggest that patients with type 1 diabetes may benefit from additional dietary counseling to enable them to improve their adherence to dietary guidelines in order to improve long-term cardiovascular outcomes while also addressing the need for achieving adequate glycaemic control.
Table 5
Table 5
Odds Ratios and 95% Confidence intervals for Association of Dietary Macronutrients and Coronary Artery Calcium
ACKNOWLEDGEMENTS
Support for this study was provided by the National Institutes of Health National Heart, Lung and Blood Institute grants R01 HL61753 and R01 HL079611, and Diabetes Endocrinology Research Center Clinical Investigation Core P30 DK57516. The study was performed at the Adult General Clinical Research Center at the University of Colorado Denver Anschutz Medical Center supported by the NIH M01 RR000051, at the Barbara Davis Center for Childhood Diabetes in Denver, CO, and at Colorado Heart Imaging Center in Denver, CO.
Abbreviations
CACCoronary artery calcium
ADAAmerican Diabetes Association
AHAAmerican Heart Association
IOMInstitute of Medicine
DRIDietary Reference Intake
EGDRestimated glucose disposal rate
SBPsystolic blood pressure
DBPdiastolic blood pressure
IAFintra-abdominal fat
MUFAmono-unsaturated fatty acids
PUFApoly-unsaturated fatty acids
GIglycaemic index

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