Study Population

A total of 114 consecutive patients with type 2 DM referred to our institution (Louis Pradel Hospital, Lyon, France) between February 2006 and March 2008 were prospectively recruited and described in a previous report regarding radial and longitudinal function. In the present study, we specifically focused on diastolic function and its relation with systolic function in the same patients and controls.

The recruitment of patients with DM was based on referral to the outpatient clinical department of diabetology of our institution. Patients were included if they met the following inclusion criteria: age between 35 and 60 years, no symptoms or history of heart disease, LV ejection fraction (LVEF) > 55%, absence of regional LV wall motion abnormalities assessed by echocardiography, and no myocardial ischemia, defined by normal results on exercise electrocardiography (54 patients) or dobutamine stress echocardiography (60 patients) in addition to myocardial perfusion (17 patients) within the month before inclusion. Exclusion criteria were the absence of sinus rhythm, coronary and valvular heart diseases, severe renal failure, echocardiographic images unsuitable for quantification, type 1 DM, severely uncontrolled DM (glycosylated hemoglobin < 12%), and uncontrolled blood pressure at rest (defined as systolic blood pressure > 180 mm Hg and/or diastolic blood pressure > 100 mm Hg). Patients had a mean DM duration of 11 ± 7 years and a mean glycosylated hemoglobin value of 7.7 ± 1.4%.

In addition, 88 age-matched healthy controls, previously enrolled in the Asklepios cohort, were included in this study. An overview of the recruitment, exclusion criteria, screening, and participant examination procedures of the Asklepios study has been provided elsewhere. Briefly, the Asklepios cohort is a cohort of 2,524 community-dwelling male and female volunteers, aged approximately 35 to 55 years at study initiation (October 2002), recruited from the twinned communities of Erpe-Mere and Nieuwerkerken, near the Belgian capital of Brussels. This cohort is representative of the general population free from overt cardiovascular disease. From this database, we selected a group of age-matched subjects with the DM group and without cardiovascular risk factors. Asklepios subjects were eligible if they me the following criteria: never smokers, systolic blood pressure < 140 mm Hg and diastolic blood pressure < 85 mm Hg on triplicate measurement, no drug treatments for hypertension, no diabetes, and normal fasting glycemia (glycemia < 110 mg/dL), triglycerides < 150 mg/dL, total cholesterol < 230 mg/dL, low-density lipoprotein cholesterol < 160 mg/dL, high-density lipoprotein cholesterol > 38.5 mg/dL, and serum creatinine < 1.25 mg/dL.

The study protocol was approved by the local ethics committees of Louis Pradel Hospital and the University of Ghent, and all subjects gave written informed consent.

Echocardiography

Transthoracic echocardiography was performed in patients with DM and controls at rest using a commercially available ultrasound system (Vivid 7; GE Vingmed Ultrasound AS, Horten, Norway). All echographic acquisitions were digitally stored from at least three consecutive heartbeats for offline analysis (EchoPAC; GE Vingmed Ultrasound AS), which was performed at Louis Pradel Hospital by two investigators (L.E., C.B.).

Conventional measures (LV end-diastolic and end-systolic diameters, LV mass [LVM], LV volumes, LVEF, and stroke volume [SV]) were obtained as previously described. Briefly, LV diameters were measured using M-mode echocardiography according to the recommended criteria, and LV volumes and LVEF were calculated from the apical views using the modified Simpson’s biplane method. LVM was determined by Devereux’s formula and index to body surface area.

In addition, longitudinal and radial systolic strains of the left ventricle were assessed by speckle-tracking imaging as previously described. As previously reported, a longitudinal systolic strain value ≥ −18% (mean value in controls − 2 SDs) was indicative of preclinical systolic dysfunction, whereas a radial systolic strain value ≤ 45% was considered to indicate preclinical radial systolic dysfunction.

Diastolic Functional Analysis

Diastolic functional parameters in patients and controls were assessed according to the current recommendations of the American Society of Echocardiography and the European Association of Echocardiography.

Diastolic Dysfunction Grading

Using the current guidelines, we assigned patients with DM to one of the four following groups: normal diastolic function or grade I, grade II, or grade III diastolic dysfunction. The first step of this evaluation consisted of the classification of patients according to septal and lateral e′ velocities and left atrial volume index. Patients with septal e′ ≥ 8 cm/sec and lateral e′ ≥ 10 cm/sec and left atrial volumes < 34 mL/m ² constituted the group with normal diastolic function. For the remaining patients, diastolic dysfunction was graded according to the following criteria: E/A ratio, mDT, average E/e′ ratio, and Ar-A time interval ( Figure 1 ).

Classification of diastolic dysfunction in patients with DM according to the American Society of Echocardiography and European Association of Echocardiography recommendations. Av ., Average; LA , left atrial.

Laboratory Measurements

Fasting blood lipid profile, glycemia, and creatinine were measured using standard procedures. In addition, glycosylated hemoglobin and microalbuminuria were also measured in patients.

Statistical Analysis

Statistical analysis was performed using SPSS version 17.0 (SPSS, Inc., Chicago, IL). Normally distributed data are expressed as mean ± SD. Data deviating from normality are expressed as median (interquartile range), and categorical variables are expressed as percentages. Baseline data in the DM group and control group were compared using unpaired t tests for continuous variables and χ ² tests for categorical variables. Then, comparison between patients with DM with and without diastolic dysfunction was also tested using the same procedures.

Multivariate linear regressions were performed in patients with DM and controls to assess independent variables associated with each diastolic functional parameter as follows: E/A ratio, mDT, IVRT, e′, E/e′ ratio, E/e′ ratio/SV, and E/SR _E . The following variables were tested: age, sex, rate-pressure product (systolic blood pressure × heart rate), DM, smoking, history of hypertension, dyslipidemia, body mass index (BMI), triglycerides, low-density lipoprotein cholesterol, creatinine, LVEF, LVM index, and wall stress. All variables significantly associated with each diastolic functional parameter on univariate analysis were entered in each corresponding general linear model. We used a backward elimination procedure with a cutoff of P < .05. In addition, using the same method in patients with DM, we analyzed the association between the same diastolic parameters and the following variables: DM duration, diabetic complications (retinopathy, neuropathy, microalbuminuria), DM imbalance (glycosylated hemoglobin), and medications (insulin, metformin, sulfonylurea, glitazones, angiotensin-converting enzyme inhibitors or angiotensin II antagonists, calcium channel blockers, β-blockers, diuretics, and statins).

Then, the prevalence of preclinical radial and longitudinal systolic dysfunction according to diastolic functional grade was calculated. P values < .05 were considered statistically significant.

Prevalence of Diastolic Dysfunction

Diastolic parameters were altered in patients compared with controls, with lower E/A ratios, longer mDTs and IVRTs, lower e′, and higher E/e′ ratios ( Table 1 ). In addition, the surrogate measure of LV diastolic elastance (E/e′ ratio/SV) was higher in patients than in controls.

According to the current recommendations, 60 patients (53%) presented normal diastolic function and 54 (47%) diastolic dysfunction. Most patients with diastolic dysfunction were grade I (33%), 14% of patients were grade II, and none were grade III ( Figure 1 ). Compared with patients with normal diastolic function, patients with diastolic dysfunction were older, had higher blood pressures and rate-pressure products, and had higher indexed LV end-diastolic volumes ( Table 2 ).

Independent Factors Associated with Diastolic Functional Parameters

Multivariate analysis was performed to determine independent factors associated with diastolic functional parameters ( Table 3 and Supplementary Table 1 ). By univariate analysis, most diastolic functional parameters were associated with DM. However, by multivariate analysis, none of the diastolic parameters except IVRT was independently associated with only DM. E/e′ ratio, mDT, and E/e′ ratio/SV were determined by cofactors other than DM, including age, rate-pressure product, smoking, and history of hypertension. Finally, the following diastolic parameters were not significantly associated with DM: E/A ratio (associated only with age and rate-pressure product), e′ velocity (associated only with age and rate-pressure product), E/SR _E ratio (associated only with history of hypertension and BMI), and E/e′ ratio/ SV (associated only with age, heart rate, and history of hypertension).

Table 3

Independent factors associated with diastolic functional parameters

Diastolic parameter	E/A ratio		E/e′ ratio		e′		mDT		IVRT		E/SR E ratio		E/e′ ratio/SV
	β	P	β	P	β	P	β	P	β	P	β	P	β	P
Age	−0.01	.02			−0.15	<.001							0.16	.008
RPP	−0.00005	<.0001	0.001	<.0001	−0.0004	.009							0.00009	<.0001
Diabetes (yes vs no)			1.8	.001			39	<.0001	0.36	<.001			0.02	.03
Smokers (yes vs no)			−1.8	.001
Hypertension (yes vs no)			1.8	.001							8.5	.004	0.03	.003
BMI					−0.13	.003					0.59	.03
LDL cholesterol							−12	.001

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