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European Journal of Heart Failure 2007 9(10):1044-1050; doi:10.1016/j.ejheart.2007.07.013
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© 2007 European Society of Cardiology

LV systolic impairment in patients with asymptomatic coronary heart disease and type 1 diabetes is related to coronary atherosclerosis, glycaemic control and advanced glycation endproducts

Kjetil Steinea,*, Jakob R. Larsenb, Marie Stugaarda, Tore Julsrud Berga, Magne Brekkeb and Knut Dahl-Jørgensenb

a Aker University Hospital N-0514 Oslo, Norway
b Ullevål University Hospital Oslo, Norway

* Corresponding author. Tel.: +47 22894743; fax: +47 22894008. E-mail address: kjetil.steine{at}medisin.uio.no (K. Steine).


   Abstract
Top
 Abstract
1. Introduction
 2. Methods
 3. Statistical analysis
 4. Results
 5. Discussion
 6. Limitations
 7. Conclusion
 References
 
Aims: To evaluate whether heart failure in type 1 diabetes is linked to poor glycaemic control, coronary atherosclerosis or advanced glycation endproducts (AGEs).

Methods: Twenty six patients with type 1 diabetes (mean duration 32±5years), and 16 age matched controls were recruited. Mean HbA1c through 18years (HbA1c18), serum levels of AGEs and coronary atherosclerotic burden (CAB) were determined by IVUS. Peak tissue velocities and strain by tissue Doppler imaging were measured in 12 LV regions as an evaluation of LV function.

Results: Systolic tissue velocity was inversely correlated to CAB (r=0.53, p<0.01), to HbA1c18 (r=0.46, p<0.05) and to the duration of diabetes (r=0.46, p<0.05). Systolic strain was inversely correlated to HbA1c18 (r=0.45, p<0.05), to duration of diabetes (r=0.41, p<0.05), and tended to correlate with AGEs (r=0.37, p=0.07). In multiple regression analyses, CAB and HbA1c18 were significant independent predictors for systolic velocity, while AGEs and duration of diabetes were significant predictors of systolic strain.

Conclusion: LV systolic function was impaired by increasing coronary atherosclerosis and worsening of glycaemic control. AGEs might be another mechanism for the increased risk of heart failure in type 1 diabetes.

Key Words: Heart failure • Diabetes type 1 • Advanced glycation endproducts • HbA1c • Coronary atherosclerosis • Tissue Doppler imaging

Received October 20, 2006; Revised April 24, 2007; Accepted July 19, 2007


   1. Introduction
Top
 Abstract
 1. Introduction
2. Methods
 3. Statistical analysis
 4. Results
 5. Discussion
 6. Limitations
 7. Conclusion
 References
 
It has been suggested that the high prevalence of heart failure in type 1 diabetes is associated with poor glycaemic control and coronary atherosclerosis [1]. However, another mechanism might be that crosslinking of advanced glycation endproducts (AGEs) between collagen in the heart muscle cells increases the stiffness of the diabetic myocardium [2,3]. AGEs have therefore been suggested as a mechanism for a specific diabetic cardiomyopathy [1,3,4]. There is, however, no clinical evidence of this diabetic heart failure [2,3].

In recent years, several studies have reported on the incidence of diastolic dysfunction assessed by echocardiography in patients with type 1 and 2 diabetes [5-7]. Diastolic dysfunction has even been demonstrated in adolescents, in young patients with type 1 diabetes [8,9] and in normotensive diabetic patients [10]. Since valvular, hypertensive and ischaemic heart disease were absent in these studies, left ventricular (LV) diastolic dysfunction is thought to be an early sign, which precedes the systolic damage in diabetic heart muscle disease, not associated with coronary atherosclerosis [11].

Previous echocardiographic studies demonstrating diastolic dysfunction in patients with diabetes mellitus have mainly been performed using standard pulsed Doppler, measuring derivations of transmitral pulsed Doppler early—(E) and atrial (A) filling waves and pulmonary vein flow [5-10]. However, these methods are all based on flow, and thus reflect LV global diastolic function indirectly. Using the new technique of tissue Doppler imaging (TDI), it is possible to examine LV myocardial function by velocity measurements directly in the LV myocardium. Recent studies using TDI, suggest impaired LV diastolic and even systolic function in the diabetic heart [4,12-15].

The aim of the present study was to explore the mechanisms associated with the increased risk of heart failure in patients with type 1 diabetes. Standard echocardiography and TDI were used to assess LV function in a cross-sectional study of patients with long-term type 1 diabetes, with no symptoms of coronary heart disease. All patients had previously undergone coronary angiography and intravascular ultrasound (IVUS) of the coronary arteries, and coronary atherosclerotic burden (CAB) had been assessed [16]. We also wanted to investigate whether early impairment of LV function was related to AGEs (as an indication of a specific diabetic cardiomyopathy), to coronary atherosclerosis, or to glycaemic control.


   2. Methods
Top
 Abstract
 1. Introduction
 2. Methods
3. Statistical analysis
 4. Results
 5. Discussion
 6. Limitations
 7. Conclusion
 References
 
2.1. Patients and normal individuals
All patients were participants in the Oslo study which recruited 45 patients with type 1 diabetes, in 1982 [17]. Results of the Oslo study showed that intensive insulin treatment with multiple injections or pump treatment was effective in delaying the development of late microvascular complications in these patients [17]. Of these 45 patients, two patients have died due to chronic lung disease and breast cancer, and four patients have been lost to follow-up. Therefore 39 patients from the original Oslo study remained and were included in a recent study by Larsen et al. [16]. Six of the 39 patients showed an abnormal exercise ECG with >1 mm ST-segment depression, but none experienced chest pain [16]. Twenty nine of the 39 patients included in the Larsen study underwent coronary angiography and IVUS examinations and were available for inclusion in the present study. However, two patients refused to participate and one patient showed an abnormal velocity configuration with a systolic peak tissue velocity of 9.8 cm/s, far beyond two standard deviations of the mean velocity in the diabetic group, and was thus excluded from all analyses. Therefore, 26 patients were included in the present study, which was performed approximately one year after the coronary angiograms and IVUS. Except for one coronary bypass operation as a result of the study by Larsen et al. [16], none of these patients had experienced any cardiovascular events.

Sixteen healthy, sex and age matched volunteer subjects from the medical staff at Aker University Hospital were also included for comparison. Control subjects with a history of diabetes, coronary, renal or other severe chronic disease requiring medication, hypertension treated by medication or blood pressure >140/90 mm Hg, were excluded. all control subjects underwent similar echocardiographic and clinical examinations to the diabetic group; however, no blood samples were taken. The study was approved by the Regional Ethics Committee, and all patients gave written informed consent prior to the study.

2.2. Coronary angiograms and intracoronary ultrasound
A detailed report of the exercise ECGs, coronary angiograms and IVUS examinations is described elsewhere [16]. Vessel stenoses >50% of the lumen diameter were classified as significant. Three patients had three-vessel, one had two-vessel and three had one vessel disease.

Intimal thickness of >0.3 mm in any segment of the coronary arteries by IVUS was considered significant for atherosclerotic plaque formation [18]. As defined in the American Heart Association's grading criteria for coronary arteries, 8-10 segments were examined in each patient [19]. In each segment, the maximal stenosis was identified, and the corresponding cross-sectional vessel area, including the intima-media and lumen areas, was measured [19]. The plaque area was calculated as the difference between the vessel area and the luminal area [19]. Percent vessel area stenosis was defined as plaque area divided by vessel area multiplied by 100 [16,19]. For the purpose of statistical analysis, the mean percent vessel area stenosis of all segments analyzed was calculated in each patient, and identified as CAB [16].

2.3. Blood samples
HbA1c was performed by DCCT standardized HPLC methods (normal reference values 4.5-6.4%, CV<3%) and measured three to four times each year over 18 years in each patient [16]. Thus, HbA1c18 is the mean HbA1c measured over this 18 year period. Serum levels of AGEs were determined during the invasive coronary study using a DELFIA-fluorescence immunoassay (Wallac, Turku, Finland) by a previously reported method [20]. While HbA1c18 and AGEs were measured approximately one year before, actual HbA1c, p-glucose (not fasting) and creatinine were measured the same day as the echocardiographic examination.

2.4. Standard echocardiography and tissue Doppler imaging
All echocardiographic recordings were performed with the participants in left lateral decubitus position and breath holding in mid expiratory phase from standard-parasternal long axis or apical views using a 2.5 Mhz transducer (System 5, GE Vingmed Ultrasound, Horten, Norway). The ECGs were recorded simultaneously. The digital data were transferred to a Macintosh computer for off-line measurements, which were performed using customized software (Echopac, GE Vingmed Ultrasound, Horten, Norway).

LV internal dimensions and septal and posterior wall thicknesses were measured, and LV mass calculated according to the recommendations of the American Society of Echocardiography [21,22]. LV volumes were calculated using the modified Simpson's rule from biplane apical views [23]. The systolic LV long axis excursion by M-mode was measured at septal and lateral mitral annulus [24]. LV diastolic function was assessed by peak velocities of pulsed Doppler transmitral E and A filling waves, the E/A ratio, E deceleration time, and peak velocities of systolic and diastolic pulmonary vein flow [25].

Using apical images from four- and two chamber and long axis views, peak- systolic and diastolic early (E') and atrial (A') tissue velocities were measured in the basal and middle segments of LV septal-, lateral-, inferior-, anterior-, posteroinferior- and anterolateral walls. The peak tissue velocities from these twelve segments were averaged to obtain an evaluation of overall LV longitudinal systolic and diastolic function. Whereas strain is a measure of tissue deformation, its temporal derivative, strain rate, is a measure of the rate of tissue deformation [26]. Strain was calculated as (ls–ld)/ld, where ld and ls are local myocardial lengths at end-diastole and systole respectively. Thus systolic strain has a negative value, but multiplied by 100 it becomes a percentage. Strain rate is calculated as (Va–Vb)/l, where Va and Vb are the velocities in point a and b, and l is the distance (8 mm) between these two points [26].

To estimate LV filling pressure non-invasively, we calculated the ratio between transmitral peak E wave by pulsed Doppler and peak early diastolic tissue velocity (E'lat) of the lateral mitral annulus, E/E'lat [27]. The measurements of all M-mode and pulsed Doppler data were done as an average of three consecutive heart beats, while the two-dimensional LV volumes, and the tissue velocity, strain and strain rate parameters were measured from one heart cycle.

All echocardiographic recordings and analyses, the standard as well as the new TDI modalities, were performed by the same person (KS), who was blinded to the group (diabetic or control) and the clinical status of the diabetic patients.


   3. Statistical analysis
Top
 Abstract
 1. Introduction
 2. Methods
 3. Statistical analysis
4. Results
 5. Discussion
 6. Limitations
 7. Conclusion
 References
 
The data are presented as sample mean values±standard deviation (SD). For comparison of the data unpaired t tests were performed. Pearson's correlation test, and simple and multiple regression analysis were also used. p<0.05 was regarded as statistically significant. CAB, HbA1c18, duration of diabetes and AGEs were chosen as predictor variables in the multiple regression analyses, since they reflected the main purpose of the study, and since they all showed significant relations to either peak systolic-tissue velocity or strain in the simple regression analyses.


   4. Results
Top
 Abstract
 1. Introduction
 2. Methods
 3. Statistical analysis
 4. Results
5. Discussion
 6. Limitations
 7. Conclusion
 References
 
Clinical characteristics of the diabetic patients and the controls are listed in Table 1. Systolic blood pressure and heart rate were significantly higher among the diabetic group as compared to the control group (Table 1). The ECGs were normal in both groups. Six patients with type 1 diabetes were being treated with anti-hypertensive drugs.


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  		Table 1 Clinical characteristics of patients with type 1 diabetes and controls

 
In the diabetic patients HbA1c18 was 8.2±1.0%, and serum levels of AGEs was 3.4±1.9 U/ml. Actual HbA1c and glucose at the time of echocardiographic examination were 7.0±1.0% and 12.1±6.2 mmol/l, respectively. One patient had slightly increased creatinine levels, 131 µmol/l, while all others were within normal limits (70-125 µmol/l). The coronary atherosclerotic burden (mean percent vessel area stenosis of all segments) was 30.2±19.3%.

4.1. Standard echocardiography
Peak transmitral E and A velocities were significantly higher in the diabetic group than among the controls, 78±15 vs. 69±11 cm/s (p=0.05) and 53±10 vs. 43±12 cm/s (p<0.01), respectively (Table 2). All other pulsed Doppler of transmitral or pulmonary vein flow data and two-dimensional and M-mode data were similar in the two groups (Table 2).


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  		Table 2 Two-dimensional, M-mode and pulsed Doppler data of the left ventricle in patients with type 1 diabetes and control individuals

 
4.2. Tissue Doppler imaging (TDI)
Although there was a tendency towards significant differences between the diabetics and the controls in several of the TDI indices, i.e. E' and E/E'lat, none reached significant difference (Table 3).


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  		Table 3 Tissue Doppler imaging data in patients with type 1 diabetes and controls

 
4.3. Correlations between LV function by TDI and four predictor variables
Peak systolic tissue velocity showed significant correlations to CAB (r=–0.53, p<0.01) (Fig. 1), to HbA1c18 (r=–0.46, p<0.05 and to duration of diabetes (r=–0.46, p<0.05), but not to AGEs (r=0.07, p=0.75). Peak systolic strain correlated significantly to HbA1c18 (r=–0.45, p<0.05), to duration of diabetes (r=–0.41, p<0.05), and tended to correlate with AGEs (r=–0.37, p=0.07) (Fig. 2), but not to CAB (r=0.22, p=0.78). E/E'lat was significantly correlated to HbA1c18 (r=0.54, p<0.01) (Fig. 3), but not to CAB (r=0.13, p=0.52), AGE (r=0.22, p=0.28) or duration of diabetes (r=0.31, p=0.13). Peak systolic strain rate was not significantly related to any of the four predictor variables.


Figure 01
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  		Fig. 1 Figure showing a significant negative correlation between left ventricular (LV) peak systolic tissue velocity and coronary atherosclerotic burden in 26 patients with long-term type 1 diabetes. Peak systolic tissue velocities were measured in the basal and middle segments of LV septal-, lateral-, inferior-, anterior-, posteroinferior- and anterolateral walls and averaged to get an assessment of LV overall longitudinal systolic function.

 


Figure 02
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  		Fig. 2 Figure showing a near significant association between LV peak systolic strain by tissue Doppler imaging and AGEs (advanced glycation endproducts) in 25 patients with long-term type 1 diabetes.

 


Figure 03
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  		Fig. 3 Correlation plot showing a significant positive association between the ratio between transmitral early diastolic (E) velocity by pulsed Doppler and peak early velocity (E'lat) at the lateral mitral annulus, E/E'lat, by tissue Doppler imaging and HbA1c18 (mean HbA1c through 18 years) in 26 patients with long-term type 1 diabetes. E/E'lat is a non-invasive echocardiographic index for LV filling pressure.

 
By multiple regression analyses including CAB, HbA1c18, AGEs and duration of diabetes as independent variables, CAB and HbA1c18 were significant predictors of peak systolic velocity (r=0.62, r2=0.39, p<0.01), while AGE and duration of diabetes were significant predictors for peak systolic strain (r=0.61, r2=0.37, p<0.01). One patient had an AGEs concentration of 12.2 mmol/l which exceeded 2 SD of the mean; this value was considered as an outlier, and the patient was excluded in all the simple as well as multiple regression analyses including AGEs.

Besides a significant correlation between the transmitral E/A ratio and CAB (r=–0.43, p<0.05), there were no other significant relationships between standard echocardiographic indices reflecting LV systolic or diastolic function and the four diabetic related predictor variables.


   5. Discussion
Top
 Abstract
 1. Introduction
 2. Methods
 3. Statistical analysis
 4. Results
 5. Discussion
6. Limitations
 7. Conclusion
 References
 
To our knowledge, this is the first study to show that LV peak systolic tissue velocities are related to coronary atherosclerosis and glycaemic control, and that LV peak systolic strain is associated with AGEs, in patients with long-term type 1 diabetes with thoroughly classified coronary atherosclerotic disease and measurements of HbA1c, over long-term follow up.

In the present study, seven of the 26 patients had one or more significant stenosis as assessed by coronary angiography, and all had atherosclerotic plaque with significant thickening of the intima as assessed by IVUS. None of the patients had chest pain on exercise ECG [16]. These results highlight the presence of a considerable amount of silent coronary atherosclerotic disease, which was also recently shown by DCCT [28] in type 1 diabetes. Moreover, peak tissue velocities, as measured in the present study, reflect contraction of longitudinal fibres, which are mainly located in the subendocardium and thus most vulnerable to ischaemia [29-31]. We also investigated whether the formation of AGEs in tissues might be a mechanism for diastolic and systolic LV dysfunction in type 1 diabetes, using TDI. Measurements of strain offer advantages over regional myocardial tissue velocities, which are affected by tethering from other myocardial segments. This means, in the current approach with a longitudinal vector from base to apex, that basal local tissue velocities may be reduced by injured tissue located in LV apex, while strain may not [32]. Thus, regional strain reflects regionally impaired LV function, by i.e. ischaemia, better than tissue velocities [32,33]. The association between AGEs and strain in the present study might therefore be the result of local ischaemia rather than an expression of a specific diabetic cardiomyopathy. On the other hand, since AGEs mainly reflect crosslinking of myocardial collagen, we can not exclude AGEs as a possible mechanism for the increased risk of heart failure in these patients [2,3,20]. We propose, however, that the majority of patients with type 1 diabetes and diastolic dysfunction, who are classified as non-ischaemic, probably have clinically important coronary atherosclerosis as the main cause of their LV dysfunction [4-7,10,12-15]. The existence of a specific diabetic cardiomyopathy not associated with coronary atherosclerosis therefore might not be as important as previously thought [1,3,4].

Since TDI is a relatively new echo modality, there are relatively few studies of LV function and type 1 or 2 diabetes [4,12-15]. The studies of Shishehbor et al. and Hansen et al. in type 1 diabetes, both showed impaired LV systolic and diastolic function by spectral tissue pulsed Doppler [4,12]. Shishehbor et al. also reported a similar correlation between non-invasive LV filling pressure E/E' and regular HbA1c to our study, as did Vinereanu et al. in patients with type 2 diabetes [4,13]. Fang et al. showed an association between regular HbA1c and strain in type 2 diabetes [14,15] similar to the present study. Compared to other studies, the present investigation shows small changes in several of the LV systolic and particularly the diastolic parameters of TDI or standard echo modalities [4-10,12-14]. Although our study subjects did not differ markedly in determinants, such as sample size, age or duration of diabetes [4-9,12-14], they did receive intensified insulin treatment for 14-18 years, and therefore may have had fewer cardiac abnormalities due to better glycaemic control [16,17].

This investigation showed an increased transmitral pulsed Doppler E filling wave in type 1 diabetes. The main predictors for E are preload and LV relaxation [34]. Our findings of a positive correlation between the estimate for LV filling pressure, E/E'lat, and HbA1c18, and the tendency for an increased E/E'lat among patients with diabetes as compared to the controls, suggests that the increased E is probably caused by increased filling pressure. The similar E/A ratio in the diabetes and the control groups might therefore be due to pseudo-normalization, which indicates diastolic dysfunction in these patients.


   6. Limitations
Top
 Abstract
 1. Introduction
 2. Methods
 3. Statistical analysis
 4. Results
 5. Discussion
 6. Limitations
7. Conclusion
 References
 
Serum levels of HbA1c18 and AGEs were all sampled approximately one year before the echocardiographic examinations. Since HbA1c levels over 18 years, remained constant in the individual patients, we do not consider that this time gap of one year was important. Unfortunately, there are no data on AGEs and the consistency of measurement changes over time in type 1 diabetes. However, a recent study in type 2 diabetes with optimization of insulin treatment showed little change in serum levels of AGEs over a time period of 6 months [35]. Assessment of AGEs should therefore be repeated in another study, with a shorter interval between blood sampling and the echocardiographic examinations.

The E'lat in the E/E'lat ratio is normally based on pulsed wave tissue Doppler, where the sample volume is placed on the septal or the lateral mitral annulus [27]. From these spectral traces E'lat is measured, not from the TDI loop as in the present study. Since these velocities reflect an average of several local velocities (pixels), they are to some extent reduced as compared to tissue spectral pulsed wave Doppler. The E/E'lat ratio in the present study is therefore slightly larger.


   7. Conclusion
Top
 Abstract
 1. Introduction
 2. Methods
 3. Statistical analysis
 4. Results
 5. Discussion
 6. Limitations
 7. Conclusion
References
 
In 26 patients with long-term type 1 diabetes and a high prevalence of silent coronary artery disease, there was an impairment of LV systolic function, which was associated with an increase in coronary atherosclerosis and worsening of glycaemic control; although this seems to be important, it is not necessarily the cause of this early deterioration in LV systolic function. The correlation between AGEs and peak systolic strain might suggest tissue protein glycation as another mechanism for the increased risk of heart failure in type 1 diabetes.


   References
Top
 Abstract
 1. Introduction
 2. Methods
 3. Statistical analysis
 4. Results
 5. Discussion
 6. Limitations
 7. Conclusion
 References
 

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R. Mogelvang, P. Sogaard, S. A. Pedersen, N. T. Olsen, P. Schnohr, and J. S. Jensen
Tissue Doppler echocardiography in persons with hypertension, diabetes, or ischaemic heart disease: the Copenhagen City Heart Study
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