Ultrasonic videodensitometric analysis of myocardium in end-stage renal disease treated with haemodialysis

Vitantonio Di Bello, Vincenzo Panichi, Roberto Pedrinelli1, Davide Giorgi, Massimiliano Bianchi, Alessio Bertini, Daniele Taccola, Stefano De Pietro, Enrica Talini, Marco Paterni2 and Costantino Giusti

1 Dipartimento di Medicina Interna e di Cardiologia, University of Pisa and 2 Istituto di Fisiologia Clinica, CNR, Pisa, Italy

Correspondence and offprint requests to: Vitantonio Di Bello, MD, Dipartimento di Medicina Interna, Università di Pisa, via Roma, 67, I-56100 Pisa, Italy.



   Abstract
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
Background. The aim of this study was to investigate videodensitometric parameters of the myocardium, in dialysis patients, who represent a complex pathophysiological model of pressure–volume overload, and in essential hypertensive patients with the same level of left ventricular mass.

Methods. We compared a group of male dialysis patients (D) with two groups: hypertensive patients (H) with comparable left ventricular mass and normotensive healthy subjects as controls (C). The groups (n=15 each) were age- (53±9 years) and gender-matched. Quantitative analysis of echocardiographic digitalized imaging was performed to calculate the mean grey level (MGL) and cyclic variation index (CVI).

Results. The haemodialysis patients had a significantly lower CVI compared with hypertensives and controls both for septum (D): -2.5±17.4% vs (H); 11.8±17% vs (C); 43.2 ±15.4% (P<0.001) and for posterior wall (D): -10.1±261% vs (H); 14.2±14.7% vs (C); 46.6.2±17.2% (P<0.001). A significant inverse relationship was found between intact parathyroid hormone (iPTH) and CVI.

Conclusion. Abnormalities of two-dimensional echocardiographic grey level distribution are present in both haemodialysis patients and hypertensive patients, but seem unrelated to the degree of echocardiographic hypertrophy. These videodensitometric myocardial alterations are significantly higher in dialysis patients than in hypertensive patients with the same extent of left ventricular hypertrophy. The iPTH level may play a role in the development of the ultrasonic myocardial alterations, which probably represent an early stage of uraemic cardiomyopathy.

Keywords: echocardiography; hypertension; uraemic cardiomyopathy; haemodialysis; videodensitometric ultrasonic tissue characterization



   Introduction
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
Cardiac disease represents the major cause of death in dialysis patients (40%); the death rate in a cohort of dialysis subjects aged 45–64 years was 3.5 higher than in an age-matched group without renal disease [1]. Left ventricular dysfunction and chronic heart failure are frequent in chronic renal failure, and cardiovascular mortality remains high in these patients. For these reasons, better and early detection of cardiac involvement in these patients is important with respect to the diagnostic, therapeutic and prognostic perspectives. Quantitative videodensitometric analysis of echocardiographic data represents a useful approach which permits characterization of myocardial tissue by ultrasound (quantitative texture analysis) [29]. Epidemiological, autopsy and functional studies in end-stage renal failure patients with haemodialysis support documented histopathological involvement of the myocardium including increased myocardial fibrosis [10] and/or a soft deposition of calcium [1113].

The purpose of this study was to analyse the myocardial echo density in a group of haemodialysis patients, compared with an age-, gender- and left ventricular mass (LVM)-matched group of hypertensive patients and normal age-matched sedentary controls. We investigated whether videodensitometry is able to detect some early myocardial ultrasonic textural changes in end-stage renal disease maintained with haemodialysis, and if some differences exist between two models of cardiac hypertrophy, `uraemic cardiomyopathy' and essential hypertensive cardiopathy [1416].



   Subjects and methods
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
Study population
A case-controlled study design included two groups of 15 age-, gender- and LVM-matched patients: haemodialysis (D) and essential hypertensive subjects (H) and one group of 15 age- and gender-matched healthy controls (C).

Haemodialysis group.
Echocardiography was performed within 6 h after the dialysis procedure. The epidemiological and clinical–serological findings of these patients are shown in Table 1Go. At the time of the study, all patients had been on dialysis for at least 6 months. Chronic renal failure (CRF) was due to chronic glomerulonephritis (n=9), chronic interstitial nephritis (n=4) and polycystic kidney disease (n=2). Eight patients were treated with haemodialysis (blood flow 350 ml/min, dialysate flow 500 ml/min) using synthetic membranes (n 5 PAN and n 3 Polysulphone) and a standard bicarbonate dialysate (NA 140 mmol/l, K 2.0 mmol/l, Ca 1.5 mmol/l, HCO3 35 mmol/l). Seven patients were treated with haemodiafiltration (HDF) with PAN membrane (1.6–1.8 m2), bicarbonate dialysate as above and a lactate-buffered (42 mmol/l) reinfusate fluid (reinfusate flow 3 l/h). Six patients were treated with antihypertensive medication (four with calcium channel blockers and two with clonidine). The mean intradialysis weight gain was 2.5±1.5 kg. No hypotensive episodes occurred during or after the dialysis procedure on the same day on which echocardiography was performed. Blood samples for biochemical examinations were taken on the day of echocardiography between 8.30 and 9.30 am. Total cholesterol and triglycerides were assayed by enzymatic colorimetric techniques (Boehringer-Mannheim, Mannheim, Germany), white cell count and haematocrit by automated methods (H1 Technicon, Cavenago Brianza, Bayer Diagnostici, Italy), and urea, creatinine and glucose by standard techniques. Total alkaline phosphatase, total calcium and phosphate were determined using standard laboratory methods (Technicon Autoanalyzer). Intact parathyroid hormone (iPTH) was determined by an immunoradiometric assay (Nichols Allegro; normal range 10–65 pg/ml) utilizing two different polyclonal antibodies purified by affinity chromography, specific for 34–84 and 1–34 regions, with an intra- and inter-assay coefficient of variability <7%.


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Table 1. Epidemiological and clinico-serological data of dialysis patients
 
Hypertensive patients.
Hypertensive patients with moderate essential arterial hypertension (range of duration: 6–36 months) were recruited from the Department of Cardiology ambulatory patients. Preliminary selection criteria included absence of the following: malignant or accelerated hypertension, congestive heart failure, cardiomyopathy, obesity (body mass index >30 kg/m2), diabetes (fasting blood glucose >6.6 mmol/l, 120 mg/dl), previous myocardial infarction or a history of connective tissue disease. Other criteria were: serum creatinine <106 µmol/l (1.2 mg/dl) and the presence of a normal acoustic window.

Patients were then excluded if valvular heart disease by Doppler analysis (including only very mild aortic or mitral regurgitation) was present, as well as a history or clinical and instrumental findings of myocardial ischaemia (presence of ECG or echocardiographic findings of myocardial ischaemia, such as echocardiographic segmentary abnormalities of myocardial contraction).

The conventional echocardiogram and tissue characterization were performed on the same day.

With these criteria, we recruited 15 subjects with hypertension who had completed a full clinical, biochemical and instrumental work-up for secondary hypertension, including fundoscopic examination, urinalysis, renal echo-Doppler examination, up to an angiographic procedure if needed. All patients had clinically uncomplicated essential arterial hypertension (without the major atherosclerotic complications: renal, retinal, carotid, coronary and leg arteries). Twelve patients were not taking any antihypertensive therapy at the time of the study and only three patients were treated with antihypertensive agents including angiotensin-converting enzyme inhibitors and/or diuretics.

Control group.
Fifteen age- and gender-matched normotensive subjects, without any evidence of organic disease, were recruited from the echocardiography laboratory after documentation of normal sonograms. These subjects underwent blood sampling for biochemical examination of the same previously described parameters.

The demographic features of these three groups are reported in Tables 2 and 3GoGo. According to institutional guidelines, the study was approved by the local Ethical Committee. Systolic (SBP) and diastolic (DBP) (Korotkoff V phase) blood pressure was measured during the echocardiographic examination [17].


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Table 2. Clinical parameters
 

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Table 3. Conventional echo-Doppler parameters
 
Conventional Doppler echocardiography
Conventional echocardiographic studies were performed with a Hewlett-Packard 77020A phased array sector scanner with a 2.5 or 3.5 MHz transducer. Two-dimensional images were obtained in the parasternal long and short axis views and apical two- and four-chamber views. Left ventricular diameters, septum and posterior wall thicknesses were measured [18] and left ventricular percentage fractional shortening was calculated. Furthermore, relative wall thickness was calculated as the ratio of twice the posterior wall thickness to the left ventricular internal diameter measured at the end of diastole. LVM was calculated by the Devereux formula (Penn convention) and normalized for body surface area (LVMbs) [19]. The pulsed Doppler trans-mitral flow velocity profile was obtained from the apical four-chamber view, and the sample volume was positioned just below the tip of the mitral valve leaflets at the maximal opening. The following parameters were evaluated: peak E (peak trans-mitral flow velocity in early diastole); peak A (peak trans-mitral flow velocity in late diastole) and the E/A ratio. To assess the reproducibility of these measurements, all recordings were analysed on two separate occasions for intra-observer variability, as well as by a blinded investigator for inter-observer variability. Inter- and intra-observer coefficients of variation averaged 7.5 and 11.4%, respectively. Measurements were derived from the average of at least five consecutive cardiac cycles.

Image digitization
During echocardiography, the grey scale transfer function was adjusted to be linear for the entire video signal range and no reject, no enhancement or dynamic range were used [2,3]. In general, an amplification of 25–30 dB and a depth setting of 18 cm were used. The echocardiographic images were transferred directly to a calibrated video digitization system. Images were converted into 256x256 pixels of 256 grey levels each (0=black, 255=white), with 8 bits of intensity range, by a commercial real-time video-digitizer. One cardiac cycle (R–R waves) was divided automatically into 12 frames independently by heart rate. The images corresponding to the end-diastolic and end-systolic phases, all in long axis projection, were selected according to an optimal visualization of the interventricular septum and the left ventricular posterior wall [2023].

Quantitative texture analysis
A trackball-controlled cursor was used to select the same region of interest of the septum (mid-septum) and posterior wall (mid-posterior), always measuring 32x42 pixels. The analysis was performed during the end of systole and the end of diastole and included only the myocardium. The endocardial and epicardial specular echoes were excluded to avoid artefacts. For each region of interest, a histogram of the echocardiographic grey level distribution was generated. The grey level distribution was plotted on the abscissa and the frequency of the occurrence on the ordinate. The intra-class correlation coefficient (ri) was calculated according to Bland and Altman, using a one-way analysis of variance for repeated measurements. One to three values of mean grey level at end diastole and systole were obtained for both the septum and posterior wall. The correlation coefficient (ri) for septum mean grey level was 0.92 for the diastolic and 0.90 for the systolic sample. The posterior wall mean grey level was 0.89 for the diastolic and 0.91 for the systolic sample.

Grey level difference measurements
The mean grey level in each cavity region (background signal) was subtracted from the absolute mean grey level in each tissue region of the same digitized images for the end-systolic and end-diastolic frames (mean grey level, background corrected: MGL). A quantitative analysis of the shape of the distribution was also performed using skewness and kurtosis of each distribution. The cyclic variation index (CVI) of the grey level amplitude was also calculated according to the formula: (MGLED–MGLES)/MGLEDx100) (Figure 1Go) [2,24].



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Fig. 1. Each panel on the left shows a digitized two-dimensional echocardiographic image of the left ventricle (parasternal long axis view) for the three groups. The graph on the right demonstrates the variations in echo intensity in a region of interest placed at the posterior wall level (in ordinates) during one cardiac cycle arbitrarily divided into 12 frames independent of heart rate for the three groups. Time 0=end-diastolic frame; time 4=end-systolic frame.

 
Statistical analysis
The statistical design of the present investigation is a close case–control study. Continuous variables were expressed as mean±1 SD. Multiple group comparison was performed by analysis of variance followed by Scheffe' test. Kruskall Wallis test was also applied to evaluate better the statistical significance of the differences between the means of the CVI for each group. Intra-group differences were evaluated using Student t-test. Quantitative histogram shape analysis was analysed by the Friedman rank test. Upper and lower 95% confidence limits for the CVI were calculated from the two tails of the Student's t-test distribution using the following formulae: mean +(2.042xSE) and mean -(2.042xSE) respectively. To evaluate the reliability of the videodensitometric method, we applied the analysis of variance for repeated measurements, according to the Bland and Altman method, obtaining the intra-class correlation coefficient (ri). Relationships between videodensitometric and two-dimensional echocardiographic measurements were expressed in terms of linear regression analysis. A P-value of <0.05 was considered to be significant.



   Results
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
The epidemiological and clinico-serological data of the dialysis patients are shown in Table 1Go. Demographic and clinical data of the three examined groups are shown in Table 2Go as mean±SD. The three groups, all males, were similar in age, height and body surface. Only weight was significantly higher in the hypertensive group and controls compared with the dialysis patients, but body mass index was similar in all three groups. Arterial pressure levels were significantly higher in the hypertensive group than in the dialysis patients and controls. The biochemical parameters for hypertensive and control subjects were all within the normal laboratory standard range.

M-mode, two-dimensional and Doppler echocardiographic findings
Conventional echo-Doppler measurements of the three study groups are displayed in Table 3Go. End-diastolic volume, parietal thickness and relative LVM were similar both in the dialysis and hypertensive groups, being significantly higher than in controls. Fractional shortening and the diastolic functional indices were similar in all three groups (Table 4Go).


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Table 4. Ultrasonic textural data (mid-septum)
 
Quantitative textural analysis
Mean values of the MGL both in systole and in diastole and the value of skewness and kurtosis of the distribution of the grey level in each region of interest (ROI) are shown in Tables 4 and 5GoGo. Mean values of the CVI for both the septum and posterior wall are shown in Tables 4 and 5GoGo. The dialysis group had a significantly lower septal (P<0.001) and posterior wall (P<0.001) CVI compared with the hypertensive and control groups (Figure 2Go). Furthermore, this parameter was significantly lower in the hypertensives compared with controls. Individual plot analysis of the CVI in the three groups revealed that this textural parameter is able to differentiate the entire dialysis population from healthy controls, while the hypertensive group showed a lesser degree of alteration of these acoustic textural parameters. No significant differences were found regarding the shape of the distribution of grey levels (i.e. skewness and kurtosis) among the three groups.


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Table 5. Ultrasonic textural data (mid-posterior wall)
 


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Fig. 2. Cyclic variation index at the mid-septum level and at the mid-left ventricular posterior wall for the three groups. See text for the statistical comparison among the groups.

 
Relationship between conventional echocardiographic measurements and quantitative texture analysis data
No significant univariate correlation was found between the corresponding wall thickness and the diastolic MGL of the septum (r=-0.16, P=0.38) and posterior wall (r=0.35, P=0.2) and between the same videodensitometric parameters and LVMbs (r=-0.16, P=0.28). No significant correlation was found between left ventricular fractional shortening and the septal (r=0.19, P=0.38) and posterior wall (r=0.28, P=0.42) CVIs. A low but significant correlation was found between SBP and CVI of the septum (r=0.30, P<0.04). A univariate significant correlation was found only between CVI and iPTH in dialysis patients (Pearson r=-0.50; P<0.02) (Figure 3Go). There was no significant correlation between the septal CVI and systolic arterial pressure in the hypertensive group (r=0.31; P=0.15), while a low but significant correlation was found between the posterior wall CVI and SBP (r=0.45; P<0.02). Furthermore, a significant correlation was found between SBP and LVMbs (r=0.52; P<0.01) in this group. In our groups, age does not appear to influence the echodensitometric parameters.



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Fig. 3. Plot of the inverse correlation between the cyclic variation index of the posterior wall and iPTH in the dialysis group.

 


   Discussion
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
The main and original finding of this study is the detection of a significantly higher degree of alteration of ultrasonic textural parameters in dialysis patients, particularly in the CVI of the septum and posterior wall, compared with age- and LVM-matched essential hypertensive patients (P<0.001) and healthy controls. Another original finding is the low, but significant inverse correlation between iPTH level and CVI values, which could represent one of the possible pathogenic links between dialysis status and myocardial ultrasonic textural dialysis alterations.

Different structural components of the myocardium influence its acoustic properties under physiological and pathological conditions (Rayleigh scattering). Collagen is a primary determinant of both scattering and attenuation of myocardial tissue; a linear relationship was found between integrated backscatter and hydroxyproline content in autopsied human hearts with fibrotic changes associated with remote myocardial infarction [25]. Furthermore, a significant direct correlation was found between collagen content analysed endobioptically and regional echo amplitude [26]. Scatter geometry is another determinant of myocardial reflectivity. In fact, myocardial scattering intensity depends directly on myocyte cellular size; the microstructural arrangement of myocardial cells embedded in a collagen matrix may provide a sufficient local acoustic impedance mismatch to account for the scattering from normal myocardium [27]. The orientation of ventricular muscle fibres might influence myocardial acoustic properties. In fact, the insonification angle might greatly influence the magnitude of both attenuation and backscatter, the backscatter being maximal in a direction perpendicular to fibre orientation. The middle portion of the left ventricular wall is comprised mainly of circumferentially oriented fibre bands. [28] Tissue water content and blood flow both influence myocardial attenuation and scattering. An increase in water content due to tissue oedema and, to a lesser degree, to a reduction in coronary blood flow associated with myocardial ischaemia might influence the acoustic properties of the myocardium. No data are available at the moment regarding the effect of anaemia on the acoustic properties of the myocardium. Some thought must also be given to the dynamic aspect of scattering. According to Wickline et al. [27], peak values occurred at end-diastole and minimal values at end-systole, but these cyclic changes in the echo amplitude are related, although not linearly, to intrinsic myocardial contractile performance.

The results of the present study confirm our previous studies in essential hypertension in which we have demonstrated that chronic pressure–volume overload of hypertension caused an altered pattern of ultrasonic texture [8,9]. In fact, prolonged pressure–volume overload due to arterial hypertension could be responsible for an increase in LVM with an increase in collagen content which probably alters the physiological collagen/myocardium ratio, as demonstrated in experimental and autopsy studies [14–16,29–31).

The high prevalence of left ventricular hypertrophy (LVH) in dialysis patients, in the absence of a history of arterial hypertension and without an association with the aetiology of CRF, represents the result of complex humoral and haemodynamic stimuli which lead to an increase in LVM. The acute and the chronic effects of haemodialysis on cardiac function and structure were well differentiated in our study. We focused on the chronic modifications induced by dialysis and for this reason we observed patients 6 h after the dialysis session under resting conditions. After removal of fluid from the circulating blood volume by ultrafiltration, refilling occurs from the extravascular compartment. This compensatory mechanism may alter cardiac contractility and rate. However, it has been established that in patients affected by CRF undergoing ultrafiltration [32], most of the redistribution of extracellular fluid loss after haemodialysis occurs in the first 2 h after haemodialysis. At 6 h after the end of dialyisis, most of the electrolyte variations occurring during haemodialysis (including ionized calcium increase) are stabilized.

Different risk factors have been ascribed to echocardiographic abnormalities found in dialysis patients [33]; Nowack et al. [34] demonstrated the role of PTH in the development of LVH in dialysis patients. Experimental studies have shown that PTH affects myocardial function [35] and structure. Furthermore, PTH has been considered to be a major uraemic toxin [36] which promotes activation of myocardial fibroblasts and, therefore, the genesis of cardiac fibrosis found in the dialysis population [37]. Autopsy studies have shown pronounced diffuse non-coronary inter-myocardiocytic fibrosis in uraemic patients which is clearly distinct from perivascular fibrosis observed in arterial hypertension and from patchy scars typical of coronary artery disease or myocarditis [38]. Mall et al. [10] documented that the inter-myocardiocytic fibrosis in uraemic patients was significantly more pronounced than that in hypertensive or diabetic type II patients. Kuzela et al. [11] demonstrated soft tissue calcification in the myocardium of uraemic patients undergoing chronical dialysis. Myocardial fibre degeneration, interstitial calcium deposits and dense interstitial fibrosis were predominantly observed. The most severe autopsy lesions consisted of dense fibrous connective tissue containing large irregular calcium deposits.

Previous studies suggest that all biological, experimental and autopsy observations could explain the high incidence of heart failure in dialysis patients, and the worst prognosis of uraemic heart in comparison with essential hypertensive cardiopathy with the same degree of LVM.

With videodensitometry, we documented that dialysis patients have a significantly lower septal and posterior wall CVI compared with hypertensive patients and controls. It is well known that the major determinants of the alteration of videodensitometric patterns are the presence of excess collagen with respect to a normal collagen/myocyte ratio and intramyocardial calcification. These elements have a significantly higher level of acoustic reflection compared with normal structures of the myocardium. The higher degree of myocardial fibrosis and calcification in dialysis patients compared with hypertensive subjects could explain the alteration in myocardial textural parameters in dialysis patients detected by the videodensitometric method.

The systolic and diastolic left ventricular functions were still within the normal range in both the hypertensive and dialysis patients. For this reason, the altered videodensitometric findings in our dialysis patients could represent an early index of altered myocardial textural patterns, which potentially might evolve toward so-called `uraemic cardiomyopathy'. Furthermore, the individual analysis of CVI permitted clear differentiation of dialysis and hypertensive patients even though they had similar LVM. In fact, the CVI is altered in the entire dialysis population, less than the 95th percentile of the normal distribution (Figure 2Go).

The strength of this case–control study was the recruitment of subjects similar in age and cardiac mass and of the same gender, thereby excluding important confounding factors. Furthermore, stringent clinical criteria avoided major confusion due to co-existent coronary artery disease which might per se influence the videodensitometric signal. However, the study is limited by the lack of histological determination of cardiac structure, but the use of this invasive technique was not ethically acceptable.

In conclusion, videodensitometry might represent a non-invasive, feasible ultrasound tissue characterization method which could integrate the conventional echo-Doppler analysis of the uraemic heart, and give us new insights into primary cardiomyopathies. Further studies are needed to understand completely the clinical and prognostic significance of the myocardial ultrasonic textural alterations.



   References
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 

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Received for publication: 24. 8.98
Accepted in revised form: 9. 4.99





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