Myocardial Ultrasound Tissue Characterization in Patients with Chronic Renal Failure
Massimo Salvetti*,
Maria Lorenza Muiesan*,
Anna Paini*,
Cristina Monteduro*,
Bianca Bonzi*,
Gloria Galbassini*,
Eugenia Belotti*,
Ezio Movilli,
Giovanni Cancarini and
Enrico Agabiti-Rosei*
* Internal Medicine; and Nephrology, University of Brescia, Brescia, Italy
Address correspondence to: Dr. Massimo Salvetti, Department of Medical and Surgical Sciences, University of Brescia, c/o Spedali Civili, 2a Medicina, Brescia 25100, Italy. Phone: +39-030-3995248; Fax: +39-030-3384348; salvetti{at}med.unibs.it
Received for publication May 12, 2006.
Accepted for publication March 6, 2007.
The objective of this study was to detect ultrastructural changesin myocardium related to collagen content by ultrasound tissuecharacterization in patients with chronic kidney disease (CKD)and in uncomplicated hypertensive control subjects. In 25 hemodialysis(HD) patients, in 25 patients with moderate to severe chronicrenal failure (CRF), and in 10 patients with essential hypertension(EH) and normal renal function matched for age, BP, and leftventricular mass index, left ventricular anatomy and functionwere evaluated by conventional echocardiography, and integratedbackscatter signal (IBS) was analyzed by acoustic densitometry.IBS mean reflectivity increased from 48% in patients with EHto 56% in patients with CRF to 62% in HD patients (ANOVA P <0.01). IBS mean cyclic variation was progressively increasedfrom 4.35 ± 1.2 dB in HD patients to 5.27 ± 0.90in patients with CRF to 6.50 ± 1.6 dB in patients withEH (ANOVA P < 0.01). At multivariate analysis, IBS mean reflectivitywas positively related to age and serum creatinine ( 0.351,P = 0.036; and = 0.408, P = 0.016, respectively). IBS meancyclic variation was inversely related to age and serum creatinine( = –0.274, P = 0.025; and = –0.262, P = 0.025,respectively) and positively related to left ventricular midwallfractional shortening and transmitral E/A ratio ( = 0.269, P< 0.05; and = 0.314, P < 0.001, respectively). The datasupport the hypothesis that interstitial collagen depositionmay appear early in the course of CKD and suggest that acousticdensitometry may represent a useful tool for the assessmentof myocardial tissue changes in patients with CKD.
Left ventricular hypertrophy (LVH) is an independent predictorof cardiovascular morbidity and mortality in patients with ESRDas well as in hypertensive patients, in patients with coronaryartery disease, and in the general population (1). It has beendemonstrated that changes in LV mass index (LVMI) over timeare associated with cardiovascular prognosis (2–4), andLVH is currently considered an important intermediate end pointin the treatment of hypertensive patients (5,6). A greater prevalenceof LVH has been reported in patients with chronic renal failure(CRF) (7), possibly contributing to the greater risk for cardiovascularevents in these patients (8,9). Experimental studies have demonstratedthat the typical changes in uremic cardiomyopathy are increasedcardiac size, interstitial and perivascular fibrosis, reducedcapillary density, and thickening of intramural myocardial arterioles(10).
Acoustic densitometry is a noninvasive tool for the evaluationof myocardial tissue characteristics and provides an integratedon-line capability to measure, display, and analyze the averageacoustic image intensity within a user-specified region of interest(ROI). Experimental studies have suggested that integrated backscatter(IBS) measures may be related to myocardial collagen content(11–14). In humans, ultrasonic backscatter indices havebeen shown to be related to myocardial collagen content as assessedby endomyocardial biopsy (15–18). Therefore, we consideredit worthwhile to analyze myocardial ultrasonic backscatter (IBS)in patients who had CRF and were undergoing hemodialysis, inpatients with mild to moderate CRF, and in patients with essentialhypertension with comparable age, BP values and LVM to evaluatewhether interstitial collagen deposition as evaluated by acousticdensitometry may appear early in the course of chronic kidneydisease (CKD).
Sixty patients were included in the study: 25 consecutive patientswho had ESRD and were undergoing hemodialysis (HD) at the Departmentof Nephrology of our University Hospital, 25 patients with moderateto severe CRF (serum creatinine 1.3 mg/dl in women and 1.5 mg/dlin men and estimated GFR [eGFR; modified Modification of Dietin Renal Disease (MDRD) formula] <60 ml/min per m2), and10 control patients with essential hypertension (EH). Patientswith CRF and EH were selected from consecutive patients attendingthe Hypertension Unit at our University Hospital. Patients withprevious cardiovascular disease were excluded. patients withEH with comparable LVMI were selected to avoid the confoundingeffect of the increase of LVM on IBS measures, because an increasein IBS absolute values and a reduction of IBS cyclic variation(CV) has been described in patients with EH with markedly increasedLVM (19).
BP was measured by the same physician with a mercury sphygmomanometer.Three measurements were taken in a sitting position after 10min of rest. The diagnosis of EH was determined according toEuropean Society of Hypertension–European Society of Cardiology(ESH-ESC) guidelines (an increase in systolic BP 140 mmHg and/ordiastolic BP 90 mmHg) (5). In all patients, an informed consentwas obtained according to the Declaration of Helsinki.
Venous blood samples were taken with the participants in sittingposition after fasting for 12 h for standard hematology andserum biochemistry tests. GFR was estimated by the simplifiedMDRD formula: 186.3 x [serum creatinine exp(–1.154)] x[age exp(–0.203)] x (0.742 if female; ml/min per 1.73m2).
Conventional Echocardiography
All patients underwent standard echocardiographic evaluationusing a Philips Sonos 5500 echocardiographic unit equipped witha broadband sector transducer (S4 fusion imaging 2 to 4 MHz,Eindhoven, The Netherlands). The examinations were performedin the morning with the patient in supine left lateral decubitusafter 20 min of rest; in all HD patients, the examination wasperformed shortly after HD. The procedure for visualizationand interpretation of the LV structure that was followed waspreviously described (2). The LV internal dimensions, interventricularseptum (IVS), and posterior wall (PW) thickness were measuredaccording to the recommendations of the American Society ofEchocardiography (20). Echocardiographic tracings were calculatedblindly by two expert independent readers, and the average measurementswere considered. Relative wall thickness (the ratio of PW thicknessto one-half LV internal dimension) was calculated, and values>0.44 were considered to indicate LV concentric geometry(21). The Penn Convention was used to calculate LVM by an anatomicallyvalidated formula (23); LVM was indexed by body height to the2.7 power (23). LV systolic function was estimated by both endocardialfractional shortening and midwall fractional shortening, aspreviously reported (24). Transmitral flow velocity profilewas evaluated by the Doppler technique, with the sample volumeplaced at the tips of mitral leaflets from the apical four-chamberview, and the peak early (E wave) flow velocity, peak late (Awave) flow velocity, and the deceleration time of the E wavewere measured. Outlines of transmitral Doppler flow patternsrecorded at mitral annulus were traced to measure early andlate diastolic filling integrals (25). LV isovolumic relaxationtime was also measured by Doppler echocardiography, with thesample volume positioned between the LV outflow tract and theanterior mitral leaflet. Diastolic dysfunction was defined accordingto the European Society of Cardiology Working Group on DiastolicHeart Failure Criteria (26).
Acoustic Densitometry
Acoustic densitometry analysis was performed with the commerciallyavailable software package included in the ultrasound system.Images were acquired in parasternal long-axis view (septum andPW were kept almost perpendicular to the ultrasound beam), ata frame rate of 25 Hz, and stored on optical disks. The signalwas sampled with the ROI (21 x 21 pixels) placed at the middleportion of the IVS, of the PW, and of the pericardium. All ofthe digital images were analyzed off-line blindly by one experiencedreader. The position of the ROI was adjusted frame by frameto analyze the same region of myocardium throughout the cardiaccycle, and care was taken to exclude specular echoes that arosefrom interfaces between myocardium and blood. Analysis of IBSamplitude and absolute systo-diastolic variation of backscatterwere considered. IBS reflectivity at IVS and PW were calculatedas the ratio between the mean IBS values and pericardial IBSx 100. Mean reflectivity (the mean of IVS and PW reflectivity)was also calculated. IBS analysis was performed by the sameoperator in all patients. Reproducibility of the IBS measurementswas tested in 20 patients by assessment of absolute IBS valuesand CV in two different acquisitions. The mean difference betweenthe two series of acquisitions performed by the same operatorwas 0.18 ± 0.45 db for myocardial IBS and 0.09 ±0.91 dB for CV of IBS (averaged variation 2.5 and 9.7%, respectively).
Statistical Analyses
Data were stored and analyzed with SPSS for Windows StatisticalSoftware (SPSS, Chicago, IL). All data are expressed as mean± SD, unless otherwise stated. One-way ANOVA and Scheffepost hoc test were used to evaluate differences among groups.Frequency distribution was analyzed by 2 test. Bivariate correlationswere evaluated by the Pearson correlation coefficient; multivariatecorrelations were evaluated by linear regression analysis. P< 0.05 was considered statistically significant.
Study Population
There was no difference in age, gender distribution, and BPvalues among the three groups of patients (Table 1). Serum creatininewas, by definition, higher in HD patients and in patients withCRF in comparison with patients with EH, and eGFR was significantlylower in HD patients and in patients with CRF in comparisonwith patients with EH. No patient with EH had an eGFR <60ml/min per m2. Serum uric acid was significantly higher in HDpatients and in patients with CRF, whereas plasma lipid profileand plasma glucose levels were comparable in the three groups.Hemoglobin levels were slightly but not significantly lowerin HD patients. Antihypertensive treatment consisted of a combinationof drugs in 84% of patients. Angiotensin-converting enzyme inhibitoror angiotensin II receptor blocker use was comparable in thethree groups (76% in HD, 84% in CRF, 80% in EH; NS).
Table 1. Demographic and hemodynamic characteristics of the patientsa
Cardiac Structure and Function LV Structure.
LVMI was not different in the three groups (hypertension controlswere selected to obtain groups with comparable LVMI). In HDpatients, LV internal dimensions tended to be lower and relativewall thickness tended to be higher, indicating a trend (althoughstatistically nonsignificant) to a more concentric geometry.Left atrial dimensions were comparable in the three groups (Table 2).
Table 2. LV geometry and function in the three groupsa
LV Function.
No significant differences among groups were observed for endocardialfractional shortening. Midwall fractional shortening increasedfrom 12.9 ± 3.3 in HD patients to 14.7 ± 3.4 inpatients with CRF to 16.0 ± 3.9 in patients with EH (P< 0.05; Table 2). There was no statistically significantdifference in the ratio of E and A transmitral flow velocitiesin the three groups. E wave deceleration time increased from193 ± 42 ms in patients with EH to 219 ± 40 msin patients with CRF to 249 ± 66 ms in HD patients (P< 0.05). LV isovolumic relaxation time progressively increasedfrom 78 ± 15 ms in patients with EH to 103 ± 25in patients with CRF to 113 ± 25 in HD patients (P <0.05). The prevalence of diastolic dysfunction was significantlygreater in HD patients in comparison with patients with EH (76versus 10%; 2P = 0.001) and with patients with CRF (76 versus48%; 2P < 0.05) and in patients with CRF as compared withpatients with EH (48 versus 10%; 2P < 0.05).
Acoustic Densitometry
IBS reflectivity measured at the IVS was progressively increasedfrom 51% in patients with EH to 62% in patients with CRF to72% in HD patients (P < 0.01). PW IBS reflectivity also wasincreased from 44% in patients with EH to 49% in patients withCRF to 52% in HD patients (NS). The calculated mean of the valuesthat were observed at the IVS and at the PW ("mean reflectivity")was progressively increased from 48% in patients with EH to56% in patients with CRF to 62% in HD patients (P < 0.01;Figure 1).
Figure 1. Integrated backscatter (IBS) mean reflectivity. HD, hemodialysis patients; CRF, patients with chronic renal failure; EH, patients with essential hypertension. *P < 0.05 versus EH; #P < 0.05 versus CRF.
IBS CV that was measured at the IVS progressively increasedfrom 4.02 ± 1.13 dB in HD patients to 4.88 ± 1.27dB in patients with CRF to 5.81 ± 1.16 dB in patientswith EH (P < 0.01). Similar results were obtained at thePW, with a progressive increase of IBS CV from 4.68 ±1.61 in HD patients to 5.86 ± 0.89 in patients with CRFto 7.18 ± 2.69 in patients with EH (P < 0.01). Thecalculated mean of CV at the IVS and at the PW (mean CV) progressivelyincreased from 4.35 ± 1.2 dB in HD patients to 5.27 ±0.90 in patients with CRF to 6.5 ± 1.6 dB in patientswith EH (P < 0.01; Figure 2).
Figure 2. IBS mean cyclic variation. *P < 0.05 versus EH; #P < 0.05 versus CRF.
At univariate analysis, IBS mean reflectivity was positivelyrelated to age and serum creatinine (r = 0.316, P < 0.01;and r = 0.430, P < 0.001, respectively) and negatively relatedto eGFR (r = –0.518, P < 0.001). IBS mean CV was negativelyrelated to age (r = –0.275, P < 0.05) and serum creatinine(r = –0.404, P < 0.001) and positively related to eGFR(r = 0.518, P < 0.001), transmitral E/A ratio (r = 0.328,P = 0.01), and LV midwall fractional shortening (r = 0.338,P < 0.01).
At multivariate analysis, IBS mean reflectivity was positivelyrelated to age ( 0.351, P = 0.036) and serum creatinine ( =0.408, P = 0.016), whereas IBS mean CV was inversely relatedto age ( = –0.274, P = 0.025) and serum creatinine ( =–0.262, P = 0.025) and positively related to eGFR ( =0.408, P < 0.001), transmitral E/A ratio ( = 0.314, P <0.001), and LV midwall fractional shortening ( = 0.269, P <0.05). In patients with diastolic dysfunction, IBS mean reflectivitywas significantly higher (54 versus 59%; P < 0.05) and IBSmean CV was significantly lower (4.7 ± 1.3 versus 5.4± 1.3; P < 0.05) than in patients with normal diastolicfunction.
The main finding of this study is represented by the significantdifference in echocardiographic indices of fibrosis observedin patients with CRF and in HD treatment in comparison withcontrol subjects with EH. In experimental studies, IBS absolutevalues have been shown to be reliable indices of LV fibrosis.In addition, they have been shown to reflect myocardial collagencontent as assessed by endomyocardial biopsy in humans (15,16,18).It has been demonstrated that even mild reductions in renalfunction are associated with a greater prevalence of LVH (27,28);the increase in IBS reflectivity that was observed in our studyalso indicates an early increase in LV collagen deposition,beginning well before the development of ESRD. In fact, theincrease in IBS reflectivity was progressive, with intermediatevalues in patients with mild to moderate CKD and with the highestvalues in HD patients. Our findings with a noninvasive techniqueare concordant with previous data demonstrating a significantincrease in interstitial collagen content in uremic cardiomyopathyand add further information to the early involvement of theleft ventricle in the less advanced stages of kidney disease.
Another interesting finding in our study is represented by thelower IBS CV that was observed in the two groups of patientswith CKD in comparison with patients with EH. As described forIBS reflectivity, the reduction in CV was progressive, withthe lowest values in HD patients. CV reflects a complex phenomenonand is significantly influenced by myocardial fiber orientationduring the cardiac cycle, by myocardial contractility, and bycollagen content. Already in 1985 Wickline et al. (29) observedin open-chest dogs that a reduced IBS CV may be paralleled bya reduction in LV contractile performance. At the same time,IBS CV was found to be significantly and inversely related tothe percent fibrosis area as assessed by endomyocardial biopsyin patients with dilated cardiomyopathy (17) and to the myocardium/fibrosisratio in patients with aortic stenosis (18). Furthermore, inpatients with EH, a decreased CV of backscatter signal is associatedwith an increase in serum procollagen type I C-peptide, a specificcirculating marker of cardiac collagen content (30). In ourstudy, the modest reduction of IBS CV that was observed in patientswith CRF and the more relevant decrease of CV IBS that was observedin patients with ESRD, as well as the significant correlationwith indices of systolic function, might reflect a progressiveimpairment of LV contractile performance, possibly associatedwith an increase in myocardial collagen content.
Our data expand previous findings in patients with CKD. Mizushigeet al. (31) observed a reduction in IBS CV in 18 patients whowere undergoing HD in comparison with 11 normotensive controlsubjects; however, the significant difference in LVMI betweengroups could have influenced the results. In another study,Akar et al. (32) observed a reduction in IBS CV in patientswith ESRD, in comparison with both normotensive control subjectsand patients with EH with normal renal function. In both studies,the authors did not report data on IBS reflectivity, limitingtheir observations to IBS CV, and did not include patients withless advanced stages of renal disease.
Some limitations deserve considerations. First, in our study,we were not able to correlate IBS measures with histologic datafrom endomyocardial biopsies for ethical reasons. The resultsthat were obtained in patients with dilated cardiomyopathy (15–17)and aortic stenosis (18) suggest, however, that ultrasonic tissuecharacterization may be a reliable indicator of the degree ofmyocardial fibrosis. As an alternative to endomyocardial biopsy,late gadolinium-enhancement cardiovascular magnetic resonance(MR) has been proposed as a useful tool for the noninvasiveevaluation of myocardial fibrosis; unfortunately, cardiac MRwas not performed in this study.
Antihypertensive treatment, in particular with drugs that interactwith the renin-angiotensin-aldosterone system, may influencemyocardial structure. All of the patients in this study weretreated with antihypertensive drugs, although the proportionof patients who were taking angiotensin-converting enzyme inhibitorsor angiotensin receptor blockers was similar in the three groupsand a strong influence of treatment on our results seems unlikely.
Our findings may give some insights into the underlying mechanismsof the elevated risk for cardiovascular events in patients withrenal dysfunction. In fact, the precocity of the impairmentof LV structural and functional properties in patients withCKD might contribute to the increased risk for cardiovascularevents that are observed in the presence of even mild derangementsof renal function. It is interesting that a reduction in myocardialIBS CV is an independent predictor of cardiovascular eventsin patients with primary amyloidosis (45).
Our data support the hypothesis that interstitial collagen deposition,one of the typical features of uremic cardiomyopathy, may appearearly in the course of CKD and suggest that acoustic densitometrymay represent a useful tool for the assessment of myocardialchanges in patients with CKD. A more extensive use of myocardialIBS analysis, a noninvasive and widely available technique withrelatively low cost, might be of value in the evaluation andfollow-up of patients with CKD. Additional studies are neededto clarify further the clinical and prognostic significanceof IBS in patients with CKD as well as the effects of varioustreatment strategies on LV structure and function.
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Abstract
Introduction
0.351, P = 0.036; and 
1.3 mg/dl in women and 
2 test. Bivariate correlations were evaluated by the Pearson correlation coefficient; multivariate correlations were evaluated by linear regression analysis. P < 0.05 was considered statistically significant. 
