NDT Advance Access originally published online on August 27, 2006
Nephrology Dialysis Transplantation 2007 22(1):163-170; doi:10.1093/ndt/gfl484
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Do ultrasound renal resistance indices reflect systemic rather than renal vascular damage in chronic kidney disease?
Medical Department IV, Nephrology, University Homburg, D-66421 Homburg, Germany
Correspondence and offprint requests to: Gunnar H. Heine, MD, Medical Department, Nephrology, University Homburg, D-66421 Homburg, Germany. Email: inghei{at}uniklinik-saarland.de
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Abstract |
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Background. In patients suffering from chronic kidney disease (CKD), ultrasound renal resistance indices predict progression of kidney disease and death. Although ultrasound resistance indices were initially considered to directly reflect intrarenal vascular resistance, they are complex composite parameters that are influenced by various vascular factors. We hypothesized that renal resistance indices reflect systemic vascular disease rather than local renal damage in patients with CKD.
Methods. In 140 patients suffering from CKD not receiving renal replacement therapy, intrarenal resistance indices were measured in interlobar arteries. For assessment of systemic atherosclerotic disease, common carotid intima-media thickness (IMT) and ankle-brachial blood pressure index were determined. Categories of risk for coronary heart diseases were defined by Framingham risk scoring.
Results. Increased renal resistance indices were associated with high Framingham risk scores and with the presence of atherosclerotic disease. In addition, ultrasound renal resistance indices progressively increased with the stage of renal function impairment, and patients suffering from diabetic nephropathy had higher resistance indices than patients suffering from other renal diseases. In a multivariate linear regression analysis, IMT, Framingham risk score, renal function, presence of diabetic nephropathy and pulse pressure independently predicted resistance indices. However, when additionally adjusting for age, IMT and Framingham risk score were no longer independent predictors of resistance indices.
Conclusions. In patients suffering from CKD, intrarenal resistance indices are independently associated with cardiovascular risk score and systemic vascular disease as well as with aetiology and stage of CKD. This may explain their strong association with both impaired renal outcome and death.
Keywords: atherosclerosis; chronic renal disease; resistive index; ultrasound
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Introduction |
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After a given insult, most chronic renal diseases progress to terminal renal failure independently of the event(s) responsible for the initial lesion [1]. Nevertheless, the rate of progression is highly variable, and prediction of this progression is of major importance for the patient and his physician.
Major risk factors which predict the progression of kidney disease are arterial hypertension, proteinuria, nicotine abuse and baseline renal function [2]. In addition to these established risk factors, elevated renal resistance indices measured by Duplex ultrasound have recently been suggested to predict the future progression of renal disease [3–6]. In the largest of these studies, Radermacher and coworkers [4] reported a resistance index value of 
80 to be an independent risk factor for progression of kidney disease and death in patients suffering from chronic renal disease even after adjustment for arterial hypertension, renal function and proteinuria.
Despite these promising data, most clinicians currently rely on measurements of blood pressure, proteinuria and glomerular filtration rate (GFR) rather than on ultrasound studies when predicting future progression of chronic kidney disease (CKD) in individual patients. In the recent K/DOQI (kidney disease outcomes quality initiative) guidelines, ultrasound resistance indices did not enter a list of various non-modifiable and modifiable factors which should be ascertained by nephrologists in order to predict the rate of decline in kidney function [2].
The current reluctance to use ultrasound resistance indices as prognostic markers partly results from our limited understanding of the physiological factors that affect renal resistance indices. Initially, it was suggested that these indices directly reflect intrarenal vascular resistance, which resulted in their denomination as ‘resistance indices’. Later, ultrasound resistance indices were shown to be a complex composite of vascular factors reflecting arterial compliance and pulse pressure rather than renal vascular resistance alone [7].
In accordance, we recently reported that in renal transplant patients, elevated resistance indices are associated with cardiovascular risk factors and with markers of systemic atherosclerotic disease [8], while they are not independently associated with transplant function [8–10]. We, therefore, suggested that resistance indices should not be considered specific markers of renal damage in transplant patients [8].
Similarly, in hypertensive subjects without markedly impaired kidney function, higher renal resistance indices are found if carotid atherosclerotic disease [11–14] or left ventricular hypertrophy [11,12,15] are present.
These observations may not directly be extrapolated to patients with CKD. In contrast to renal transplant recipients and to hypertensive patients with intact renal function, patients suffering from CKD present with a broader spectrum of renal pathological lesions. In these patients, ultrasound renal resistance indices may thus be more organ-specific markers of local kidney damage than in transplant recipients or in hypertensive patients with intact renal function.
The present study aimed to evaluate how far renal resistance indices are associated with systemic atherosclerotic disease and left ventricular hypertrophy in patients with different stages of CKD.
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Subjects and methods |
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Subjects
A total of 140 patients (80 males, 60 females) suffering from chronic renal disease were studied between March 2004 and October 2004. All patients regularly visited our out-patient department and gave informed consent to their study participation. Patients who were undergoing renal replacement therapy, who had received a kidney allograft, or who suffered from rapid deterioration of renal function [increase in serum creatinine >1.0 mg/dl (>88.4 µmol/l) within 28 days] or from untreated renal-artery stenosis resulting in a >50% reduction in the luminal diameter were excluded.
Data acquisition and ultrasound studies were performed by a single investigator (B.R.). The study was approved by the local ethics committee.
Blood was taken from all subjects under standardized conditions. Plasma glucose, creatinine, total cholesterol, low-density lipoprotein cholesterol (LDL-C), high-density lipoprotein cholesterol (HDL-C), C-reactive protein, lipoprotein (a), HbA1c, parathyroid hormone, cardiac troponin T and homocysteine were obtained using standard techniques. Definition and classification of chronic renal disease followed the K/DOQI guidelines [2], and GFR was calculated using the MDRD study equation 3 [2].
Assessment of cardiovascular risk factors and comorbidity
A standardized questionnaire was used to record a history of smoking, diabetes, current drug intake, and cardiovascular comorbidity. Additionally, comorbidity was assessed by chart review. Coronary artery disease was diagnosed in patients who had a history of myocardial infarction or who had undergone coronary artery angioplasty, stenting and/or bypass surgery. In patients who had a history of stroke or had undergone carotid endarterectomy or stenting, cerebrovascular disease was diagnosed. Finally, in patients who had undergone non-traumatic lower extremity amputation, lower limb artery angioplasty, stenting and/or bypass surgery, peripheral artery disease was diagnosed. Patients were defined as having cardiovascular disease if they had coronary artery disease, cerebrovascular disease and/or peripheral artery disease.
Patients were categorized as active smokers if they were current smokers or had stopped smoking <1 month before entry into the study. Patients with self-reported diabetes mellitus, with a non-fasting blood sugar level of >200 mg/dl, with a fasting blood sugar level of >126 mg/dl or with current use of hypoglycemic medication were categorized as diabetic.
Body mass index (BMI) was calculated as weight (kg)/height (m)2. Systolic blood pressure (SBP), diastolic blood pressure (DBP) and heart rate were measured after 5 min of rest. Mean blood pressure was calculated as DBP + [(SBP – DBP)/3], and pulse pressure was calculated as SBP – DBP.
Categories of risk for coronary heart disease (CHD) were defined by Framingham risk scoring. 10-year risk for myocardial infarction and coronary death were determined using electronic calculators, which are available on the ATP III page of the National Heart, Lung, and Blood Institute Website (www.nhlbi.nih.gov/guidelines/cholesterol). According to the Third Report of the National Cholesterol Education Program (NCEP), patients with a Framingham risk score of >20%, with prevalent cardiovascular disease (as defined earlier) or with diabetes mellitus were classified to have ‘high CHD risk’ (10-year CHD risk >20%). Accordingly, patients with a 10-year CHD risk of 10–20% and of <10% according to the Framingham score were defined to have ‘intermediate CHD risk’ and ‘low CHD risk’, respectively.
Presence of left ventricular hypertrophy was diagnosed by electrocardiography. According to the criteria proposed and validated by the LIFE trial group, electrocardiographic left ventricular hypertrophy was defined in patients who had a Cornell voltage-duration product [product of QRS duration times Cornell voltage (RavL ± SV3, with 6 mm added in women)] >2440 mm*ms and/or a Sokolow–Lyon voltage (SV1 ± RV5-6) >38 mm [16].
Renal resistance indices
Color Doppler examinations were performed with a phased-array transducer (Acuson Sequoia; Mountainview, CA, USA; B-mode frequency: 4 MHz; Doppler frequency: 2.5 MHz) in supine position.
In each kidney, intrarenal Doppler spectra were obtained at three representative locations from the interlobar arteries along the border of medullary pyramids. The resistance index (RI) was calculated according to the following formula:
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Carotid ultrasound studies
The intima-media thickness (IMT) of the common carotid artery was measured from high-resolution, 2-dimensional ultrasound images obtained by a linear-array 8 MHz transducer (Acuson Sequoia). With the subject in supine position and the head slightly extended and turned to the opposite direction, the distal common carotid artery and the carotid bulb were identified by longitudinal scanning. IMT was defined as the distance between the leading edges of the lumen interface and the media-adventitia interface of the far wall.
Three representative IMT measurements were performed on both the left and right sides in the far wall of the common carotid arteries at predefined positions (1.0, 2.0 and 3.0 cm proximal to the bifurcation), and these six IMT readings were averaged to give the mean common carotid intima-media thickness (IMT mean). IMT was not measured at the site of a carotid plaque.
Ankle-brachial blood pressure index (ABI)
Arm blood pressure (brachial artery) and bilateral ankle blood pressure (posterior tibial artery), measured by handheld Doppler (handydop, ELCAT, Wolfratshausen, Germany), were taken with the subject supine. ABI was calculated by the ratio of the ankle systolic pressure divided by the arm systolic pressure, using the lower value of the two ankle blood pressure values obtained by bilateral measurement.
Participants who had an ABI < 1.10 were categorized as having low ABI. Participants were categorized as having high ABI if they had an ABI measure >1.40 or if the ankle pressure of either leg could not be obtained because of arterial stiffening (pulse could not be obliterated with a pressure of >300 mmHg). Participants were defined as having normal ABI if ABI measures were >1.10 and <1.40.
Statistics
Data management and statistical analysis were performed with the Prism 4.00 statistical software (Graphpad, San Diego, USA). Unless indicated otherwise, continuous data are expressed as means ± SD, and compared by independent-samples t-test, or by one-way analysis of variances (ANOVA) followed by Scheffé post-test, as appropriate. Correlation coefficients were calculated by Spearman test.
Subsequently, a multivariate linear regression analysis was used to determine independent predictors of intrarenal resistance indices. Model 1 included GFR, IMT, presence of diabetic nephropathy, presence of left ventricular hypertrophy and high CHD risk, model 2 additionally included pulse pressure, model 3 additionally included age, and model 4 additionally included plasma phosphorus. The level of significance was set at P < 0.05.
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Results |
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Patient characteristics of the 140 patients with CKD included in the study are depicted in Table 1.
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Ultrasound renal resistance indices linearly increased with a progressive impairment of renal function (Figure 1; ANOVA: P < 0.001). Patients suffering from diabetic nephropathy had higher resistance indices than patients suffering from other renal diseases, whereas no significant differences were observed between other pathological types of CKD (Figure 2; ANOVA: P < 0.001).
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Association between cardiovascular risk factors and renal resistance indices
RI measurements did not differ between male and female patients (75.6 ± 9.6 vs 74.9 ± 9.0, P = 0.633), or between smokers and non-smokers (72.1 ± 7.0 vs 75.7 ± 9.5, P = 0.168). The group of diabetic patients (whether suffering from diabetic nephropathy or from non-diabetic kidney disease) had increased RI measurements compared with non-diabetic patients (80.7 ± 8.5 vs 73.0 ± 8.7, P < 0.001).
SBP was positively correlated with resistance indices, whereas a negative correlation was found between DBP and resistance indices (Table 2). Thus, pulse pressure highly significantly correlated with RI measurements (Figure 3), whereas mean blood pressure did not (Table 2). Among other traditional and non-traditional cardiovascular risk factors, age, BMI, parathyroid hormone, plasma phosphorus, calcium–phosphorus product, C-reactive protein, troponin T and homocysteine were positively correlated with renal resistance indices, whereas total cholesterol was negatively correlated (Table 2).
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According to the Framingham risk score, 77 patients had ‘high CHD risk’ (10-year CHD risk >20%), 28 patients had ‘intermediate CHD risk’ (10-year CHD risk 10–20%) and 35 patients had ‘low CHD risk’ (10-year CHD risk <10%). Intrarenal resistance indices significantly differed between these three groups, and high-risk patients had significantly higher resistance indices than low-risk and intermediate-risk patients (Figure 4; ANOVA P < 0.001).
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A total of 21 patients had electrocardiographic signs of left ventricular hypertrophy. In these patients, RI measurements did not differ from patients without left ventricular hypertrophy (75.9 ± 9.9 vs 74.8 ± 9.2, P = 0.617).
Association between markers of subclinical atherosclerosis and renal resistance indices
ABI were measured in 110 patients, 44 of whom had normal ABI, 57 had low ABI, and nine had high ABI. Patients with normal ABI were younger than patients with pathological ABI (57.5 ± 14.2 vs 63.5 ± 12.0 years, P = 0.018). They had lower SBP (159.2 ± 21.6 vs 172.7 ± 27.9 mmHg, P = 0.008) and pulse pressure (60.9 ± 16.2 vs 75.1 ± 22.2 mmHg, P < 0.001). The two groups did not differ in DBP, BMI, total cholesterol, HDL-C, LDL-C, HbA1c, parathyroid hormone, Lp(a), homocysteine, troponin T and C-reactive protein (data not shown).
Patients with normal ABI had lower ultrasound resistance indices than patients with pathological ABI (72.8 ± 8.6 vs 76.5 ± 9.5, P = 0.043).
Correlations between common carotid IMT and cardiovascular risk factors are shown in Table 2. Ultrasound renal resistance indices were highly significantly correlated with IMT measurements (R = 0.380, P < 0.001, Figure 5).
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Subsequently, a multivariate linear regression analysis was calculated, which included IMT as a marker of subclinical atherosclerosis, Framingham risk score (categorized as ‘high CHD risk’ vs ‘no high CHD risk’), presence of left ventricular hypertrophy, calculated GFR, and presence of diabetic nephropathy. With the exception of left ventricular hypertrophy, all variables were independent predictors of ultrasound resistance indices (Table 3, model 1). They remained so after inclusion of pulse pressure into the linear regression analysis (model 2). However, IMT and high Framingham risk score were no longer significant independent predictors of resistance indices when finally including age (model 3) and plasma phosphorus (model 4) into the model.
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Discussion |
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TopAbstractIntroductionSubjects and methodsResultsDiscussionConclusionReferences |
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In a series of large prospective clinical trials, Radermacher and coworkers recently reported an increase in the ultrasound renal resistance index
80 to independently predict an unfavourable outcome in kidney transplant patients [17], in patients with renal artery stenosis [18], and in patients suffering from CKD [4]. In the latter group of patients, the prognostic impact of elevated resistance indices was confirmed by several smaller studies [3,5,6]. The authors subsequently suggested measurements of ultrasound renal resistance indices as a valuable tool in the regular diagnostic armamentarium in CKD [4]. Before that, however, a more profound understanding of the factors that affect these indices seems mandatory. Principally, the observed association between increased ultrasound resistance indices and progression of kidney disease and mortality may be explained by two different mechanisms: first, an elevation of these indices may be caused by an increase in local renal vascular resistance because of a non-specific renal scarring process with a subsequent reduction in the number and area of intrarenal vessels. This predominantly assumed relationship has provided the theoretical framework supporting the use of Doppler technique in the evaluation of renal disease [4,12,19], and led to the denomination of ‘resistance indices’. In some reports the terms ‘resistance indices’ and ‘renal vascular resistance’ are even used interchangeably.
Experimental studies, however, suggest that the ultrasound resistance index is a complex composite parameter that reflects a variety of vascular factors: in an in vitro model which studied the interrelationship between ultrasound resistance indices, vascular compliance and vascular resistance, ultrasound resistance indices depend on both vascular compliance and vascular resistance. Ultrasound resistance indices, however, become less and less dependent on resistance as compliance decreases, and are completely independent of vascular resistance when compliance is zero [20]. In an ex vivo pulsatile perfusion system, ultrasound resistance indices in rabbit kidneys are strongly correlated with pulse pressure, whereas only marked, likely non-physiological increases in renal vascular resistance elevate ultrasound resistance indices [21]. In an in vivo model of acute urinary obstruction in Yorkshire pigs, ultrasound resistance indices strongly correlate with ureteral pressure and renal perfusion pressure, but poorly with vascular resistance [22]. These findings were confirmed in another ex vivo pulsatile perfusion system: in isolated rabbit kidneys, a rise in ureteral pressure, mimicking acute urinary obstruction, results in increased renal vascular resistance [23]. Ultrasound resistance indices are correlated with both ureteral pressure and renal vascular resistance. In contrast, the association between ultrasound resistance indices and renal vascular resistance is much weaker with pharmacological elevation of vascular resistance. Thus, high renal resistance indices in acute urinary obstruction are not sufficiently explained by increased vascular resistance alone. Instead, urinary obstruction raises renal resistance indices by altering vascular distensibility via an increase in interstitial pressure, which determines the area of compliant vessels by decreasing transmural pressure (the mathematical difference between intra-arterial pressure and interstitial pressure). In acute urinary obstruction, the impact of interstitial pressure on the vessel area is most marked at diastole. Thus, the ratio between systolic and diastolic blood velocities is affected, and ultrasound resistance indices rise.
Admittedly, these findings from in vitro models and animal studies cannot blindly be transferred to the in vivo state in humans. A major limitation of these models is the inability to adequately preserve renal autoregulatory systems. For instance, the ex vivo pulsatile perfusion system in rabbit kidneys which found that ultrasound resistance indices are more closely correlated to pulse pressure than to renal vascular resistance [21] utilized a perfusion fluid containing a haematocrit of only 1.25%. As haemoglobin may act as a nitric oxide (NO) sink, such a low-haematocrit perfusion system may have a high background activity of vasodilatory NO because of a lack of scavenging of NO by haemoglobin. Thus, this system may not autoregulate well and may have a very low renal vascular resistance compared with the in vivo state.
Nevertheless, these experimental data weaken the theoretical understanding that renal vascular resistance is the major factor controlling ultrasound resistance indices. Instead, they suggest impaired vascular compliance and increased pulse pressure, which may both result from systemic vascular damage, as principal causes of pathological ultrasound resistance indices. As patients with advanced systemic vascular damage are at high risk for progression of CKD and death, the prognostic impact of increased ultrasound resistance indices as an outcome marker may be explained by the association of systemic vascular damage with both ultrasound indices as well as renal and patient outcome.
In line with this concept of considering ultrasound resistance indices as systemic vascular rather than local renal markers, are recent histopathological and clinical studies: in kidney biopsy specimen, only the degree of arteriolosclerotic alterations is independently associated with pre-biopsy ultrasound resistance indices, whereas interstitial fibrosis, tubular atrophy, glomerular sclerosis or interstitial infiltration are not [6]. In kidney transplant patients, intrarenal resistance indices are associated with carotid IMT and with ankle-brachial blood pressure indices, both of which are markers of systemic atherosclerotic disease, but not with transplant function [8]. In hypertensive subjects without markedly impaired kidney function, high renal resistance indices are associated with carotid atherosclerotic disease (measured as IMT [11,13,14] or as plaque score [12]) and with left ventricular hypertrophy [11,12,15].
To our best knowledge, we are the first group to study the relationship between ultrasound renal resistance indices and systemic vascular disease in patients suffering from CKD. In contrast to in vitro models [20], we assessed vascular disease by measuring atherosclerotic vascular changes (ankle-brachial blood pressure indices and common carotid IMT) rather than by measuring arterial compliance directly. In clinical studies, a decrease in arterial compliance is, however, strongly associated with the atherosclerotic burden [24,25], either because the presence of atherosclerosis leads to stiffening of the arteries and thus to reduced compliance, or because decreased arterial compliance leads to vessel wall damage with subsequent atherosclerotic vascular changes.
We found that both local renal disease, assessed as type and stage of kidney disease, and systemic atherosclerotic vascular changes are independent predictors of ultrasound renal resistance indices. This strengthens information from earlier studies which reported a strong correlation between renal function and ultrasound resistance indices in CKD, but which did not control for systemic atherosclerotic burden [4].
This correlation between renal function and resistance indices in chronic renal disease is in contrast to the findings in stable renal transplant patients, in whom renal function is not significantly associated with transplant renal function in univariate [8,10] or multivariate [9] analyses. This might be explained by the observation that an impairment in renal function in long-term transplant recipients is mostly due to chronic allograft nephropathy. Chronic allograft nephropathy is characterized by rather uniform intrarenal pathological changes which mostly affect the intrarenal vasculature [26]. In contrast, patients suffering from CKD present with a more heterogeneous spectrum of pathological renal changes, which may comprise vascular, glomerular, tubular and interstitial lesions of various extent, and which might therefore result in more organ-specific changes in duplex measurements. This might explain why the degree of impairment in kidney function is associated with ultrasound renal resistance indices in patients suffering from CKD, but not in transplant patients.
Surprisingly, we found that the association between ultrasound resistance indices and systemic vascular changes, assessed as carotid IMT, can largely be explained by the correlation of age with both carotid IMT and ultrasound resistance indices. When adjusting for age, carotid atherosclerosis no longer independently predicted ultrasound renal resistance indices.
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Conclusion |
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In CKD, ultrasound intrarenal resistance indices independently reflect both local renal damage and systemic vascular disease. This may explain why they have been found before to predict both progression of CKD and death. Future ultrasound studies should examine whether a more specific assessment of intrarenal damage may be achieved by correcting renal resistance indices for subclinical atherosclerosis, or by comparing intrarenal resistance indices to resistance indices measured in arteries of non-renal organs, such as splenic arteries.
Conflict of interest statement. None declared.
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[Abstract/Free Full Text]
Accepted in revised form: 19. 7.06
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