Carmine Zoccali,
Francesca Mallamaci and
Pietro Finocchiaro
Unità Opertativa di Nefrologia, Dialisi e Trapianto and CNR Centro di Fisiologia Clinica, Reggio Calabria, Italy.
Correspondence to Dr. Carmine Zoccali, CNR Centro di Fisiologia Clinica, Via Sbarre Inferiori, 39, 89131 Reggio Cal. Italy. Phone: 39-09-653-97010; Fax: 39-09-655-93341;
ABSTRACT. Atherosclerotic renal artery stenosis is the mostcommon primary disease of the renal arteries, and it is associatedwith two major clinical syndromes, ischemic renal disease andhypertension. The prevalence of this disease in the populationis undefined because there is no simple and reliable test thatcan be applied on a large scale. Renal artery involvement inpatients with coronary heart disease and/or heart failure isfrequent, and it may influence cardiovascular outcomes and survivalin these patients. Suspecting renal arterial stenosis in patientswith recurrent episodes of pulmonary edema is justified by observationsshowing that about one third of elderly patients with heartfailure display atherosclerotic renal disease. Whether interventionsaimed at restoring arterial patency may reduce the high mortalityin patients with heart failure is still unclear because, todate, no prospective study has been carried out in these patients.Increased awareness of the need for cost containment has renewedthe interest in clinical cues for suspecting renovascular hypertension.In this regard, the DRASTIC study constitutes an important attemptat validating clinical prediction rules. In this study, a clinicalrule was derived that predicted renal artery stenosis as efficientlyas renal scintigraphy (sensitivity: clinical rule, 65% versusscintigraphy, 72%; specificity: 87% versus 92%). When testedin a systematic and quantitative manner, clinical findings canperform as accurately as more complex tests in the detectionof renal artery stenosis. E-mail: carmine.zoccali@tin.it
Atherosclerotic renal artery stenosis is the most common primarydisease of the renal arteries, and it is associated with twomajor clinical syndromes, ischemic renal disease and hypertension.Renal artery stenosis, ischemic disease, and hypertension maybe variously combined (1). Indeed, hypertension does not representa universal sequela of renal artery stenosis, and renal functionmay be maintained in the presence of bilateral renal arterialdisease. Accurate staging of hypertension and renal dysfunctionis fundamental in these patients because the concomitant presenceof arterial hypertension and renal ischemia constitutes a situationof high cardiovascular risk. In this review, we will focus onsome critical points of the problem from epidemiology to therelationship among atherosclerotic renal artery disease, heartfailure, and survival. We will conclude by touching on the importanceof clinical prediction rules in the screening of this multifaceteddisease.
Renal angiography is the undisputed golden standard in the diagnosticwork-up for renovascular disease; in clinical practice, it isapplied to establish the location and the degree of renal arterystenosis. However, the objectivity of this technique must notbe considered beyond question. There is much disagreement amongone or two observers as to the severity of stenosis. It hasbeen emphasized that even when using broad categories, e.g.,stenosis <70% versus stenosis >70%, in a substantial proportionof cases, the evaluation of radiologists differ as to whethera stenosis is clinically important or not (2). Interobservervariability problems apart, establishing the prevalence andthe incidence rate of hypertension attributable to atheroscleroticrenal disease is also difficult because the degree of renalartery stenosis considered sufficient to cause hypertensionis variable across studies. Undoubtedly, the more severe theprocess, the more likely a given arterial narrowing is to besignificant. This is the reason why 75% narrowing is often theselected cut-off. Yet, studies considering a 50% stenosis significantare not rare (3). From a hemodynamic point of view, a givenstenosis is significant when there is a demonstrable pressuregradient because the pressure drop beyond the stenosis setsin motion intrarenal adaptive mechanisms eventually leadingto renal ischemia and hypertension. In the 1960s, it was observedthat at least a 50% narrowing is required in dogs to generatea pressure gradient (4). This finding is in keeping with a recentstudy in humans (5), which approached the problem by combiningthree-dimensional magnetic resonance angiography and directmeasurement of pressure in the renal artery across the stenotictract.
Another factor that hinders the definition of the problem isthat there is no study on the prevalence of renal artery stenosisat population level. Such a study would demand the availabilityof a simple and reliable screening test, and this is beyondavailable diagnostic technology. The large majority of studiesperformed so far selected patients having the risk factors ofthis disease (e.g., hypertension or renal insufficiency). Theproblem is relevant because hemodynamically significant renalartery stenosis may occur in patients with normal BP and/ornormal GFR. Autopsy series are often quoted as an unbiased sourceof information. However such series are based on patients whodied in hospital, i.e., on series where atherosclerosis is likelyto be a contributor to the cause of death because atheroscleroticcomplications often lead to hospitalization. Furthermore autopsiesare not universally performed on patients who die in hospital.Due to the variability of hospital populations and to a selectionprocess that is difficult to define, it comes as no surprisethat the frequency of renal artery stenosis ranged from 12%to 53% in series examining fewer than 300 patients (6–8)and that it was only 4% in a very large series (over 5000 patients)collected over an 8-yr period (9). In the aggregate, it clearlyemerges that hypertension is not an obligatory sequela of arterialstenosis of the kidney and that this disease is strongly age-dependent.
Systemic Atherosclerosis and Renal Artery Atherosclerosis
Atherosclerosis is a systemic disease. Although asymmetriesin arterial involvement in atherosclerosis may occur, the diseaseusually proceeds in parallel in various organ systems. Froma clinical perspective, knowing the prevalence of renal arteryinvolvement in patients with evidence of atherosclerosis inother organs is important because this knowledge may be incorporatedinto diagnostic algorithms (see Clinical Prediction Rules).There are a number of studies examining the renal arterial systemas a part of abdominal aortography or peripheral arteriographyor as an examination complementary to arterial coronography.The prevalence of renal artery stenosis ranges from 14% to 42%in studies performed on patients with aortic (abdominal) orperipheral vascular disease (10–16). It is somewhat less(11% to 23%) in patients with documented coronary artery disease(17–19). Overall, the larger the study, the lower theprevalence of renal artery stenosis (Figure 1). In the mostextensive study so far (18), 11% of patients had greater than50% unilateral narrowing, 2.4% had bilateral 50% to 75% narrowing,and 1.6% had very severe bilateral stenosis (>75%). Notably,in this study the severity of renal artery disease was predictedby old age, gender, peripheral vascular disease, congestiveheart failure, renal insufficiency, smoking, and by the degreeof coronary artery involvement.
Figure 1. Prevalence of atherosclerotic renal artery stenosis in patients who underwent abdominal aortography or peripheral or coronary angiography. The probability of renal arterial involvement tends to be lower in larger studies.
It is fairly well established that atherosclerotic renal arterystenosis is a progressive disease. Sequential angiographic studieshave documented that progression of arterial stenosis occursat a variable rate in patients followed up for a minimum of6 mo to a maximum of 180 mo (20–25). However, progressionis not universal, and it is well documented that, at least insome cases, risk factor modification may allow partial regressionof stenosis (26,27). Furthermore, bias may inflate the estimateof the risk of progression because patients who are felt tobe at high risk are more intensively investigated. Noninvasivetechniques may give an unbiased estimate of the progressionof the disease. In this regard, well-conceived echo-color Dopplerstudies (28,29) have shown that about one fourth of patientswith nonsignificant stenosis develop a degree of narrowing greaterthan 60% after 1 yr of follow-up and that about one patientout of ten with significant stenosis at baseline develops completearterial occlusion within 2 yr. A large study in over 1000 patientsshowed that the severity of stenosis is linked to the severityof renal insufficiency because serum creatinine was about 40%higher in patients with significant stenosis (>75% RAS) thanin those with a less severe degree of arterial narrowing (30).Overall these findings indicate that it is unlikely that atheroscleroticrenal disease stabilizes without specific therapeutic interventions.
Beyond the Stenosis: Parenchymal Renal Damage and Medium-Small Vessel Disease
The degree of arterial narrowing has long been considered theleading factor, if not the sole, responsible for renal functionloss in patients with atherosclerotic renal artery stenosis.However, clinical studies performed during the last 20 yr havedemonstrated that renal function after revascularization rarelyshows significant improvements. Single-kidney GFR measured byreliable isotopic techniques remains almost unchanged aftersuccessful angioplasty (31,32). Accordingly, the severity ofproximal renal artery stenosis is poorly related to GFR (creatinineclearance) because GFR is similarly reduced in patients withmild and severe stenosis and in those with severe bilateralstenosis (33). These observations may appear at odds with clinicalexperience because renal disease progression is very often fasterin patients with severe stenosis. The contradiction may be onlyapparent because the severity of stenosis probably representsan indicator of other processes responsible for the evolutionof renal insufficiency, e.g., heart failure and nephrosclerosisin the controlateral kidney. The above-mentioned radioisotopicsingle-kidney studies (32) provide firm evidence that renalparenchymal damage is the major factor responsible for renalfunction loss in atherosclerotic renal disease, but these findingsshould not be interpreted as evidence that interventions aimedat restoring arterial patency are of inherently limited value.The scope of angioplasty or surgery is to slow the rate of lossof renal function rather than improving it. Renal revascularizationby restoring parenchymal blood flow reverses only the ischemiccomponent of kidney damage. Apart from stenosis, many factorsmay conjure to damage the kidney. Thus cholesterol embolizationis increasingly recognized as a significant factor in the evolutionof renal failure in these patients (31). On the other hand,damage to medium and small arteries in the kidney, i.e., nephrosclerosis,is an important reason why angioplasty does not restore normalrenal function in most cases. Nephrosclerosis runs in parallelwith systemic atherosclerosis. Indeed in about 300 protocolautopsies in the Honolulu Heart Study (34), it was found thatin subjects with hypertension and diabetes hyalinization ofarterioles and fibroplasia of small arteries in the renal cortexis associated to BP, glucose level, and alcohol intake. Importantly,these associations appeared to be independent predictors ofhyalinization in renal arterioles, giving support to the hypothesisthat this type of renal vasculopathy may be a marker for atherosclerosisin other vascular beds.
Renal Atherosclerosis as a Predictor of Cardiovascular Outcomes and Death
Heart Failure and Atherosclerotic Renal Artery Stenosis
Pickering et al. (35) were the first to draw attention to pulmonaryedema as a complication of bilateral renal artery stenosis.This complication has been attributed to sodium retention andto an increase in permeability in pulmonary microcirculationpromoted by angiotensin II. The hypothesis that renal arterystenosis may be instrumental in precipitating heart failureis supported by the fact that renal angioplasty is associatedwith an objective amelioration of cardiac insufficiency in patientswith severe renovascular disease (35–37). Suspecting renalarterial stenosis in patients with recurrent episodes of pulmonaryedema is also justified by recent observations showing thatthe prevalence of atherosclerotic renal disease in elderly patientswith decompensated cardiac failure is 34% (38). The identificationof these patients is also important because they are at riskof acute renal failure when treated with ACE inhibitors. Theoverall risk of ACE inhibitor–induced acute renal failurein patients with heart failure is about 2% (39). Notwithstandingthe rarity of this complication, serum creatinine should befrequently monitored in patients with compromised left ventricularfunction on treatment with ACE inhibitors or angiotensin IIreceptor antagonists.
Survival
As discussed, atherosclerotic renal disease is frequently associatedwith other cardiovascular complications. For this reason, thepresence of renal arterial disease may be considered a riskmarker for all-cause and cardiovascular mortality. Five-yearsurvival in two historical prospective studies was 7% lowerin patients with renal artery stenosis than in well-matchedessential hypertensives (40) and 23% lower than in the generalpopulation (41). A prospective study by Conlon (42) in 900 patientssubmitted to coronary angiography and abdominal aortographyhas fully confirmed these findings. Indeed 4-yr survival was21% lower in patients with renal artery stenosis than in patientswithout renal artery involvement. Furthermore, atheroscleroticrenal disease had a strong independent effect on long-term survivalindependently of coronary artery disease. More recent observationsby the same group have shown that the probability of survivalis proportional to the severity of arterial narrowing (30).These observations are in line with experimental and clinicaldata, suggesting that renal ischemia may act as a direct triggerof cardiovascular events in renovascular disease. However interestingthey may seem, these observations still leave open the questionas to whether or not angioplasty or renal artery surgery mayreduce the high mortality in heart failure because to date thereis no prospective study on the effect of revascularization procedureson survival in these patients.
In recent years, Echo-color Doppler has emerged as a reliablemethod to orient the diagnostic work up of patients with suspectedrenovascular stenosis. However, this method is partially operator-dependent,and it is difficult to apply on a large scale. Using noninvasivetests for the screening of atherosclerotic renal disease inan indiscriminate manner would have a major impact on cost andon the workload of nuclear medicine, radiology, and internalmedicine departments. As already mentioned, the probabilityof diagnosing renal artery stenosis depends on the particularclinical setting in which the disease occurs. The likelihoodof atherosclerotic renal disease in a patient with coronaryor cerebrovascular disease is higher than that in patients withoutsuch atherosclerotic complications. This pretest probabilityis important because the posttest probability of the diseaseresults from the product of pretest probability and the likelihoodratio of the tests being applied (Figure 2). Prediction rulesmay greatly help the clinician to select patients for angiography.The most quoted clinical features suggestive of renovasculardisease are those reported by the investigators of the time-honoredCooperative Study on Renovascular Hypertension (43). These featureswere identified by comparing a group of 339 essential hypertensivepatients with a group of 175 patients with renovascular hypertension(i.e., hypertension treated by renal artery surgery), and thislatter group was characterized by age, hypertension of shortduration or accelerated hypertension, retinopathy, presenceof coronary, peripheral, and cerebrovascular disease. The validityof this set of clinical findings suggestive of renal arterystenosis in the Cooperative Study has never been formally testedin a prospective study. Furthermore, this information gap stillremains to be bridged because until now no such study exists.Increased awareness of the need for cost containment has renewedthe interest in the clinical signs of renovascular hypertension.The DRASTIC study is the most recent attempt at validating clinicalprediction rules. In this study, the clinical characteristicsof 477 patients selected because drug-resistant hypertensionor an increase in serum creatinine during therapy with ACE inhibitorswere accurately analyzed (44). A regression model predictingthe probability of renal artery stenosis was developed; fromthis model, a clinical prediction rule was derived. The validityof the model was tested by bootstrapping techniques, i.e., bydeveloping the regression model in a randomly selected sub-sampleof patients and then testing the prediction power of the modelin patients not included in the fitting procedure. This approachis an important step forward, but it still does not representthe ideal test because clinical findings do not represent anexception to the rule that independent and prospective assessmentis the gold standard for validating diagnostic procedures. Theimportant result of this study is that the clinical rule predictedrenal artery stenosis as efficiently as renal scintigraphy (sensitivity:clinical rule, 65% versus scintigraphy, 72%; specificity: 87%versus 92%). When tested in a systematic and quantitative manner,clinical findings can perform as accurately as more complextests in the detection of renal artery stenosis.
Figure 2. Performance of a diagnostic test in two different clinical settings. The likelihood ratio of the test is 8 (identical in both situations). In the first situation, the prevalence rate of the disease is 10%; in the second situation, the rate is 40%. As shown in the figure, the posttest probability is low (47%) in the first situation and high (84%) in the second. The formulae for the calculation of pretest and posttest odds and likelihood ratio are also presented.
Knowledge on the clinical evolution and on the cardiovascularsequelae of atherosclerotic renal disease has made substantialprogress in recent years. The impact of angioplasty or surgeryon heart failure and on survival in high-risk patients remainsto be investigated in appropriate clinical trials. In an eraof expanding diagnostic technology, renewed scientific interestin clinical findings may produce a refreshing reanalysis ofthe diagnostic and prognostic pathways of this complex disease.
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Abstract
Introduction
