Fibromuscular Dysplasia
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《新英格兰医药杂志》
Fibromuscular dysplasia is a nonatherosclerotic, noninflammatory vascular disease that most commonly affects the renal and internal carotid arteries but has been described in almost every arterial bed in the body (Table 1).1,2,3,4,5,6,7,8,9,10,11,12 Although the disease was first described by Leadbetter and Burkland in 1938,13 the report by McCormack and coworkers two decades later of four cases of "fibromuscular hyperplasia" was the first accurate pathological description of this entity.14 The clinical presentation may vary from an asymptomatic condition to a multisystem disease that mimics necrotizing vasculitis,15 depending on the arterial segment involved, the degree of stenosis, and the type of fibromuscular dysplasia.
Table 1. Arterial Involvement in Fibromuscular Dysplasia.
Types of Fibromuscular Dysplasia
The pathological classification scheme for fibromuscular lesions of the renal arteries is based on the arterial layer — intima, media, or adventitia — in which the lesion predominates.16 Macroaneurysms and dissections are complications of fibromuscular dysplasia and do not represent distinct histopathological categories.
Medial fibroplasia, which is characterized by its classic "string of beads" appearance, represents the most common dysplastic lesion.4,16 Typically, the beading is larger than the normal caliber of the artery and is located in the middle-to-distal portion of the artery (Figure 1).17 Histologically, there is involvement of the media, whereas the intima, internal elastic lamina, and adventitia are preserved.4,16 The lesion of perimedial fibroplasia is characterized by a homogeneous collar of elastic tissue at the junction of the media and the adventitia. The elastic elements of the media and intima appear normal. Perimedial fibroplasia is diagnosed when focal stenoses and, occasionally, multiple constrictions are observed, often with a robust collateral network. The "beads" are usually less numerous than in medial fibroplasia and are typically smaller in diameter than the normal caliber of the artery (Figure 2).18 Medial hyperplasia accounts for less than 1 percent of arterial stenoses and may be indistinguishable angiographically from intimal fibroplasia.19
Figure 1. Imaging of Fibroplasia.
Panel A shows typical medial fibroplasia ("string of beads" appearance) on an angiogram of a right renal artery. Characteristically, the beads are larger than the normal caliber of the artery. Fibromuscular dysplasia is often located at the middle-to-distal portion of the renal artery. This 55-year-old woman presented with hypertension that was difficult to control. Panel B shows gadolinium-enhanced magnetic resonance angiography in the same patient, revealing bilateral medial fibroplasia of the renal arteries and a large marginal artery of Drummond (arrow), indicating that there is disease of the superior mesenteric artery. This patient had severe medial fibroplasia of the superior mesenteric artery (not shown). In Panel C, a 16-row-multidetector computed tomographic angiogram (a three-dimensional reconstructed image) of the internal carotid artery reveals beading typical of that seen in medial fibroplasia (courtesy of Corey Goldman, M.D., Ph.D., Ochsner Clinic, New Orleans). In Panel D, duplex ultrasonography (power imaging) of the carotid artery shows typical beading of medial fibroplasia in the internal carotid artery several centimeters distal to the carotid bifurcation.
Figure 2. Perimedial Fibroplasia of the Renal Artery (Panel A) and a Near-Normal Renal Artery after Percutaneous Balloon Angioplasty (Panel B).
Careful observation shows that the beads (arrow) in perimedial fibroplasia are less numerous and smaller than those in medial fibroplasia. There is usually a robust collateral circulation in patients with perimedial fibroplasia. (Images courtesy of Anthony W. Stanson, M.D., Mayo Clinic, Rochester, Minnesota.)
Intimal fibroplasia occurs in less than 10 percent of patients with arterial fibrodysplasia.4,16 Angiographically, it may appear as a focal, concentric stenosis (Figure 3A and Figure 3B); a long, smooth narrowing similar to that seen in large-artery vasculitides such as giant-cell arteritis or Takayasu's arteritis17; or a redundancy of the artery (Figure 3C).
Figure 3. Carotid Arteriography in a Patient with Transient Ischemic Attacks.
The arteriogram in Panel A was obtained at presentation; it shows a severe concentric stenosis in the distal internal carotid artery (arrow) in a 36-year-old female patient with a right hemispheric transient ischemic attack (left hemiparesis). This angiographic appearance is typical of intimal fibroplasia. After percutaneous balloon angioplasty, the internal carotid artery had a normal appearance on angiography (Panel B, arrow). Several months later, this patient had several left hemispheric transient ischemic attacks (aphasia and right-sided weakness). The left carotid arteriogram (Panel C) shows a severe redundancy (arrow) and a kink (not demonstrated in this view) in the distal internal carotid artery. This lesion was resected with an end-to-end anastomosis. The pathological features were typical of intimal fibromuscular dysplasia. The patient was asymptomatic from the cerebrovascular standpoint after this operation. (Panels A and B reprinted with permission from Begelman and Olin17; Panel C reprinted with permission from Begelman and Olin.20)
Adventitial (periarterial) hyperplasia is the rarest type of fibrodysplastic lesion.4,16 Although there is currently limited angiographic information, sharply localized, tubular areas of stenosis have been observed.18,19
Pathogenesis
Although a variety of genetic, mechanical, and hormonal factors have been proposed, the cause of fibromuscular dysplasia remains unknown. Cigarette smoking and a history of hypertension are associated with an increased risk of this condition. No association has been found between fibromuscular dysplasia and previous use of oral contraceptives or abnormalities of endogenous sex hormones.21 Genetic factors may play a part in the development of fibromuscular dysplasia, since the disease is more common among the first-degree relatives of patients with fibromuscular dysplasia of the renal arteries22,23 and among persons with the angiotensin-converting–enzyme allele ACE-I.24
Differential Diagnosis
It is usually not difficult to differentiate atherosclerosis from fibromuscular dysplasia. Atherosclerosis generally occurs at the origin or proximal portion of the artery in older patients with typical cardiovascular risk factors. In contrast, fibromuscular dysplasia occurs in the middle or distal arterial segments in younger patients with few cardiovascular risk factors.
The Ehlers–Danlos syndrome (type IV) has been associated with medial fibroplasia.25 This syndrome should be suspected in patients with multiple aneurysms in addition to the typical angiographic findings of fibromuscular dysplasia. There have been isolated reports of fibromuscular dysplasia associated with Alport's syndrome,26 pheochromocytoma,27,28 Marfan's syndrome,29 and Takayasu's arteritis.30,31
At times, it may be difficult to distinguish fibromuscular dysplasia from vasculitis. Fibromuscular dysplasia is, by definition, a noninflammatory process and is therefore not associated with anemia, thrombocytopenia, or abnormalities of acute-phase reactants, except when it occurs during acute infarction. Large-vessel vasculitis may occur in the absence of changes in acute-phase reactants in up to 40 percent of cases.32 When histologic proof or markers of inflammation are unavailable, it may be difficult to distinguish these entities, because their angiographic appearance may be similar, especially if the intimal fibroplasia is of the multivessel type. Although magnetic resonance angiography may show wall thickening in patients with giant-cell arteritis or Takayasu's arteritis,33 it is not useful in patients with renal or intestinal fibromuscular dysplasia, because the resolution of magnetic resonance angiography is inadequate for the visualization of branch-vessel involvement. In some cases, intravascular ultrasonography may help to distinguish fibromuscular dysplasia from vasculitis.34 Multiple-organ involvement in fibromuscular dysplasia is particularly troublesome, since ischemia may be associated with increased risks of complications and death.35
Fibromuscular Dysplasia of the Renal Arteries
Renovascular fibromuscular dysplasia tends to affect women between 15 and 50 years of age. It is not uncommon, however, to encounter patients in whom it first presents after 60 years of age. In most cases, these persons have been asymptomatic for many years, and fibromuscular dysplasia is discovered incidentally during the investigation of another problem. According to recent reports, fibromuscular dysplasia accounts for less than 10 percent of cases of renovascular hypertension.36
The natural history of renal fibromuscular dysplasia has been described in several studies.19,37,38,39,40 The progression of angiographic disease, defined by the occurrence of a new focal lesion, worsening arterial stenosis, or the enlargement of a mural aneurysm, occurs in up to 37 percent of patients with renal fibromuscular dysplasia.19,40 It is often difficult to assess disease progression according to angiographic criteria, especially in patients with medial fibroplasia, in whom it is difficult to gauge the degree of stenosis (Figure 1A).38
Monitoring for changes in the renal parenchyma may provide another means of assessing disease progression. Mounier-Vehier and colleagues used computed tomographic angiography to compare the mean cortical thickness and renal length in 20 patients who had essential hypertension with those in 20 patients who had hypertension and unilateral renal-artery fibromuscular dysplasia.41 As compared with the patients with essential hypertension, the patients with unilateral renal fibromuscular dysplasia had significantly decreased mean cortical thickness and reduced renal length. In the unaffected contralateral kidney, the cortical thickness was also markedly decreased, although the renal length was preserved. Although the loss of renal mass occurs in up to 63 percent of patients with renal-artery fibromuscular dysplasia, renal failure is rare in these patients.38
Imaging
Various imaging methods have been used to detect renal-artery stenosis. Duplex imaging of the renal arteries can accurately detect elevated blood-flow velocities in the proximal portion of these arteries, as well as in the middle-to-distal portion.42,43 Since atherosclerosis rarely occurs in the distal portion of the renal arteries, elevations of velocity in those segments are most often due to fibromuscular dysplasia. Consequently, it is important to scan patients not only by means of an anterior approach, but also with an oblique or flank approach, in order to visualize the distal portions of the renal arteries adequately.34,43 Duplex ultrasonography of the renal arteries serves two other important functions: by measuring the resistive index in the cortical blood vessels, one can predict with a high degree of accuracy the likelihood of a favorable response to revascularization. (The resistive index = x 100.) In a study by Radermacher et al.,44 subjects were more likely to have an improvement in blood pressure and renal function when the resistive index was less than 80 than when it was 80 or higher. However, the resistive index has not been tested in patients with renal-artery stenosis secondary to fibromuscular dysplasia. In addition, duplex ultrasonography is an excellent means by which to assess restenosis after percutaneous intervention.45,46
Although 16-row, multidetector computed tomographic (CT) scanners may play an increasing part in the diagnosis and follow-up of renal-artery fibromuscular dysplasia, there are no good data comparing CT angiography with catheter-based angiography at present.47,48 Similarly, the role of magnetic resonance angiography in the evaluation of renal-artery fibromuscular dysplasia remains uncertain. Even with better equipment and the use of gadolinium contrast medium, the spatial resolution of magnetic resonance angiography (approximately 1 mm) remains inferior to that of catheter angiography (200 to 300 μm).49 The combination of decreased spatial resolution and the movement of the patient may result in an appearance of beading when none exists. Despite improvements in noninvasive imaging methods, catheter-based angiography remains the most accurate method for diagnosing fibromuscular dysplasia.
Although captopril renography was once the noninvasive diagnostic method of choice for patients with renal-artery stenosis, it has now been relegated to use in secondary screening, since the quality of other noninvasive imaging methods is so high. The sensitivity and specificity of captopril renography decrease in the presence of azotemia, bilateral disease, or disease in a solitary functioning kidney.50,51
Therapy
Pharmacologic therapy for hypertension in patients with renal-artery fibromuscular dysplasia should follow the guidelines of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure.52 Revascularization should be considered in certain types of patients: those with a recent onset of hypertension in whom the goal is to cure the hypertension; those in whom blood-pressure control has proved difficult to achieve despite the use of a comprehensive antihypertensive regimen; those with an intolerance to antihypertensive medications; those whose blood pressure has been difficult to control because of noncompliance; and those who have lost renal volume because of ischemic nephropathy.
Before the advent of percutaneous transluminal angioplasty, surgical revascularization was the primary therapeutic alternative for patients with refractory hypertension.3,53,54,55,56 Overall, the technical success rates ranged from 89 to 97 percent. Hypertension was cured in 33 to 63 percent of patients, improved in 24 to 57 percent, and failed to improve in 3 to 33 percent. A longer duration of hypertension, concomitant atherosclerotic disease, and complex branch-vessel repair all adversely affect the results of surgical revascularization.54,56
Although there is a paucity of prospective data demonstrating the superiority of percutaneous transluminal angioplasty over surgical revascularization, the percutaneous approach has emerged as the mainstay of treatment for patients with fibromuscular dysplasia who meet the criteria for intervention. Percutaneous transluminal angioplasty is less costly than surgical revascularization, is less invasive, can be performed on an outpatient basis, and is associated with lower morbidity; moreover, if it is unsuccessful, surgical therapy may still be used (Table 2).3,55,57,58,59,60,61,62,63,64,65,66,67,68 Important advances in the designs of guidewires, catheters, and balloons, as well as improvement in the relevant skills of clinicians, have made it possible to perform angioplasty for even the most complex renal-artery lesions, and it is equally effective in the main renal artery and in branch-artery stenoses.69 Although stents have been used extensively for the treatment of atherosclerotic renal-artery stenosis, the use of stents for fibromuscular dysplasia has been reserved as a "bailout" procedure in cases in which there are suboptimal results with balloon angioplasty or in which renal-artery dissection occurs.64,66 Adjunctive intravascular ultrasonography may be useful in determining whether an intervention has been technically successful.34 Complications of percutaneous intervention occur in up to 14 percent of patients and most commonly involve minor access-related problems. Rarely, renal-artery perforation, dissection, or segmental renal infarction occurs.57,59,60
Table 2. Results of Percutaneous Transluminal Angioplasty of the Renal Arteries in Patients with Fibromuscular Renovascular Disease and Hypertension.
Successful angioplasty often results in a substantial and rapid reduction of both the systolic and the diastolic blood pressure. Improved blood-pressure control correlates with a marked reduction in plasma renin activity and angiotensin II levels.67 Correlates of successful outcome include an age of less than 50 years, the absence of associated coronary or carotid stenoses, and a duration of hypertension of less than eight years.66 The rate of restenosis after balloon angioplasty has ranged from 7 to 27 percent over follow-up periods of six months to two years.61,63,70,71 In rare cases, fibrodysplastic stenosis may coexist with an aneurysm.72 This condition may be treated percutaneously with the use of a covered stent graft or may be repaired surgically.73
Patients who are treated with endovascular or surgical revascularization should undergo duplex ultrasonographic imaging periodically to detect progression of disease, restenosis, or loss of kidney volume.43,71,74 Imaging should be performed soon after revascularization to assess the adequacy of the intervention,46 again after 6 months and after 12 months, and yearly thereafter, or whenever there is a recurrence or worsening of hypertension.
Cerebrovascular Fibromuscular Dysplasia
Cerebrovascular fibromuscular dysplasia may be asymptomatic or associated with a variety of nonspecific symptoms, including headache, tinnitus, vertigo, lightheadedness, and syncope.8,75,76 The more specific neurologic syndromes of transient ischemic attack, amaurosis fugax, stroke, Horner's syndrome, and cranial-nerve palsies may be the first presentation of fibromuscular dysplasia involving the carotid or vertebral arteries8,76 (Figure 3). Cerebrovascular symptoms may be related to critical stenosis or occlusions of major arteries, rupture of an intracranial aneurysm, or cerebral embolism originating from intravascular thrombi in stenotic regions.77 Intracranial or extracranial cerebrovascular fibromuscular dysplasia may also be discovered incidentally as the cause of a cervical bruit or when angiography or some other imaging method is performed for unrelated reasons. The mean age of patients with cerebrovascular fibromuscular dysplasia is approximately 50 years. The natural history of cerebrovascular fibromuscular dysplasia of the medial type is generally benign.78,79,80
Several imaging methods may be used for the detection of intracranial or extracranial cerebrovascular fibromuscular dysplasia. Duplex ultrasonography of the carotid arteries may demonstrate irregular patterns of stenosis and aneurysm81 (Figure 1D), but color-coded duplex ultrasonography has a lower sensitivity than angiography for the detection of cerebrovascular fibromuscular dysplasia.81 Since fibromuscular dysplasia affects the middle and distal portions of the carotid and vertebral arteries at the level of the first and second cervical vertebrae,82 it may be difficult to visualize these lesions by means of duplex ultrasonography. There has been little experience with computed tomographic angiography (Figure 1C) or magnetic resonance angiography for the detection of cerebrovascular fibromuscular dysplasia; however, magnetic resonance angiography should be performed to rule out the presence of intracranial aneurysms in patients with such dysplasia.
Before the use of percutaneous revascularization became widespread, surgery was the mainstay of therapy for patients with symptomatic cerebrovascular fibromuscular dysplasia. The surgical technique used depended on the type of lesion and its location, but the most widely used procedure was graduated intraluminal dilatation.82,83,84,85 Other procedures that have been used include intraoperative balloon angioplasty,86 placement of a polytetrafluoroethylene-covered endograft,87 resection of the diseased segment and primary anastomosis (Figure 3C), grafting of autogenous saphenous vein, resection of the aneurysm, and carotid endarterectomy.82,88,89
During the past 10 years, percutaneous angioplasty has become the preferred treatment for symptomatic cerebrovascular fibromuscular dysplasia90,91,92,93,94,95,96,97 (Figure 3A and Figure 3B). There have been no randomized, controlled trials comparing surgery with balloon angioplasty in this condition. Studies in patients with atherosclerotic carotid artery disease suggest that the use of cerebral protection devices may reduce the frequency of ischemic neurologic events during stenting of the carotid artery.98,99,100 When these devices receive approval from the Food and Drug Administration, they will probably be used during percutaneous intervention for the treatment of fibromuscular dysplasia in the carotid artery.
Fibromuscular Dysplasia in Other Vascular Territories
Of the arteries that supply blood to the lower extremities, the iliac arteries are the most likely to be affected by fibromuscular dysplasia, although this condition has been described in the femoral, popliteal, and tibioperoneal arteries as well.9,101 Patients with fibromuscular dysplasia in the pelvic or leg arteries may present with intermittent claudication, critical limb ischemia, or peripheral microembolism that manifests as pain and cyanosis in the toes. In the arms, fibromuscular dysplasia is identified most frequently in the subclavian arteries but has also been described in the brachial and axillary arteries.5,6 In severe cases, patients have weakness, paresthesias, or claudication in their arms. For symptomatic fibromuscular dysplasia in the arms or legs, treatment consists of percutaneous balloon angioplasty.102,103
Fibromuscular dysplasia in the visceral arteries typically involves the celiac, superior mesenteric, inferior mesenteric, hepatic, and splenic arteries.2,104 Intestinal angina may occur when at least two of the major mesenteric arteries are obstructed. In unusual cases, the stenosis progresses to total occlusion, leading to acute intestinal ischemia.105,106 Treatment options include percutaneous intervention and surgical bypass.
As is the case with most rare diseases, it is difficult to conduct a prospective study of various treatment options. Therefore, most treatment decisions are based on data derived from retrospective case series and anecdotal reports. Thanks to advances in imaging methods and enhancement of the interventional armamentarium, treatment has become less invasive and is now at least as effective as previous surgical approaches while being associated with lower morbidity. Future studies will involve the use of protection devices at the time of percutaneous intervention in order to prevent distal embolization. There is no role for stent implantation as a primary treatment for fibromuscular dysplasia, since angioplasty alone is quite effective. Further study of the pathogenesis of fibromuscular dysplasia is needed so that we may gain a better understanding of this disease.
Dr. Slovut reports having received grant support from Volcano Therapeutics.
We are indebted to Jonathan L. Halperin, M.D., for his helpful suggestions and to Micheline Watt for assistance in the preparation of the manuscript.
Source Information
From the Zena and Michael A. Wiener Cardiovascular Institute, Mount Sinai School of Medicine, New York.
Address reprint requests to Dr. Olin at the Zena and Michael A. Wiener Cardiovascular Institute, Mount Sinai School of Medicine, 1 Gustave L. Levy Pl., Box 1033, New York, NY 10029-6574, or at jeffrey.olin@msnyuhealth.org.
References
Kojima A, Shindo S, Kubota K, et al. Successful surgical treatment of a patient with multiple visceral artery aneurysms due to fibromuscular dysplasia. Cardiovasc Surg 2002;10:157-160.
Insall RL, Chamberlain J, Loose HW. Fibromuscular dysplasia of visceral arteries. Eur J Vasc Surg 1992;6:668-672.
Luscher TF, Keller HM, Imhof HG, et al. Fibromuscular hyperplasia: extension of the disease and therapeutic outcome: results of the University Hospital Zurich Cooperative Study on Fibromuscular Hyperplasia. Nephron 1986;44:109-114.
Stanley JC, Gewertz BL, Bove EL, Sottiurai V, Fry WJ. Arterial fibrodysplasia: histopathologic character and current etiologic concepts. Arch Surg 1975;110:561-566.
Cutts S, Grewal RS, Downing R. Bilateral brachial artery fibromuscular dysplasia. Eur J Vasc Endovasc Surg 2000;19:667-668.
Suzuki H, Daida H, Sakurai H, Yamaguchi H. Familial fibromuscular dysplasia of bilateral brachial arteries. Heart 1999;82:251-252.
Radhi JM, McKay R, Tyrrell MJ. Fibromuscular dysplasia of the aorta presenting as multiple recurrent thoracic aneurysms. Int J Angiol 1998;7:215-8.
Mettinger KL. Fibromuscular dysplasia and the brain. II. Current concept of the disease. Stroke 1982;13:53-58.
van den Dungen JJ, Boontje AH, Oosterhuis JW. Femoropopliteal arterial fibrodysplasia. Br J Surg 1990;77:396-399.
Rybka SJ, Novick AC. Concomitant carotid, mesenteric and renal artery stenosis due to primary intimal fibroplasia. J Urol 1983;129:798-800.
Wessely Z, Guerry RL, Klavins JV. Disseminated fibromuscular hyperplasia of vascular channels. Arch Pathol 1973;96:179-182.
Rosenberger A, Adler O, Lichtig H. Angiographic appearance of the renal vein in a case of fibromuscular dysplasia of the artery. Radiology 1976;118:579-580.
Leadbetter WF, Burkland CE. Hypertension in unilateral renal disease. J Urol 1938;39:611-626.
McCormack LJ, Hazard JB, Poutasse EF. Obstructive lesions of the renal artery associated with remediable hypertension. Am J Pathol 1958;34:582-582. abstract.
Olin JW. Syndromes that mimic vasculitis. Curr Opin Cardiol 1991;6:768-774.
Harrison EG Jr, McCormack LJ. Pathologic classification of renal arterial disease in renovascular hypertension. Mayo Clin Proc 1971;46:161-167.
Begelman SM, Olin JW. Fibromuscular dysplasia. Curr Opin Rheumatol 2000;12:41-47.
McCormack LJ, Poutasse EF, Meaney TF, Noto TJ Jr, Dustan HP. A pathologic-arteriographic correlation of renal arterial disease. Am Heart J 1966;72:188-198.
Kincaid OW, Davis GD, Hallermann FJ, Hunt JC. Fibromuscular dysplasia of the renal arteries: arteriographic features, classification, and observations on natural history of the disease. Am J Roentgenol Radium Ther Nucl Med 1968;104:271-282.
Begelman SM, Olin JW. Nonatherosclerotic arterial disease of the extracranial cerebrovasculature. Semin Vasc Surg 2000;13:153-164.
Sang CN, Whelton PK, Hamper UM, et al. Etiologic factors in renovascular fibromuscular dysplasia: a case-control study. Hypertension 1989;14:472-479.
Pannier-Moreau I, Grimbert P, Fiquet-Kempf B, et al. Possible familial origin of multifocal renal artery fibromuscular dysplasia. J Hypertens 1997;15:1797-1801.
Grimbert P, Fiquet-Kempf B, Coudol P, et al. étude génétique de la dysplasie fibromusculaire des artères rénales. Arch Mal Coeur Vaiss 1998;91:1069-1071.
Bofinger A, Hawley C, Fisher P, Daunt N, Stowasser M, Gordon R. Polymorphisms of the renin-angiotensin system in patients with multifocal renal arterial fibromuscular dysplasia. J Hum Hypertens 2001;15:185-190.
Schievink WI, Limburg M. Angiographic abnormalities mimicking fibromuscular dysplasia in a patient with Ehlers-Danlos syndrome, type IV. Neurosurgery 1989;25:482-483.
Hudgins LB, Limbacher JP II. Fibromuscular dysplasia in Alport's syndrome. J Tenn Med Assoc 1982;75:733-735.
Qunibi WJ, Taylor TK, Knight TF, Senekjian HO, Gomez L, Weinman EJ. Pheochromocytoma and fibromuscular hyperplasia. South Med J 1979;72:1481-1482.
de Mendonca WC, Espat PA. Pheochromocytoma associated with arterial fibromuscular dysplasia. Am J Clin Pathol 1981;75:749-754.
Schievink WI, Bjornsson J, Piepgras DG. Coexistence of fibromuscular dysplasia and cystic medial necrosis in a patient with Marfan's syndrome and bilateral carotid artery dissections. Stroke 1994;25:2492-2496.
Janzen J, Vuong PN, Rothenberger-Janzen K. Takayasu's arteritis and fibromuscular dysplasia as causes of acquired atypical coarctation of the aorta: retrospective analysis of seven cases. Heart Vessels 1999;14:277-282.
D'Souza SJ, Tsai WS, Silver MM, et al. Diagnosis and management of stenotic aorto-arteriopathy in childhood. J Pediatr 1998;132:1016-1022.
Jaff MR, Olin JW, Young JR. Failure of acute phase reactants to predict disease activity in Takayasu's arteritis. J Vasc Med Biol 1993;4:223-7.
Flamm SD, White RD, Hoffman GS. The clinical application of `edema-weighted' magnetic resonance imaging in the assessment of Takayasu's arteritis. Int J Cardiol 1998;66:Suppl 1:S151-S161.
Gowda MS, Loeb AL, Crouse LJ, Kramer PH. Complementary roles of color-flow duplex imaging and intravascular ultrasound in the diagnosis of renal artery fibromuscular dysplasia: should renal arteriography serve as the "gold standard"? J Am Coll Cardiol 2003;41:1305-1311.
Stokes JB, Bonsib SM, McBride JW. Diffuse intimal fibromuscular dysplasia with multiorgan failure. Arch Intern Med 1996;156:2611-2614.
Safian RD, Textor SC. Renal-artery stenosis. N Engl J Med 2001;344:431-442.
Cragg AH, Smith TP, Thompson BH, et al. Incidental fibromuscular dysplasia in potential renal donors: long-term clinical follow-up. Radiology 1989;172:145-147.
Goncharenko V, Gerlock AJ Jr, Shaff MI, Hollifield JW. Progression of renal artery fibromuscular dysplasia in 42 patients as seen on angiography. Radiology 1981;139:45-51.
Meaney TF, Dustan HP, McCormack LJ. Natural history of renal artery disease. Radiology 1968;91:881-887.
Schreiber MJ, Pohl MA, Novick AC. The natural history of atherosclerotic and fibrous renal artery disease. Urol Clin North Am 1984;11:383-392.
Mounier-Vehier C, Lions C, Jaboureck O, et al. Parenchymal consequences of fibromuscular dysplasia renal artery stenosis. Am J Kidney Dis 2002;40:1138-1145.
Olin JW, Piedmonte M, Young JR, DeAnna S, Grubb M, Childs MB. Utility of duplex scanning of the renal arteries for diagnosing significant renal artery stenosis. Ann Intern Med 1995;122:833-838.
Carman TL, Olin JW, Czum J. Noninvasive imaging of renal arteries. Urol Clin North Am 2001;28:815-826.
Radermacher J, Chavan A, Bleck J, et al. Use of Doppler ultrasonography to predict the outcome of therapy for renal-artery stenosis. N Engl J Med 2001;344:410-417.
Napoli V, Pinto S, Bargellini I, et al. Duplex ultrasonographic study of the renal arteries before and after renal artery stenting. Eur Radiol 2002;12:796-803.
Edwards JM, Zaccardi MJ, Strandness DE Jr. A preliminary study of the role of duplex scanning in defining the adequacy of treatment of patients with renal artery fibromuscular dysplasia. J Vasc Surg 1992;15:604-611.
Rubin GD. MDCT imaging of the aorta and peripheral vessels. Eur J Radiol 2003;45:Suppl 1:S42-S49.
Funabashi N, Komiyama N, Komuro I. Fibromuscular dysplasia in renovascular hypertension demonstrated by multislice CT: comparison with conventional angiogram and intravascular ultrasound. Heart 2003;89:639-639.
Marcos HB, Choyke PL. Magnetic resonance angiography of the kidney. Semin Nephrol 2000;20:450-455.
Fommei E, Ghione S, Hilson AJ, et al. Captopril radionuclide test in renovascular hypertension: a European multicentre study. Eur J Nucl Med 1993;20:617-623.
van Jaarsveld BC, Krijnen P, Derkx FH, Oei HY, Postma CT, Schalekamp MA. The place of renal scintigraphy in the diagnosis of renal artery stenosis: fifteen years of clinical experience. Arch Intern Med 1997;157:1226-1234.
Chobanian AV, Bakris GL, Black HR, et al. The Seventh Report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure: the JNC 7 report. JAMA 2003;289:2560-2572.
Reiher L, Pfeiffer T, Sandmann W. Long-term results after surgical reconstruction for renal artery fibromuscular dysplasia. Eur J Vasc Endovasc Surg 2000;20:556-559.
Anderson CA, Hansen KJ, Benjamin ME, Keith DR, Craven TE, Dean RH. Renal artery fibromuscular dysplasia: results of current surgical therapy. J Vasc Surg 1995;22:207-216.
Hagg A, Aberg H, Eriksson I, Lorelius LE, Morlin C. Fibromuscular dysplasia of the renal artery -- management and outcome. Acta Chir Scand 1987;153:15-20.
Novick AC, Ziegelbaum M, Vidt DG, Gifford RW Jr, Pohl MA, Goormastic M. Trends in surgical revascularization for renal artery disease: ten years' experience. JAMA 1987;257:498-501.
Sos TA, Pickering TG, Sniderman K, et al. Percutaneous transluminal renal angioplasty in renovascular hypertension due to atheroma or fibromuscular dysplasia. N Engl J Med 1983;309:274-279.
Baert AL, Wilms G, Amery A, Vermylen J, Suy R. Percutaneous transluminal renal angioplasty: initial results and long-term follow-up in 202 patients. Cardiovasc Intervent Radiol 1990;13:22-28.
Tegtmeyer CJ, Selby JB, Hartwell GD, Ayers C, Tegtmeyer V. Results and complications of angioplasty in fibromuscular disease. Circulation 1991;83:Suppl I:I-155.
Bonelli FS, McKusick MA, Textor SC, et al. Renal artery angioplasty: technical results and clinical outcome in 320 patients. Mayo Clin Proc 1995;70:1041-1052.
Jensen G, Zachrisson BF, Delin K, Volkmann R, Aurell M. Treatment of renovascular hypertension: one year results of renal angioplasty. Kidney Int 1995;48:1936-1945.
Davidson RA, Barri Y, Wilcox CS. Predictors of cure of hypertension in fibromuscular renovascular disease. Am J Kidney Dis 1996;28:334-338.
Klow NE, Paulsen D, Vatne K, Rokstad B, Lien B, Fauchald P. Percutaneous transluminal renal artery angioplasty using the coaxial technique: ten years of experience from 591 procedures in 419 patients. Acta Radiol 1998;39:594-603.
Birrer M, Do DD, Mahler F, Triller J, Baumgartner I. Treatment of renal artery fibromuscular dysplasia with balloon angioplasty: a prospective follow-up study. Eur J Vasc Endovasc Surg 2002;23:146-152.
Surowiec SM, Sivamurthy N, Rhodes JM, et al. Percutaneous therapy for renal artery fibromuscular dysplasia. Ann Vasc Surg 2003;17:650-655.
de Fraissinette B, Garcier JM, Dieu V, et al. Percutaneous transluminal angioplasty of dysplastic stenoses of the renal artery: results on 70 adults. Cardiovasc Intervent Radiol 2003;26:46-51.
Airoldi F, Palatresi S, Marana I, et al. Angioplasty of atherosclerotic and fibromuscular renal artery stenosis: time course and predicting factors of the effects on renal function. Am J Hypertens 2000;13:1210-1217.
Archibald GR, Beckmann CF, Libertino JA. Focal renal artery stenosis caused by fibromuscular dysplasia: treatment by percutaneous transluminal angioplasty. AJR Am J Roentgenol 1988;151:593-596.
Cluzel P, Raynaud A, Beyssen B, Pagny JY, Gaux JC. Stenoses of renal branch arteries in fibromuscular dysplasia: results of percutaneous transluminal angioplasty. Radiology 1994;193:227-232.
Plouin PF, Darne B, Chatellier G, et al. Restenosis after a first percutaneous transluminal renal angioplasty. Hypertension 1993;21:89-96.
Baumgartner I, Triller J, Mahler F. Patency of percutaneous transluminal renal angioplasty: a prospective sonographic study. Kidney Int 1997;51:798-803.
Krumme B, Blum U. Renal artery aneurysm and fibromuscular dysplasia. Nephrol Dial Transplant 1997;12:1067-1069.
Bisschops RH, Popma JJ, Meyerovitz MF. Treatment of fibromuscular dysplasia and renal artery aneurysm with use of a stent-graft. J Vasc Interv Radiol 2001;12:757-760.
Olin JW. Atherosclerotic renal artery disease. Cardiol Clin 2002;20:547-562.
Van Damme H, Sakalihasan N, Limet R. Fibromuscular dysplasia of the internal carotid artery: personal experience with 13 cases and literature review. Acta Chir Belg 1999;99:163-168.
Mettinger KL, Ericson K. Fibromuscular dysplasia and the brain. I. Observations on angiographic, clinical and genetic characteristics. Stroke 1982;13:46-52.
Luscher TF, Lie JT, Stanson AW, Houser OW, Hollier LH, Sheps SG. Arterial fibromuscular dysplasia. Mayo Clin Proc 1987;62:931-952.
Stewart MT, Moritz MW, Smith RB III, Fulenwider JT, Perdue GD. The natural history of carotid fibromuscular dysplasia. J Vasc Surg 1986;3:305-310.
Wells RP, Smith RR. Fibromuscular dysplasia of the internal carotid artery: a long term follow-up. Neurosurgery 1982;10:39-43.
Wesen CA, Elliott BM. Fibromuscular dysplasia of the carotid arteries. Am J Surg 1986;151:448-451.
Arning C. Nonatherosclerotic disease of the cervical arteries: role of ultrasonography for diagnosis. Vasa 2001;30:160-167.
Effeney DJ, Krupski WC, Stoney RJ, Ehrenfeld WK. Fibromuscular dysplasia of the carotid artery. Aust N Z J Surg 1983;53:527-531.
Collins GJ Jr, Rich NM, Clagett GP, Spebar MJ, Salander JM. Fibromuscular dysplasia of the internal carotid arteries: clinical experience and follow-up. Ann Surg 1981;194:89-96.
Starr DS, Lawrie GM, Morris GC Jr. Fibromuscular disease of carotid arteries: long term results of graduated internal dilatation. Stroke 1981;12:196-199.
Chiche L, Bahnini A, Koskas F, Kieffer E. Occlusive fibromuscular disease of arteries supplying the brain: results of surgical treatment. Ann Vasc Surg 1997;11:496-504.
Smith LL, Smith DC, Killeen JD, Hasso AN. Operative balloon angioplasty in the treatment of internal carotid artery fibromuscular dysplasia. J Vasc Surg 1987;6:482-487.
Finsterer J, Strassegger J, Haymerle A, Hagmuller G. Bilateral stenting of symptomatic and asymptomatic internal carotid artery stenosis due to fibromuscular dysplasia. J Neurol Neurosurg Psychiatry 2000;69:683-686.
Moreau P, Albat B, Thevenet A. Fibromuscular dysplasia of the internal carotid artery: long-term surgical results. J Cardiovasc Surg (Torino) 1993;34:465-472.
Martin EC, Diamond NG, Casarella WJ. Percutaneous transluminal angioplasty in non-atherosclerotic disease. Radiology 1980;135:27-33.
Ballard JL, Guinn JE, Killeen JD, Smith DC. Open operative balloon angioplasty of the internal carotid artery: a technique in evolution. Ann Vasc Surg 1995;9:390-393.
Brown MM. Balloon angioplasty for cerebrovascular disease. Neurol Res 1992;14:Suppl:159-163.
Garrido E, Montoya J. Transluminal dilatation of internal carotid artery in fibromuscular dysplasia: a preliminary report. Surg Neurol 1981;16:469-471.
Belan A, Vesela M, Vanek I, Weiss K, Peregrin JH. Percutaneous transluminal angioplasty of fibromuscular dysplasia of the internal carotid artery. Cardiovasc Intervent Radiol 1982;5:79-81.
Wilms GE, Smits J, Baert AL, De Wolf L. Percutaneous transluminal angioplasty in fibromuscular dysplasia of the internal carotid artery: one year clinical and morphological follow-up. Cardiovasc Intervent Radiol 1985;8:20-23.
Dublin AB, Baltaxe HA, Cobb CA III. Percutaneous transluminal carotid angioplasty and detachable balloon embolization in fibromuscular dysplasia. AJNR Am J Neuroradiol 1984;5:646-648.
Welch EL, Lemkin JA, Geary JE. Gruntzig balloon dilation for fibromuscular dysplasia of the internal carotid arteries. N Y State J Med 1985;85:115-117.
Tsai FY, Matovich V, Hieshima G, et al. Percutaneous transluminal angioplasty of the carotid artery. AJNR Am J Neuroradiol 1986;7:349-358.
Al-Mubarak N, Roubin GS, Vitek JJ, Iyer SS, New G, Leon MB. Effect of the distal-balloon protection system on microembolization during carotid stenting. Circulation 2001;104:1999-2002.
Ohki T, Veith FJ, Grenell S, et al. Initial experience with cerebral protection devices to prevent embolization during carotid artery stenting. J Vasc Surg 2002;36:1175-1185.
Henry M, Henry I, Klonaris C, et al. Benefits of cerebral protection during carotid stenting with the PercuSurge GuardWire system: midterm results. J Endovasc Ther 2002;9:1-13.
Vertruyen M, Garcez JL. Fibromuscular dysplasia of the superficial femoral artery: an unusual localization. Acta Chir Belg 1993;93:249-251.
Yoshida T, Ohashi I, Suzuki S, Iwai T. Fibromuscular disease of the brachial artery with digital emboli treated effectively by transluminal angioplasty. Cardiovasc Intervent Radiol 1994;17:99-101.
Mandke JV, Sharma S, Phatak AM, Sanzgiri VP, Loya YS, Desai DM. Catheter atherectomy of intimal fibroplasia of the common iliac artery. Cathet Cardiovasc Diagn 1993;30:30-32.
Yamaguchi R, Yamaguchi A, Isogai M, Hori A, Kin Y. Fibromuscular dysplasia of the visceral arteries. Am J Gastroenterol 1996;91:1635-1638.
Hamed RM, Ghandour K. Abdominal angina and intestinal gangrene -- a catastrophic presentation of arterial fibromuscular dysplasia: case report and review of the literature. J Pediatr Surg 1997;32:1379-1380.
Horie T, Seino Y, Miyauchi Y, et al. Unusual petal-like fibromuscular dysplasia as a cause of acute abdomen and circulatory shock. Jpn Heart J 2002;43:301-305.(David P. Slovut, M.D., Ph)
Table 1. Arterial Involvement in Fibromuscular Dysplasia.
Types of Fibromuscular Dysplasia
The pathological classification scheme for fibromuscular lesions of the renal arteries is based on the arterial layer — intima, media, or adventitia — in which the lesion predominates.16 Macroaneurysms and dissections are complications of fibromuscular dysplasia and do not represent distinct histopathological categories.
Medial fibroplasia, which is characterized by its classic "string of beads" appearance, represents the most common dysplastic lesion.4,16 Typically, the beading is larger than the normal caliber of the artery and is located in the middle-to-distal portion of the artery (Figure 1).17 Histologically, there is involvement of the media, whereas the intima, internal elastic lamina, and adventitia are preserved.4,16 The lesion of perimedial fibroplasia is characterized by a homogeneous collar of elastic tissue at the junction of the media and the adventitia. The elastic elements of the media and intima appear normal. Perimedial fibroplasia is diagnosed when focal stenoses and, occasionally, multiple constrictions are observed, often with a robust collateral network. The "beads" are usually less numerous than in medial fibroplasia and are typically smaller in diameter than the normal caliber of the artery (Figure 2).18 Medial hyperplasia accounts for less than 1 percent of arterial stenoses and may be indistinguishable angiographically from intimal fibroplasia.19
Figure 1. Imaging of Fibroplasia.
Panel A shows typical medial fibroplasia ("string of beads" appearance) on an angiogram of a right renal artery. Characteristically, the beads are larger than the normal caliber of the artery. Fibromuscular dysplasia is often located at the middle-to-distal portion of the renal artery. This 55-year-old woman presented with hypertension that was difficult to control. Panel B shows gadolinium-enhanced magnetic resonance angiography in the same patient, revealing bilateral medial fibroplasia of the renal arteries and a large marginal artery of Drummond (arrow), indicating that there is disease of the superior mesenteric artery. This patient had severe medial fibroplasia of the superior mesenteric artery (not shown). In Panel C, a 16-row-multidetector computed tomographic angiogram (a three-dimensional reconstructed image) of the internal carotid artery reveals beading typical of that seen in medial fibroplasia (courtesy of Corey Goldman, M.D., Ph.D., Ochsner Clinic, New Orleans). In Panel D, duplex ultrasonography (power imaging) of the carotid artery shows typical beading of medial fibroplasia in the internal carotid artery several centimeters distal to the carotid bifurcation.
Figure 2. Perimedial Fibroplasia of the Renal Artery (Panel A) and a Near-Normal Renal Artery after Percutaneous Balloon Angioplasty (Panel B).
Careful observation shows that the beads (arrow) in perimedial fibroplasia are less numerous and smaller than those in medial fibroplasia. There is usually a robust collateral circulation in patients with perimedial fibroplasia. (Images courtesy of Anthony W. Stanson, M.D., Mayo Clinic, Rochester, Minnesota.)
Intimal fibroplasia occurs in less than 10 percent of patients with arterial fibrodysplasia.4,16 Angiographically, it may appear as a focal, concentric stenosis (Figure 3A and Figure 3B); a long, smooth narrowing similar to that seen in large-artery vasculitides such as giant-cell arteritis or Takayasu's arteritis17; or a redundancy of the artery (Figure 3C).
Figure 3. Carotid Arteriography in a Patient with Transient Ischemic Attacks.
The arteriogram in Panel A was obtained at presentation; it shows a severe concentric stenosis in the distal internal carotid artery (arrow) in a 36-year-old female patient with a right hemispheric transient ischemic attack (left hemiparesis). This angiographic appearance is typical of intimal fibroplasia. After percutaneous balloon angioplasty, the internal carotid artery had a normal appearance on angiography (Panel B, arrow). Several months later, this patient had several left hemispheric transient ischemic attacks (aphasia and right-sided weakness). The left carotid arteriogram (Panel C) shows a severe redundancy (arrow) and a kink (not demonstrated in this view) in the distal internal carotid artery. This lesion was resected with an end-to-end anastomosis. The pathological features were typical of intimal fibromuscular dysplasia. The patient was asymptomatic from the cerebrovascular standpoint after this operation. (Panels A and B reprinted with permission from Begelman and Olin17; Panel C reprinted with permission from Begelman and Olin.20)
Adventitial (periarterial) hyperplasia is the rarest type of fibrodysplastic lesion.4,16 Although there is currently limited angiographic information, sharply localized, tubular areas of stenosis have been observed.18,19
Pathogenesis
Although a variety of genetic, mechanical, and hormonal factors have been proposed, the cause of fibromuscular dysplasia remains unknown. Cigarette smoking and a history of hypertension are associated with an increased risk of this condition. No association has been found between fibromuscular dysplasia and previous use of oral contraceptives or abnormalities of endogenous sex hormones.21 Genetic factors may play a part in the development of fibromuscular dysplasia, since the disease is more common among the first-degree relatives of patients with fibromuscular dysplasia of the renal arteries22,23 and among persons with the angiotensin-converting–enzyme allele ACE-I.24
Differential Diagnosis
It is usually not difficult to differentiate atherosclerosis from fibromuscular dysplasia. Atherosclerosis generally occurs at the origin or proximal portion of the artery in older patients with typical cardiovascular risk factors. In contrast, fibromuscular dysplasia occurs in the middle or distal arterial segments in younger patients with few cardiovascular risk factors.
The Ehlers–Danlos syndrome (type IV) has been associated with medial fibroplasia.25 This syndrome should be suspected in patients with multiple aneurysms in addition to the typical angiographic findings of fibromuscular dysplasia. There have been isolated reports of fibromuscular dysplasia associated with Alport's syndrome,26 pheochromocytoma,27,28 Marfan's syndrome,29 and Takayasu's arteritis.30,31
At times, it may be difficult to distinguish fibromuscular dysplasia from vasculitis. Fibromuscular dysplasia is, by definition, a noninflammatory process and is therefore not associated with anemia, thrombocytopenia, or abnormalities of acute-phase reactants, except when it occurs during acute infarction. Large-vessel vasculitis may occur in the absence of changes in acute-phase reactants in up to 40 percent of cases.32 When histologic proof or markers of inflammation are unavailable, it may be difficult to distinguish these entities, because their angiographic appearance may be similar, especially if the intimal fibroplasia is of the multivessel type. Although magnetic resonance angiography may show wall thickening in patients with giant-cell arteritis or Takayasu's arteritis,33 it is not useful in patients with renal or intestinal fibromuscular dysplasia, because the resolution of magnetic resonance angiography is inadequate for the visualization of branch-vessel involvement. In some cases, intravascular ultrasonography may help to distinguish fibromuscular dysplasia from vasculitis.34 Multiple-organ involvement in fibromuscular dysplasia is particularly troublesome, since ischemia may be associated with increased risks of complications and death.35
Fibromuscular Dysplasia of the Renal Arteries
Renovascular fibromuscular dysplasia tends to affect women between 15 and 50 years of age. It is not uncommon, however, to encounter patients in whom it first presents after 60 years of age. In most cases, these persons have been asymptomatic for many years, and fibromuscular dysplasia is discovered incidentally during the investigation of another problem. According to recent reports, fibromuscular dysplasia accounts for less than 10 percent of cases of renovascular hypertension.36
The natural history of renal fibromuscular dysplasia has been described in several studies.19,37,38,39,40 The progression of angiographic disease, defined by the occurrence of a new focal lesion, worsening arterial stenosis, or the enlargement of a mural aneurysm, occurs in up to 37 percent of patients with renal fibromuscular dysplasia.19,40 It is often difficult to assess disease progression according to angiographic criteria, especially in patients with medial fibroplasia, in whom it is difficult to gauge the degree of stenosis (Figure 1A).38
Monitoring for changes in the renal parenchyma may provide another means of assessing disease progression. Mounier-Vehier and colleagues used computed tomographic angiography to compare the mean cortical thickness and renal length in 20 patients who had essential hypertension with those in 20 patients who had hypertension and unilateral renal-artery fibromuscular dysplasia.41 As compared with the patients with essential hypertension, the patients with unilateral renal fibromuscular dysplasia had significantly decreased mean cortical thickness and reduced renal length. In the unaffected contralateral kidney, the cortical thickness was also markedly decreased, although the renal length was preserved. Although the loss of renal mass occurs in up to 63 percent of patients with renal-artery fibromuscular dysplasia, renal failure is rare in these patients.38
Imaging
Various imaging methods have been used to detect renal-artery stenosis. Duplex imaging of the renal arteries can accurately detect elevated blood-flow velocities in the proximal portion of these arteries, as well as in the middle-to-distal portion.42,43 Since atherosclerosis rarely occurs in the distal portion of the renal arteries, elevations of velocity in those segments are most often due to fibromuscular dysplasia. Consequently, it is important to scan patients not only by means of an anterior approach, but also with an oblique or flank approach, in order to visualize the distal portions of the renal arteries adequately.34,43 Duplex ultrasonography of the renal arteries serves two other important functions: by measuring the resistive index in the cortical blood vessels, one can predict with a high degree of accuracy the likelihood of a favorable response to revascularization. (The resistive index = x 100.) In a study by Radermacher et al.,44 subjects were more likely to have an improvement in blood pressure and renal function when the resistive index was less than 80 than when it was 80 or higher. However, the resistive index has not been tested in patients with renal-artery stenosis secondary to fibromuscular dysplasia. In addition, duplex ultrasonography is an excellent means by which to assess restenosis after percutaneous intervention.45,46
Although 16-row, multidetector computed tomographic (CT) scanners may play an increasing part in the diagnosis and follow-up of renal-artery fibromuscular dysplasia, there are no good data comparing CT angiography with catheter-based angiography at present.47,48 Similarly, the role of magnetic resonance angiography in the evaluation of renal-artery fibromuscular dysplasia remains uncertain. Even with better equipment and the use of gadolinium contrast medium, the spatial resolution of magnetic resonance angiography (approximately 1 mm) remains inferior to that of catheter angiography (200 to 300 μm).49 The combination of decreased spatial resolution and the movement of the patient may result in an appearance of beading when none exists. Despite improvements in noninvasive imaging methods, catheter-based angiography remains the most accurate method for diagnosing fibromuscular dysplasia.
Although captopril renography was once the noninvasive diagnostic method of choice for patients with renal-artery stenosis, it has now been relegated to use in secondary screening, since the quality of other noninvasive imaging methods is so high. The sensitivity and specificity of captopril renography decrease in the presence of azotemia, bilateral disease, or disease in a solitary functioning kidney.50,51
Therapy
Pharmacologic therapy for hypertension in patients with renal-artery fibromuscular dysplasia should follow the guidelines of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure.52 Revascularization should be considered in certain types of patients: those with a recent onset of hypertension in whom the goal is to cure the hypertension; those in whom blood-pressure control has proved difficult to achieve despite the use of a comprehensive antihypertensive regimen; those with an intolerance to antihypertensive medications; those whose blood pressure has been difficult to control because of noncompliance; and those who have lost renal volume because of ischemic nephropathy.
Before the advent of percutaneous transluminal angioplasty, surgical revascularization was the primary therapeutic alternative for patients with refractory hypertension.3,53,54,55,56 Overall, the technical success rates ranged from 89 to 97 percent. Hypertension was cured in 33 to 63 percent of patients, improved in 24 to 57 percent, and failed to improve in 3 to 33 percent. A longer duration of hypertension, concomitant atherosclerotic disease, and complex branch-vessel repair all adversely affect the results of surgical revascularization.54,56
Although there is a paucity of prospective data demonstrating the superiority of percutaneous transluminal angioplasty over surgical revascularization, the percutaneous approach has emerged as the mainstay of treatment for patients with fibromuscular dysplasia who meet the criteria for intervention. Percutaneous transluminal angioplasty is less costly than surgical revascularization, is less invasive, can be performed on an outpatient basis, and is associated with lower morbidity; moreover, if it is unsuccessful, surgical therapy may still be used (Table 2).3,55,57,58,59,60,61,62,63,64,65,66,67,68 Important advances in the designs of guidewires, catheters, and balloons, as well as improvement in the relevant skills of clinicians, have made it possible to perform angioplasty for even the most complex renal-artery lesions, and it is equally effective in the main renal artery and in branch-artery stenoses.69 Although stents have been used extensively for the treatment of atherosclerotic renal-artery stenosis, the use of stents for fibromuscular dysplasia has been reserved as a "bailout" procedure in cases in which there are suboptimal results with balloon angioplasty or in which renal-artery dissection occurs.64,66 Adjunctive intravascular ultrasonography may be useful in determining whether an intervention has been technically successful.34 Complications of percutaneous intervention occur in up to 14 percent of patients and most commonly involve minor access-related problems. Rarely, renal-artery perforation, dissection, or segmental renal infarction occurs.57,59,60
Table 2. Results of Percutaneous Transluminal Angioplasty of the Renal Arteries in Patients with Fibromuscular Renovascular Disease and Hypertension.
Successful angioplasty often results in a substantial and rapid reduction of both the systolic and the diastolic blood pressure. Improved blood-pressure control correlates with a marked reduction in plasma renin activity and angiotensin II levels.67 Correlates of successful outcome include an age of less than 50 years, the absence of associated coronary or carotid stenoses, and a duration of hypertension of less than eight years.66 The rate of restenosis after balloon angioplasty has ranged from 7 to 27 percent over follow-up periods of six months to two years.61,63,70,71 In rare cases, fibrodysplastic stenosis may coexist with an aneurysm.72 This condition may be treated percutaneously with the use of a covered stent graft or may be repaired surgically.73
Patients who are treated with endovascular or surgical revascularization should undergo duplex ultrasonographic imaging periodically to detect progression of disease, restenosis, or loss of kidney volume.43,71,74 Imaging should be performed soon after revascularization to assess the adequacy of the intervention,46 again after 6 months and after 12 months, and yearly thereafter, or whenever there is a recurrence or worsening of hypertension.
Cerebrovascular Fibromuscular Dysplasia
Cerebrovascular fibromuscular dysplasia may be asymptomatic or associated with a variety of nonspecific symptoms, including headache, tinnitus, vertigo, lightheadedness, and syncope.8,75,76 The more specific neurologic syndromes of transient ischemic attack, amaurosis fugax, stroke, Horner's syndrome, and cranial-nerve palsies may be the first presentation of fibromuscular dysplasia involving the carotid or vertebral arteries8,76 (Figure 3). Cerebrovascular symptoms may be related to critical stenosis or occlusions of major arteries, rupture of an intracranial aneurysm, or cerebral embolism originating from intravascular thrombi in stenotic regions.77 Intracranial or extracranial cerebrovascular fibromuscular dysplasia may also be discovered incidentally as the cause of a cervical bruit or when angiography or some other imaging method is performed for unrelated reasons. The mean age of patients with cerebrovascular fibromuscular dysplasia is approximately 50 years. The natural history of cerebrovascular fibromuscular dysplasia of the medial type is generally benign.78,79,80
Several imaging methods may be used for the detection of intracranial or extracranial cerebrovascular fibromuscular dysplasia. Duplex ultrasonography of the carotid arteries may demonstrate irregular patterns of stenosis and aneurysm81 (Figure 1D), but color-coded duplex ultrasonography has a lower sensitivity than angiography for the detection of cerebrovascular fibromuscular dysplasia.81 Since fibromuscular dysplasia affects the middle and distal portions of the carotid and vertebral arteries at the level of the first and second cervical vertebrae,82 it may be difficult to visualize these lesions by means of duplex ultrasonography. There has been little experience with computed tomographic angiography (Figure 1C) or magnetic resonance angiography for the detection of cerebrovascular fibromuscular dysplasia; however, magnetic resonance angiography should be performed to rule out the presence of intracranial aneurysms in patients with such dysplasia.
Before the use of percutaneous revascularization became widespread, surgery was the mainstay of therapy for patients with symptomatic cerebrovascular fibromuscular dysplasia. The surgical technique used depended on the type of lesion and its location, but the most widely used procedure was graduated intraluminal dilatation.82,83,84,85 Other procedures that have been used include intraoperative balloon angioplasty,86 placement of a polytetrafluoroethylene-covered endograft,87 resection of the diseased segment and primary anastomosis (Figure 3C), grafting of autogenous saphenous vein, resection of the aneurysm, and carotid endarterectomy.82,88,89
During the past 10 years, percutaneous angioplasty has become the preferred treatment for symptomatic cerebrovascular fibromuscular dysplasia90,91,92,93,94,95,96,97 (Figure 3A and Figure 3B). There have been no randomized, controlled trials comparing surgery with balloon angioplasty in this condition. Studies in patients with atherosclerotic carotid artery disease suggest that the use of cerebral protection devices may reduce the frequency of ischemic neurologic events during stenting of the carotid artery.98,99,100 When these devices receive approval from the Food and Drug Administration, they will probably be used during percutaneous intervention for the treatment of fibromuscular dysplasia in the carotid artery.
Fibromuscular Dysplasia in Other Vascular Territories
Of the arteries that supply blood to the lower extremities, the iliac arteries are the most likely to be affected by fibromuscular dysplasia, although this condition has been described in the femoral, popliteal, and tibioperoneal arteries as well.9,101 Patients with fibromuscular dysplasia in the pelvic or leg arteries may present with intermittent claudication, critical limb ischemia, or peripheral microembolism that manifests as pain and cyanosis in the toes. In the arms, fibromuscular dysplasia is identified most frequently in the subclavian arteries but has also been described in the brachial and axillary arteries.5,6 In severe cases, patients have weakness, paresthesias, or claudication in their arms. For symptomatic fibromuscular dysplasia in the arms or legs, treatment consists of percutaneous balloon angioplasty.102,103
Fibromuscular dysplasia in the visceral arteries typically involves the celiac, superior mesenteric, inferior mesenteric, hepatic, and splenic arteries.2,104 Intestinal angina may occur when at least two of the major mesenteric arteries are obstructed. In unusual cases, the stenosis progresses to total occlusion, leading to acute intestinal ischemia.105,106 Treatment options include percutaneous intervention and surgical bypass.
As is the case with most rare diseases, it is difficult to conduct a prospective study of various treatment options. Therefore, most treatment decisions are based on data derived from retrospective case series and anecdotal reports. Thanks to advances in imaging methods and enhancement of the interventional armamentarium, treatment has become less invasive and is now at least as effective as previous surgical approaches while being associated with lower morbidity. Future studies will involve the use of protection devices at the time of percutaneous intervention in order to prevent distal embolization. There is no role for stent implantation as a primary treatment for fibromuscular dysplasia, since angioplasty alone is quite effective. Further study of the pathogenesis of fibromuscular dysplasia is needed so that we may gain a better understanding of this disease.
Dr. Slovut reports having received grant support from Volcano Therapeutics.
We are indebted to Jonathan L. Halperin, M.D., for his helpful suggestions and to Micheline Watt for assistance in the preparation of the manuscript.
Source Information
From the Zena and Michael A. Wiener Cardiovascular Institute, Mount Sinai School of Medicine, New York.
Address reprint requests to Dr. Olin at the Zena and Michael A. Wiener Cardiovascular Institute, Mount Sinai School of Medicine, 1 Gustave L. Levy Pl., Box 1033, New York, NY 10029-6574, or at jeffrey.olin@msnyuhealth.org.
References
Kojima A, Shindo S, Kubota K, et al. Successful surgical treatment of a patient with multiple visceral artery aneurysms due to fibromuscular dysplasia. Cardiovasc Surg 2002;10:157-160.
Insall RL, Chamberlain J, Loose HW. Fibromuscular dysplasia of visceral arteries. Eur J Vasc Surg 1992;6:668-672.
Luscher TF, Keller HM, Imhof HG, et al. Fibromuscular hyperplasia: extension of the disease and therapeutic outcome: results of the University Hospital Zurich Cooperative Study on Fibromuscular Hyperplasia. Nephron 1986;44:109-114.
Stanley JC, Gewertz BL, Bove EL, Sottiurai V, Fry WJ. Arterial fibrodysplasia: histopathologic character and current etiologic concepts. Arch Surg 1975;110:561-566.
Cutts S, Grewal RS, Downing R. Bilateral brachial artery fibromuscular dysplasia. Eur J Vasc Endovasc Surg 2000;19:667-668.
Suzuki H, Daida H, Sakurai H, Yamaguchi H. Familial fibromuscular dysplasia of bilateral brachial arteries. Heart 1999;82:251-252.
Radhi JM, McKay R, Tyrrell MJ. Fibromuscular dysplasia of the aorta presenting as multiple recurrent thoracic aneurysms. Int J Angiol 1998;7:215-8.
Mettinger KL. Fibromuscular dysplasia and the brain. II. Current concept of the disease. Stroke 1982;13:53-58.
van den Dungen JJ, Boontje AH, Oosterhuis JW. Femoropopliteal arterial fibrodysplasia. Br J Surg 1990;77:396-399.
Rybka SJ, Novick AC. Concomitant carotid, mesenteric and renal artery stenosis due to primary intimal fibroplasia. J Urol 1983;129:798-800.
Wessely Z, Guerry RL, Klavins JV. Disseminated fibromuscular hyperplasia of vascular channels. Arch Pathol 1973;96:179-182.
Rosenberger A, Adler O, Lichtig H. Angiographic appearance of the renal vein in a case of fibromuscular dysplasia of the artery. Radiology 1976;118:579-580.
Leadbetter WF, Burkland CE. Hypertension in unilateral renal disease. J Urol 1938;39:611-626.
McCormack LJ, Hazard JB, Poutasse EF. Obstructive lesions of the renal artery associated with remediable hypertension. Am J Pathol 1958;34:582-582. abstract.
Olin JW. Syndromes that mimic vasculitis. Curr Opin Cardiol 1991;6:768-774.
Harrison EG Jr, McCormack LJ. Pathologic classification of renal arterial disease in renovascular hypertension. Mayo Clin Proc 1971;46:161-167.
Begelman SM, Olin JW. Fibromuscular dysplasia. Curr Opin Rheumatol 2000;12:41-47.
McCormack LJ, Poutasse EF, Meaney TF, Noto TJ Jr, Dustan HP. A pathologic-arteriographic correlation of renal arterial disease. Am Heart J 1966;72:188-198.
Kincaid OW, Davis GD, Hallermann FJ, Hunt JC. Fibromuscular dysplasia of the renal arteries: arteriographic features, classification, and observations on natural history of the disease. Am J Roentgenol Radium Ther Nucl Med 1968;104:271-282.
Begelman SM, Olin JW. Nonatherosclerotic arterial disease of the extracranial cerebrovasculature. Semin Vasc Surg 2000;13:153-164.
Sang CN, Whelton PK, Hamper UM, et al. Etiologic factors in renovascular fibromuscular dysplasia: a case-control study. Hypertension 1989;14:472-479.
Pannier-Moreau I, Grimbert P, Fiquet-Kempf B, et al. Possible familial origin of multifocal renal artery fibromuscular dysplasia. J Hypertens 1997;15:1797-1801.
Grimbert P, Fiquet-Kempf B, Coudol P, et al. étude génétique de la dysplasie fibromusculaire des artères rénales. Arch Mal Coeur Vaiss 1998;91:1069-1071.
Bofinger A, Hawley C, Fisher P, Daunt N, Stowasser M, Gordon R. Polymorphisms of the renin-angiotensin system in patients with multifocal renal arterial fibromuscular dysplasia. J Hum Hypertens 2001;15:185-190.
Schievink WI, Limburg M. Angiographic abnormalities mimicking fibromuscular dysplasia in a patient with Ehlers-Danlos syndrome, type IV. Neurosurgery 1989;25:482-483.
Hudgins LB, Limbacher JP II. Fibromuscular dysplasia in Alport's syndrome. J Tenn Med Assoc 1982;75:733-735.
Qunibi WJ, Taylor TK, Knight TF, Senekjian HO, Gomez L, Weinman EJ. Pheochromocytoma and fibromuscular hyperplasia. South Med J 1979;72:1481-1482.
de Mendonca WC, Espat PA. Pheochromocytoma associated with arterial fibromuscular dysplasia. Am J Clin Pathol 1981;75:749-754.
Schievink WI, Bjornsson J, Piepgras DG. Coexistence of fibromuscular dysplasia and cystic medial necrosis in a patient with Marfan's syndrome and bilateral carotid artery dissections. Stroke 1994;25:2492-2496.
Janzen J, Vuong PN, Rothenberger-Janzen K. Takayasu's arteritis and fibromuscular dysplasia as causes of acquired atypical coarctation of the aorta: retrospective analysis of seven cases. Heart Vessels 1999;14:277-282.
D'Souza SJ, Tsai WS, Silver MM, et al. Diagnosis and management of stenotic aorto-arteriopathy in childhood. J Pediatr 1998;132:1016-1022.
Jaff MR, Olin JW, Young JR. Failure of acute phase reactants to predict disease activity in Takayasu's arteritis. J Vasc Med Biol 1993;4:223-7.
Flamm SD, White RD, Hoffman GS. The clinical application of `edema-weighted' magnetic resonance imaging in the assessment of Takayasu's arteritis. Int J Cardiol 1998;66:Suppl 1:S151-S161.
Gowda MS, Loeb AL, Crouse LJ, Kramer PH. Complementary roles of color-flow duplex imaging and intravascular ultrasound in the diagnosis of renal artery fibromuscular dysplasia: should renal arteriography serve as the "gold standard"? J Am Coll Cardiol 2003;41:1305-1311.
Stokes JB, Bonsib SM, McBride JW. Diffuse intimal fibromuscular dysplasia with multiorgan failure. Arch Intern Med 1996;156:2611-2614.
Safian RD, Textor SC. Renal-artery stenosis. N Engl J Med 2001;344:431-442.
Cragg AH, Smith TP, Thompson BH, et al. Incidental fibromuscular dysplasia in potential renal donors: long-term clinical follow-up. Radiology 1989;172:145-147.
Goncharenko V, Gerlock AJ Jr, Shaff MI, Hollifield JW. Progression of renal artery fibromuscular dysplasia in 42 patients as seen on angiography. Radiology 1981;139:45-51.
Meaney TF, Dustan HP, McCormack LJ. Natural history of renal artery disease. Radiology 1968;91:881-887.
Schreiber MJ, Pohl MA, Novick AC. The natural history of atherosclerotic and fibrous renal artery disease. Urol Clin North Am 1984;11:383-392.
Mounier-Vehier C, Lions C, Jaboureck O, et al. Parenchymal consequences of fibromuscular dysplasia renal artery stenosis. Am J Kidney Dis 2002;40:1138-1145.
Olin JW, Piedmonte M, Young JR, DeAnna S, Grubb M, Childs MB. Utility of duplex scanning of the renal arteries for diagnosing significant renal artery stenosis. Ann Intern Med 1995;122:833-838.
Carman TL, Olin JW, Czum J. Noninvasive imaging of renal arteries. Urol Clin North Am 2001;28:815-826.
Radermacher J, Chavan A, Bleck J, et al. Use of Doppler ultrasonography to predict the outcome of therapy for renal-artery stenosis. N Engl J Med 2001;344:410-417.
Napoli V, Pinto S, Bargellini I, et al. Duplex ultrasonographic study of the renal arteries before and after renal artery stenting. Eur Radiol 2002;12:796-803.
Edwards JM, Zaccardi MJ, Strandness DE Jr. A preliminary study of the role of duplex scanning in defining the adequacy of treatment of patients with renal artery fibromuscular dysplasia. J Vasc Surg 1992;15:604-611.
Rubin GD. MDCT imaging of the aorta and peripheral vessels. Eur J Radiol 2003;45:Suppl 1:S42-S49.
Funabashi N, Komiyama N, Komuro I. Fibromuscular dysplasia in renovascular hypertension demonstrated by multislice CT: comparison with conventional angiogram and intravascular ultrasound. Heart 2003;89:639-639.
Marcos HB, Choyke PL. Magnetic resonance angiography of the kidney. Semin Nephrol 2000;20:450-455.
Fommei E, Ghione S, Hilson AJ, et al. Captopril radionuclide test in renovascular hypertension: a European multicentre study. Eur J Nucl Med 1993;20:617-623.
van Jaarsveld BC, Krijnen P, Derkx FH, Oei HY, Postma CT, Schalekamp MA. The place of renal scintigraphy in the diagnosis of renal artery stenosis: fifteen years of clinical experience. Arch Intern Med 1997;157:1226-1234.
Chobanian AV, Bakris GL, Black HR, et al. The Seventh Report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure: the JNC 7 report. JAMA 2003;289:2560-2572.
Reiher L, Pfeiffer T, Sandmann W. Long-term results after surgical reconstruction for renal artery fibromuscular dysplasia. Eur J Vasc Endovasc Surg 2000;20:556-559.
Anderson CA, Hansen KJ, Benjamin ME, Keith DR, Craven TE, Dean RH. Renal artery fibromuscular dysplasia: results of current surgical therapy. J Vasc Surg 1995;22:207-216.
Hagg A, Aberg H, Eriksson I, Lorelius LE, Morlin C. Fibromuscular dysplasia of the renal artery -- management and outcome. Acta Chir Scand 1987;153:15-20.
Novick AC, Ziegelbaum M, Vidt DG, Gifford RW Jr, Pohl MA, Goormastic M. Trends in surgical revascularization for renal artery disease: ten years' experience. JAMA 1987;257:498-501.
Sos TA, Pickering TG, Sniderman K, et al. Percutaneous transluminal renal angioplasty in renovascular hypertension due to atheroma or fibromuscular dysplasia. N Engl J Med 1983;309:274-279.
Baert AL, Wilms G, Amery A, Vermylen J, Suy R. Percutaneous transluminal renal angioplasty: initial results and long-term follow-up in 202 patients. Cardiovasc Intervent Radiol 1990;13:22-28.
Tegtmeyer CJ, Selby JB, Hartwell GD, Ayers C, Tegtmeyer V. Results and complications of angioplasty in fibromuscular disease. Circulation 1991;83:Suppl I:I-155.
Bonelli FS, McKusick MA, Textor SC, et al. Renal artery angioplasty: technical results and clinical outcome in 320 patients. Mayo Clin Proc 1995;70:1041-1052.
Jensen G, Zachrisson BF, Delin K, Volkmann R, Aurell M. Treatment of renovascular hypertension: one year results of renal angioplasty. Kidney Int 1995;48:1936-1945.
Davidson RA, Barri Y, Wilcox CS. Predictors of cure of hypertension in fibromuscular renovascular disease. Am J Kidney Dis 1996;28:334-338.
Klow NE, Paulsen D, Vatne K, Rokstad B, Lien B, Fauchald P. Percutaneous transluminal renal artery angioplasty using the coaxial technique: ten years of experience from 591 procedures in 419 patients. Acta Radiol 1998;39:594-603.
Birrer M, Do DD, Mahler F, Triller J, Baumgartner I. Treatment of renal artery fibromuscular dysplasia with balloon angioplasty: a prospective follow-up study. Eur J Vasc Endovasc Surg 2002;23:146-152.
Surowiec SM, Sivamurthy N, Rhodes JM, et al. Percutaneous therapy for renal artery fibromuscular dysplasia. Ann Vasc Surg 2003;17:650-655.
de Fraissinette B, Garcier JM, Dieu V, et al. Percutaneous transluminal angioplasty of dysplastic stenoses of the renal artery: results on 70 adults. Cardiovasc Intervent Radiol 2003;26:46-51.
Airoldi F, Palatresi S, Marana I, et al. Angioplasty of atherosclerotic and fibromuscular renal artery stenosis: time course and predicting factors of the effects on renal function. Am J Hypertens 2000;13:1210-1217.
Archibald GR, Beckmann CF, Libertino JA. Focal renal artery stenosis caused by fibromuscular dysplasia: treatment by percutaneous transluminal angioplasty. AJR Am J Roentgenol 1988;151:593-596.
Cluzel P, Raynaud A, Beyssen B, Pagny JY, Gaux JC. Stenoses of renal branch arteries in fibromuscular dysplasia: results of percutaneous transluminal angioplasty. Radiology 1994;193:227-232.
Plouin PF, Darne B, Chatellier G, et al. Restenosis after a first percutaneous transluminal renal angioplasty. Hypertension 1993;21:89-96.
Baumgartner I, Triller J, Mahler F. Patency of percutaneous transluminal renal angioplasty: a prospective sonographic study. Kidney Int 1997;51:798-803.
Krumme B, Blum U. Renal artery aneurysm and fibromuscular dysplasia. Nephrol Dial Transplant 1997;12:1067-1069.
Bisschops RH, Popma JJ, Meyerovitz MF. Treatment of fibromuscular dysplasia and renal artery aneurysm with use of a stent-graft. J Vasc Interv Radiol 2001;12:757-760.
Olin JW. Atherosclerotic renal artery disease. Cardiol Clin 2002;20:547-562.
Van Damme H, Sakalihasan N, Limet R. Fibromuscular dysplasia of the internal carotid artery: personal experience with 13 cases and literature review. Acta Chir Belg 1999;99:163-168.
Mettinger KL, Ericson K. Fibromuscular dysplasia and the brain. I. Observations on angiographic, clinical and genetic characteristics. Stroke 1982;13:46-52.
Luscher TF, Lie JT, Stanson AW, Houser OW, Hollier LH, Sheps SG. Arterial fibromuscular dysplasia. Mayo Clin Proc 1987;62:931-952.
Stewart MT, Moritz MW, Smith RB III, Fulenwider JT, Perdue GD. The natural history of carotid fibromuscular dysplasia. J Vasc Surg 1986;3:305-310.
Wells RP, Smith RR. Fibromuscular dysplasia of the internal carotid artery: a long term follow-up. Neurosurgery 1982;10:39-43.
Wesen CA, Elliott BM. Fibromuscular dysplasia of the carotid arteries. Am J Surg 1986;151:448-451.
Arning C. Nonatherosclerotic disease of the cervical arteries: role of ultrasonography for diagnosis. Vasa 2001;30:160-167.
Effeney DJ, Krupski WC, Stoney RJ, Ehrenfeld WK. Fibromuscular dysplasia of the carotid artery. Aust N Z J Surg 1983;53:527-531.
Collins GJ Jr, Rich NM, Clagett GP, Spebar MJ, Salander JM. Fibromuscular dysplasia of the internal carotid arteries: clinical experience and follow-up. Ann Surg 1981;194:89-96.
Starr DS, Lawrie GM, Morris GC Jr. Fibromuscular disease of carotid arteries: long term results of graduated internal dilatation. Stroke 1981;12:196-199.
Chiche L, Bahnini A, Koskas F, Kieffer E. Occlusive fibromuscular disease of arteries supplying the brain: results of surgical treatment. Ann Vasc Surg 1997;11:496-504.
Smith LL, Smith DC, Killeen JD, Hasso AN. Operative balloon angioplasty in the treatment of internal carotid artery fibromuscular dysplasia. J Vasc Surg 1987;6:482-487.
Finsterer J, Strassegger J, Haymerle A, Hagmuller G. Bilateral stenting of symptomatic and asymptomatic internal carotid artery stenosis due to fibromuscular dysplasia. J Neurol Neurosurg Psychiatry 2000;69:683-686.
Moreau P, Albat B, Thevenet A. Fibromuscular dysplasia of the internal carotid artery: long-term surgical results. J Cardiovasc Surg (Torino) 1993;34:465-472.
Martin EC, Diamond NG, Casarella WJ. Percutaneous transluminal angioplasty in non-atherosclerotic disease. Radiology 1980;135:27-33.
Ballard JL, Guinn JE, Killeen JD, Smith DC. Open operative balloon angioplasty of the internal carotid artery: a technique in evolution. Ann Vasc Surg 1995;9:390-393.
Brown MM. Balloon angioplasty for cerebrovascular disease. Neurol Res 1992;14:Suppl:159-163.
Garrido E, Montoya J. Transluminal dilatation of internal carotid artery in fibromuscular dysplasia: a preliminary report. Surg Neurol 1981;16:469-471.
Belan A, Vesela M, Vanek I, Weiss K, Peregrin JH. Percutaneous transluminal angioplasty of fibromuscular dysplasia of the internal carotid artery. Cardiovasc Intervent Radiol 1982;5:79-81.
Wilms GE, Smits J, Baert AL, De Wolf L. Percutaneous transluminal angioplasty in fibromuscular dysplasia of the internal carotid artery: one year clinical and morphological follow-up. Cardiovasc Intervent Radiol 1985;8:20-23.
Dublin AB, Baltaxe HA, Cobb CA III. Percutaneous transluminal carotid angioplasty and detachable balloon embolization in fibromuscular dysplasia. AJNR Am J Neuroradiol 1984;5:646-648.
Welch EL, Lemkin JA, Geary JE. Gruntzig balloon dilation for fibromuscular dysplasia of the internal carotid arteries. N Y State J Med 1985;85:115-117.
Tsai FY, Matovich V, Hieshima G, et al. Percutaneous transluminal angioplasty of the carotid artery. AJNR Am J Neuroradiol 1986;7:349-358.
Al-Mubarak N, Roubin GS, Vitek JJ, Iyer SS, New G, Leon MB. Effect of the distal-balloon protection system on microembolization during carotid stenting. Circulation 2001;104:1999-2002.
Ohki T, Veith FJ, Grenell S, et al. Initial experience with cerebral protection devices to prevent embolization during carotid artery stenting. J Vasc Surg 2002;36:1175-1185.
Henry M, Henry I, Klonaris C, et al. Benefits of cerebral protection during carotid stenting with the PercuSurge GuardWire system: midterm results. J Endovasc Ther 2002;9:1-13.
Vertruyen M, Garcez JL. Fibromuscular dysplasia of the superficial femoral artery: an unusual localization. Acta Chir Belg 1993;93:249-251.
Yoshida T, Ohashi I, Suzuki S, Iwai T. Fibromuscular disease of the brachial artery with digital emboli treated effectively by transluminal angioplasty. Cardiovasc Intervent Radiol 1994;17:99-101.
Mandke JV, Sharma S, Phatak AM, Sanzgiri VP, Loya YS, Desai DM. Catheter atherectomy of intimal fibroplasia of the common iliac artery. Cathet Cardiovasc Diagn 1993;30:30-32.
Yamaguchi R, Yamaguchi A, Isogai M, Hori A, Kin Y. Fibromuscular dysplasia of the visceral arteries. Am J Gastroenterol 1996;91:1635-1638.
Hamed RM, Ghandour K. Abdominal angina and intestinal gangrene -- a catastrophic presentation of arterial fibromuscular dysplasia: case report and review of the literature. J Pediatr Surg 1997;32:1379-1380.
Horie T, Seino Y, Miyauchi Y, et al. Unusual petal-like fibromuscular dysplasia as a cause of acute abdomen and circulatory shock. Jpn Heart J 2002;43:301-305.(David P. Slovut, M.D., Ph)