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Occlusive Fibromuscular Disease of Arteries Supplying the Brain: Results of Surgical Treatment
Occlusive Fibromuscular Disease of Arteries Supplying the Brain: Results of Surgical Treatment Laurent Chiche, MD, Amine Bahnini, MD, Fabien Koskas, MD, and Edouard Kieffer, MD, Paris, France Occlusive fibromuscular disease (FMD) of arteries supplying the brain is a documented cause of neurologic complications. From September 1976 to December 1994, 70 patients underwent surgery for occlusive FMD involving arteries supplying the brain. Isolated dysplastic aneurysms and coilings or kinkings were not included in this series. Twenty-two patients had experienced previous nonlethal ischemic stroke, 25 patients had experienced transient ischemic attacks, and 32 patients had vertebrobasilar insufficiency with or without associated carotid symptoms. Lesions involved one (n = 36) or two (n = 29) internal carotid arteries, and one (n = 18) or two (n = 14) vertebral arteries. Twenty-seven patients had simultaneous involvement of both carotid and vertebral arteries. Ten patients had FMD at another site, four had intracranial aneurysm, and four had an aberrant right subclavian artery. Seventy-seven carotid procedures including 67 graduated intraluminal dilatations were performed and 18 vertebral arteries were revascularized. One patient (1.4%) died postoperatively from hemorrhagic stroke and two patients (2.8%) presented nonlethal stroke. Sixty-two patients were followed postoperatively from 2 to 184 months (mean 86.2 ± 54.4). Actuarial survival rates at 5 and 10 years were 96.4 ± 5.0% and 82.1 ± 14.9%, respectively. Actuarial primary patency rate at 5 and 10 years was 94.3 ± 5.5%. Actuarial probability of stroke-free survival rates at 5 and 10 years were 94.2 ± 5.6% and 88.6% ± 10.3%, respectively. We conclude that improvement of symptoms, prevention of stroke, and stable long-term results justify surgical treatment in symptomatic patients with FMD of arteries supplying the brain. (Ann Vasc Surg 1997;11:496-504.)
INTRODUCTION Fibromuscular disease (FMD) is a common feature on renal arteries but it is rarely responsible for occlusive disease of extracranial arteries supplying the brain.1 FMD of the internal carotid artery is observed in less than 2.5% of patients who undergo angiography for evaluation of cerebrovascular disFrom the Service de Chirurgie Vasculaire, Groupe Hospitalier Pitie´-Salpe´trie`re, Paris, France. Presented at the Annual Meeting of the Societe´ de Chirurgie Vasculaire de Langue Franc¸aise, Bruges, Belgium, June 1-3, 1995. Correspondence to: A. Bahnini, MD, Service de Chirurgie Vasculaire, Groupe Hospitalier Pitie´-Salpe´trie`re, 45-83 boulevard de l’hoˆpital, 75651 Paris Cedex 13, France. 496
ease.2 This condition is more common than fibrodysplastic lesions of the vertebral arteries.2 The pathogenesis of the disease is unclear but a strong female predominance suggests a relationship with hormonal factors.2 While the natural history and outcome of the disease is not well documented, it is generally agreed that FMD may lead to neurologic complications and surgical treatment is usually undertaken in symptomatic patients.3 In this report, we describe our series of 70 patients who underwent surgery for occlusive FMD of the carotid or vertebral artery during an 18-year period.
PATIENTS AND METHODS From September 1976 to December 1994, 70 patients with occlusive FMD involving extracranial ar-
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Table I. Clinical manifestations in 70 patients with FMD of arteries supplying the brain Clinical manifestations
n
%
Isolated carotid symptoms Isolated VBI symptoms Carotid and VBI symptoms Headache or bruit Total Carotid TIA Carotid stroke Vertebrobasilar TIA Vertebrobasilar stroke
32 20 12 6 70 25 19 29 3
45.5 28.5 17.0 9 100 36 27 41 4
FMD, fibromuscular dysplasia; VBI, vertebrobasilar insufficiency; TIA, transient ischemic attack.
teries supplying the brain underwent surgery at the Department of Vascular Surgery of Pitie´-Salpe´trie`re University Hospital. There were 62 women (89%) and eight men (11%) with a mean age of 61.0 ± 14.5 years (range: 7 to 82 years). A total of 78 procedures were performed on 89 dysplastic arteries. Previously reported isolated dysplastic aneurysms and cases of coiling or kinking4-6 were not included in this series. Sixty-four patients (91%) presented previous focal neurologic ischemic symptoms. Six patients had no neurologic symptoms but complained of headaches and bruits. Neurologic symptoms are listed in Table I. Of 44 patients with carotid symptoms, four had bilateral symptoms. Twelve patients had both carotid and vertebral symptoms either successively or concomitantly. Twenty-five patients had experienced one or more transient ischemic attacks (TIA) in carotid territory including 18 hemispheric and seven ocular (transient amaurosis) events. Nineteen patients had presented stroke due to carotid artery disease including 13 hemispheric and six ocular events. Thirty-two patients had vertebrobasilar insufficiency (VBI) with clinical manifestation including vertigo, diplopia, or balance or postural derangement. Of these 32 patients, three had presented a vertebrobasilar stroke. In all, 22 patients (31%) recovered from stroke usually with minimal sequelae. In nine of these patients, CTscan documented cerebral infarctions. Thirteen patients (19%) presented with angina. Four had a history of myocardial infarction and one presented a crescendo angina requiring coronary artery bypass of grafting. Thirty-one patients (44%) had hypertension (>160/95 mmHg) including six that did not respond to medical treatment. All patients underwent semi-selective or selective arteriography of the four vessels supplying the
brain as well as duplex ultrasonography. In most patients, assessment of the renal arteries was also performed. No complications were observed during work-up procedures. Only occlusive FMD that generated the ‘‘string of beads’’ pattern, tubular stenosis, or focal stenosis on arteriographic images were taken into account for this study (Fig. 1). FMD involved the internal carotid artery in 65 patients (93%), unilaterally in 36 patients and bilaterally in 29 patients. Of these 65 patients, five presented unilateral carotid artery occlusion. In 18 cases, FMD of the internal carotid artery was associated with significant lengthening of the vessel with formation of a coil or a kink distal to the stenosis. FMD involved the vertebral artery in 32 patients (46%), unilaterally in 18 cases and bilaterally in 14 cases. The lesion was associated with lengthening and kinking in 16 cases. Twenty-seven patients presented FMD of both the carotid and vertebral arteries (Table II). One patient also presented bilateral involvement of the external carotid arteries. Ten patients (14%) presented FMD at other sites. One patient presented FMD of both subclavian arteries. Nine patients (13%) presented FMD of the renal arteries including five bilaterally. All of these patients had hypertension including four that did not respond to medical treatment. Four patients (6%) presented FMD of the visceral arteries (celiac artery in two cases, superior mesenteric artery in two cases, and splenic artery in one case). Of two patients with FMD of the external iliac arteries, one had bilateral involvement. Eighteen patients (26%) presented one or more associated atherosclerotic lesions. The site of atherosclerosis was the internal carotid artery in 12 cases, the vertebral artery in five cases, and the subclavian artery in eight cases. Five patients presented an occlusion of the subclavian artery. One patient presented an aortic arch aneurysm and two patients presented bilateral iliofemoral occlusive lesions. Arteriography allowed diagnosis of intracranial artery aneurysm in four patients. The site of aneurysm was the intrapetrous internal carotid artery in two cases, a pericallosal artery in one case, and a middle cerebral artery in one case. Four patients presented an uncomplicated aberrant subclavian artery. Five patients had previously undergone vascular procedures. In three cases, previous treatment consisted of endarterectomy for atherosclerotic stenosis of the contralateral internal carotid artery. In one case, resection with vein graft reconstruction had been performed for dysplastic aneurysm of the contralateral internal carotid artery. The youngest patient in this series had undergone percutaneous transluminal angioplasty for revascularization of
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Fig. 1. Arteriography showing fibrodysplastic stenosis of the left internal carotid artery with the characteristic ‘‘string of beads’’ pattern. Fig. 2. Arteriography showing satisfactory anatomical result 103 months after graduated intraluminal dilatation of the carotid artery and carotid-to-vertebral artery vein bypass.
Table II. Distribution of occlusive FMD in 27 patients with carotid and vertebral involvement Fibrodysplastic lesions
n = 70
%
1 carotid 2 carotid 1 carotid 2 carotid Total
5 9 4 9 27
7 13 6 13 39
artery + 1 vertebral artery arteries + 1 vertebral artery artery + 2 vertebral arteries arteries + 2 vertebral arteries
both renal arteries and of the superior mesenteric artery. Seventy-eight procedures were performed on 95 arteries including 89 that were dysplastic. The internal carotid artery was involved in 77 cases with the lesion being located on the right in 38 cases and left in 39 cases. The vertebral artery was involved in 18 cases with the lesion being located on the right in eight cases and on the left in 10 cases. Of these 18 cases, six vertebral arteries were not dysplastic but were revascularized at the same time as the dysplastic carotid artery. The underlying lesion in these six cases was atherosclerotic stenosis in three patients, kinking in two patients, and an abnormal level of entry of the artery into the transverse foramen that resulted in position-induced extrinsic compression in one patient. Revascularization involved one (n = 39) or both (n = 13) carotid arteries in 52 patients, one isolated vertebral artery in six
patients, and both carotid and vertebral arteries in 12 patients (Table III). Of the 13 patients (19%) in whom bilateral carotid artery revascularization was performed, five underwent single-staged procedures. They had nine graduated intraluminal dilatations of the internal carotid artery and one ligature of a dilated stump proximal to fibrodysplastic occlusion of the internal carotid artery. Eight other patients underwent double-staged procedures on a 3-week to 4-month period. Graduated intraluminal dilatation of the internal carotid artery was performed in 15 cases, alone in nine cases, and in association with another procedure in six cases (endarterectomy in three cases, resection-anastomosis in two cases, and redundancy correction in one case). In one case, exposure of the intrapetrous internal carotid artery allowed management of distal FMD by placement of a vein graft from the carotid artery bifurcation. One patient in this group also underwent vein bypass between the common carotid artery and the distal ipsilateral vertebral artery. Fifty-seven patients (81%) underwent unilateral revascularization involving an internal carotid artery in 51 cases and a vertebral artery in 17 cases. Of the 51 carotid artery procedures, graduated intraluminal dilatation was performed in 43 cases, alone in 22 cases and in association with another procedure in 21 cases (endarterectomy in 10 cases, resection anastomosis in two, shortening plasty in four, patch-angioplasty in four, and embolectomy
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Table III. Distribution of operated arteries supplying the brain in 70 patients with fibromuscular disease Patients
Arteries
FMD
Arteries operated
n
%
n
%
n
%
Unilateral carotid artery Bilateral carotid arteries Isolated vertebral artery Carotid + vertebral arteries Total
39 13 6 12 70
56 18.5 8.5 17 100
39 26 6 24 95
41 27.5 6.5 25 100
39 26 6 18 89
44 29 7 20 100
in one). Five patients underwent bypass between the carotid bifurcation and the distal internal carotid artery at the level of the C1. In four of these cases a saphenous vein graft was used. In the remaining case a superficial femoral artery autograft was used, this artery being replaced by a saphenous vein graft. The distal approach was used via the preor retro-jugular territory with successive dissection of the 12th and 9th cranial nerves, division of the digastric muscle, the occipital artery, and the styloid muscles, and resection of styloid process in order to reach the internal carotid artery at the base of the skull. One patient underwent ligation of the carotid artery for an internal carotid artery aneurysm distal to fibrodysplastic stenosis. One patient had isolated endarterectomy for an atherosclerotic lesion associated with minimal FMD. One patient had resection anastomosis for a short accessible dysplastic lesion. In 17 patients, vertebral artery revascularization was performed: alone in 6 patients and in association with carotid reconstruction in 11 patients (Fig. 2). Eight vein bypasses to the distal segment of the vertebral artery were made from the common carotid artery in six cases, the internal carotid artery in one case, and the ipsilateral subclavian artery in one case. In nine cases, the first segment of the vertebral artery was transposed to the common carotid artery in five cases, the subclavian artery in one case. Distal vertebral artery was transposed to the internal carotid artery in three cases. Overall, 77 procedures were performed on the internal carotid artery including 67 graduated intraluminal dilatations (27 in association with another procedure), six bypasses, two ligatures, one endarterectomy, and one isolated resectionanastomosis. All but two of the dilatation procedures were done surgically using Bakes metallic dilators of increasing diameter from 2.5 to 5 mm. Two dilatations were performed surgically using a balloon angioplasty catheter. In one of these cases, adjuvant metallic dilatation was required. No cases of perforation were observed during any dilatation procedure in this series. Eighteen vertebral arteries
were revascularized by bypass in nine cases and transposition in nine cases. Four patients with poorly controlled hypertension underwent concomitant surgery for FMD of the renal artery. The procedure consisted of renal autotransplantation in one case, aortorenal bypass using a superficial femoral artery autograft in two cases, and left splenorenal artery anastomosis in one case. Of these four patients, two underwent treatment for FMD of the external iliac arteries either by metallic graduated intraluminal dilatation or by iliofemoral venous bypass. All procedures were performed under general anesthesia without shunting. Early anatomic control was performed by intraoperative arteriography or angioscopy, or by duplex ultrasonography and/ or arteriography before discharge from hospital.
RESULTS Early Results There was one early postoperative death (1.4%) due to ipsilateral hemispheric hemorrhagic stroke following carotid dilatation. This patient had undergone surgery on the contralateral internal carotid artery 4 months earlier. Two patients (2.8%) presented nonlethal stroke and six presented TIA (8.5%). Of the two nonlethal strokes, one was a sequelae hemispheric event that occurred after early thrombosis of a carotidovertebral bypass performed simultaneously with carotidocarotid bypass. This patient recovered with only minimal sequelae in the upper extremity. The other nonlethal stroke was a vertebrobasilar event that occurred following a postoperative arteriographic control. This patient recovered fully within a few days. Five of the six TIAs involved territories supplied by the carotid artery: four were hemispheric (including one transient aggravation of a pre-existing deficit), and one was ocular. The remaining TIA was a vertebrobasilar event that occurred after early occlusion of a transposed vertebral artery. Early occlusion after vertebral revascularization
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Fig. 3. Actuarial survival curve for 70 patients that underwent surgical revascularization for occlusive fibrodysplastic lesions of arteries supplying the brain. The 5% confidence interval is indicated between the two thin lines.
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Fig. 4. Actuarial stroke-free survival curve for 78 revascularization procedures performed for occlusive fibrodysplastic lesions of arteries supplying the brain. The 5% confidence interval is indicated between the two thin lines.
was observed in three cases and led to one nonlethal stroke, one TIA, and one asymptomatic occlusion. All three cases involved the distal vertebral artery (two vein bypasses and one transposition into the internal carotid artery). Unilateral hearing loss was observed in one patient in whom the intrapetrous approach to the carotid artery had been used. Deafness was associated with paralysis of the facial nerve which regressed within 3 months. Transient paresis of cranial nerves (VII, IX, and XII) or Horner syndrome were observed in three other patients after posterior infraparotid approach.
Late Results Sixty-two patients have a mean follow-up of 86.2 ± 54.4 months (range: 2 to 184 months). In this group, 58 patients (94%) have undergone late duplex ultrasonography and/or arteriography (Fig. 2). Seven patients died during follow-up. The cause of death was unknown in one case, cancer in three cases, acute ischemia of the lower extremity in one case, heart disease in one case, and stroke in one case. The cause of stroke was unclear since it occurred 7 months postoperatively despite satisfactory anatomic control findings a few months earlier. Actuarial survival rates at five and 10 years (including operative mortality) were 96.4 ± 5.0% and 82.1 ± 14.9%, respectively (Fig. 3). Five patients presented nonlethal neurologic events during follow-up: stroke in two cases, TIA in one case, and persistence of preoperative transient amaurosis in one case. The first stroke occurred in a
Fig. 5. Actuarial primary patency curve for 78 revascularization procedures performed for occlusive fibrodysplastic lesions of arteries supplying the brain. The 5% confidence interval is indicated between the two thin lines.
patient with poor physical status in whom FMD of the contralateral carotid artery could not be treated and led to occlusion at 19 months. The second stroke occurred at 27 months in a patient with cardiac arrhythmia due to atrial fibrillation. The arteries supplying the brain were normal in this patient. Actuarial probability of stroke-free survival at 5 and 10 years (including postoperative strokes) was 94.2 ± 5.6% and 88.6 ± 10.3%, respectively (Fig. 4). The two late postoperative ipsilateral TIAs occurred at 19 and 37 months and could not be attributed to a specific cause. Of 32 patients who presented VBI, 25 were cured or significantly improved. Symptoms recurred in three of these patients, including a patient with
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early thrombosis of the vertebral revascularization. In one patient VBI was unchanged. In the remaining six patients, including two patients that died, clinical outcome was not specified. Asymptomatic occlusion of a distal carotid-tovertebral artery bypass occurred in one patient during the 4th postoperative month. No other late changes were observed. Overall actuarial primary patency rates of reconstructed carotid and vertebral arteries at 5 and 10 years were 94.3 ± 5.5% (Fig. 5). Six patients underwent one or more surgical procedures during follow-up. None of these procedures involved an already-treated dysplastic artery. The procedure consisted of four endarterectomies for atherosclerotic stenosis of the contralateral carotid artery, two distal carotid-to-vertebral artery bypasses (one for atherosclerotic stenosis and the other for position-induced extrinsic compression), one renal autotransplantation with contralateral nephrectomy, one repair of an aortic arch aneurysm, and one aortobiiliac bypass. One patient required neurosurgical repair of a middle cerebral artery aneurysm in the 3rd postoperative month. One patient has developed FMD of a contralateral carotid artery at 103 months and is scheduled for surgery.
DISCUSSION This study describes late clinical and anatomic results in an 18-year series of 70 patients that underwent surgery of occlusive FMD of arteries supplying the brain. Since the graduated intraluminal dilatation technique was used in most patients, histologic data were usually not available and diagnosis of FMD was based mainly on the angiographic imaging showing the ‘‘string of beads’’ pattern (Fig. 1).7 This feature, considered pathognomonic of FMD, usually corresponds to medial dysplasia which accounts for 90% of obstructive fibrodysplastic lesions. Tubular stenosis and focal stenosis account for the remaining 10% of lesions.8 The exact incidence of FMD involving arteries supplying the brain is unclear. Although less common than renal arteries, involvement of extracranial arteries has been reported in 2.5% to 6.8% of patients undergoing carotid artery arteriography.9 Involvement of the internal carotid artery is more frequent than involvement of the vertebral artery.10 However this series, like previous studies in which all four vessels supplying the brain were routinely studied,11,12 shows a high proportion (46%) of vertebral lesions (Fig. 6) occurring alone or in association with carotid lesions. Our series also confirms the previously reported female predomi-
Fig. 6. Arteriography showing fibrodysplastic stenosis of a distal vertebral artery with characteristic redundant length.
nance13,14 and the younger age of patients with fibrodysplastic lesions as compared to those presenting atherosclerotic lesions.11,14 In this regard, it should be noted that Moreau et al.15 reported a series of 58 patients including 23 men in which there were nine fibrodysplastic dissections and seven aneurysms, thus suggesting a different distribution according to sex for these lesions. The youngest patient in this series (a 7-year-old male) presented multiple severe dysplastic lesions. This observation raises doubt on the hypothesis implicating mechanical and hormonal factors in the pathogenesis of FMD.8 One such hypothesis states that FMD may result from unusual stresses acting on a longer than normal segment of arterial wall with few branches and that has a poor medial blood supply from vasa vasorum.16 It has also been speculated that hormonal-dependent medial ischemic damage could lead to disruption of the internal elastic lamina.17 Recently severe alpha-1 antitrypsin deficiency has been implicated in the pathogenesis of FMD,18 thus providing an explanation for the
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occurrence of multiple arterial lesions, particularly in young patients. Ten patients in this series presented a total of 24 occlusive fibrodysplastic lesions at various sites, i.e., the renal, visceral, external iliac, and subclavian arteries. Since arterial hypertension is usually the only symptom associated with these lesions, diagnosis requires complete arteriography. Using this technique we discovered an aberrant subclavian artery (ASA) in four patients. To our knowledge the association between FMD and ASA is uncommon and none of the 33 patients who underwent surgery for ASA in our 1994 series19 presented this combination. However, it should be noted that, although FMD rarely involves the subclavian artery,11 Chambers et al. reported an isolated fibrodysplastic lesion involving an ASA.20 Patients with FMD must also be routinely screened for intracranial aneurysm, which is a common cause of severe symptoms or complications due to rupture.15,21 The incidence of the association between obstructive FMD and aneurysms ranges from 3% to 50% and may raise the indication for neurosurgery or interventional neuroradiology.10,22,23 Of the four patients that presented intracranial aneurysm in our series, neurosurgery was performed in only one case. The presence of intracranial arterial lesions must be taken into account in the interpretation of symptoms. It can be difficult to determine the role of FMD in neurologic symptoms. In many cases, lesions of arteries to the brain are asymptomatic and discovered only coincidentally during assessment of FMD in other sites, particularly the renal arteries.24,25 Diagnosis may be suggested by headaches, pulsatile tinnitus, and cervical bruit detected either upon auscultation or by the patient himself (six patients in our series). Nevertheless, 31% of our patients had stroke and others had TIA. The mechanism underlying neurologic events due to FMD remains unclear. 2 Possible explanations include emboli from fibrino-cruoric material contained between the fibrous diaphragms, relative hypoperfusion distal to the stenosis, neurologic manifestations of hypertension in patients that do not respond to medical treatment, or of occlusive or aneurysmal intracranial dysplastic lesions.16,17 While preventive treatment for thromboembolism is widely prescribed, there is no etiologic treatment for FMD.24 Despite the proposal of Effeney et al.3 no prospective multicenter study is presently available concerning the natural history of FMD of arteries supplying the brain. Little data has been published concerning the outcome of the FMD in unoperated patients13,14,26 and no anatomic and neurologic criteria have been proposed to
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stage the progression of FMD lesions. However, it seems reasonable to speculate that obstructive lesions are progressive. Two findings of the present series support this conclusion, i.e., the finding at 103 months after the operation of progression of a mild contralateral carotid artery lesion and the occurrence of a lethal stroke in a patient with a previously noted carotid lesion that could not be repaired due to the patient’s poor physical status. Thus, though sometimes considered benign,26 FMD can lead to complications ranging from TIA to lethal stroke. As recommended by Effeney et al.3 surgical repair seems justified in symptomatic patients with accessible lesions provided the surgical group has the necessary experience to insure durable operative repair and long-lasting benefits from repair with minimal risk. Surgical graduated intraluminal dilatation is the most widely used procedure for FMD lesions.9 It can be used to treat distal lesions with a low risk of embolism since back bleeding following removal of the dilatator allows to wash free possible intimal fragments or thrombi.1 Use of a surgical approach for dilatation allows association of carotid endarterectomy, angioplasty, and resection-anastomosis if necessary to shorten the artery. We have little experience with operative balloon dilatation as performed by Smith et al.27 The theoretical advantage of this method is the application of a radial force against the arterial wall rather than a longitudinal shear force, thereby making intimal damage less likely and thus lowering the risk of perforation. Regarding the risk of perforation and dissection, we recommend arteriographic control immediately after dilatation. Long-term angiographic findings generally demonstrate perfect remodeling of the artery even if findings immediately after dilatation show residual minor ragged defects (Fig. 7).1 The increasing use of endoluminal revascularization techniques has led some groups to propose percutaneous transluminal angioplasty (PTA) using a balloon catheter for FMD of the carotid artery.28-32 This technique has been widely used for FMD of the renal arteries and seems applicable to arteries supplying the brain depending on the skill of the operator. However, redundancy coils and kinks are high-risk factors for injury during placement of the guidewire and balloon catheter.27 In the present series, these abnormalities were present in 18 carotid arteries and 16 vertebral arteries and as a result PTA would not have been indicated. The risk for stroke due to embolism of fibrino-cruoric fragments contained in the fibrous diaphragms cannot be ruled out and intimal dissection is inevitable.33,34 Although most dissections are limited to the zone of
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Fig. 7. A Postoperative arteriography showing residual minor ragged defects in an internal carotid artery immediately after progressive dilatation associated with a transposition of the vertebral artery into the common carotid artery. B Arteriography of the same artery 1 month later showing complete remodeling of the internal carotid artery.
angioplasty, cases requiring surgical repair have been reported.30 The triple coaxial catheter with an occlusive balloon described by Theron et al.31 theoretically prevents migration and allows aspiration of intimal fragments. However, placement of this device is difficult and is at risk of hemodynamic complications due to occlusion.33 Because of insufficient follow-up and low number of reported cases, it is presently impossible to draw any conclusions regarding the efficiency of PTA for treatment of FMD of arteries supplying the brain. The rate of restenosis, which is estimated to be 15% per year after dilatation of atherosclerotic lesions of the carotid artery,32,33 has not been determined for FMD. Nor has the benefit of stenting in this location been documented. Conversely, PTA is useful for treatment of FMD of renal or visceral arteries as shown by the successful treatment of one patient in this series. In our opinion, occurrence of severe hypertension is an indication for single-stage revascularization of the renal and carotid arteries. The rationale for this approach is to prevent the risk of cerebral hypovascularization if only renal artery lesions are corrected and cerebral hypervascularization if only carotid artery lesions are repaired. However, in four patients presenting severe hypertension in this series, PTA of the renal arteries was not feasible for anatomical reasons and conventional surgery was performed. The simultaneous performance of these two procedures did not increase the incidence of complications. On the other hand, the combined repair of the distal vertebral artery with revascularization of a fibrodysplastic carotid artery was associated with an increase in postoperative anatomic
and neurologic complications. Because of the limited number of such patients, it is difficult to state whether this increased morbidity is related to the multiple involvement of arteries supplying the brain, or to the combination of these two cerebral revascularization procedures. Based upon this observation, we believe that patients may, in some occasions, benefit from surgical refrain or postponed treatment of vertebral artery lesions. This recommendation is supported by the fact that recurrence of occlusion in distal vertebral artery remains asymptomatic in 50% of cases. In conclusion, although the natural history of occlusive fibromuscular dysplasia of arteries supplying the brain remains poorly documented, there is strong evidence that, like atherosclerotic lesions, these lesions lead to potentially serious neurologic complications. Despite the absence of a randomized prospective study, the results of this series suggest that surgery improves neurologic symptoms, particularly in patients with VBI, and achieves shortand long-term prevention of stroke. In this series, operative morbidity and lasting anatomical results are in accordance with those reported in patients with atherosclerotic lesions. These results suggest that surgery should be performed in symptomatic patients with occlusive FMD of the arteries supplying the brain.
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2. Natuzzi ES, Stoney RJ. Fibromuscular disease of the carotid artery. In Ernst CB, Stanley JC, ed. Current Therapy in Vascular Surgery. St Louis: Mosby-Year Book, Inc., 1995, pp 114-118. 3. Effeney DJ, Ehrenfeld WK, Stoney RJ, Wylie EJ. Why operate on carotid fibromuscular dysplasia? Arch Surg 1980; 115:1261-1265. 4. Ruotolo C, Kieffer E. Ane´vrysmes disse´quants chroniques de la carotide interne: Place du traitement chirurgical. In Kieffer E, Bousser MG, eds. Indications et Re´sultats de la Chirurgie Carotidienne. Paris: AERCV, 1988, pp 253-258. 5. Koskas F, Bahnini A, Walden R, Kieffer E. Stenotic coiling and kinking of the internal carotid artery. Ann Vasc Surg 1993;7:530-540. 6. Koskas F, Kieffer E, Bahnini A. Boucles et plicatures des arte`res carotides et verte´brales: Indications de la chirurgie. J Mal Vasc 1994;19:51-54. 7. Osborn AG, Anderson RE. Angiographic spectrum of cervical and intracranial fibromuscular dysplasia. Stroke 1977;8: 617-626. 8. Mettinger KL. Fibromuscular dysplasia and the brain II. Current concept of the disease. Stroke 1982;13:53-58. 9. Ehrenfeld WK. Dysplasie fibro-musculaire de la carotide: Indications chirurgicales et re´sultats. In Kieffer E, Bousser MG, eds. Indications et Re´sultats de la Chirurgie Carotidienne. Paris: AERCV, 1988, pp 241-244. 10. Furie DM, Tien RD. Fibromuscular dysplasia of arteries of the head and neck. Imaging findings. AJR 1994;162:12051209. 11. Manelfe C, Clarisse J, Fredy D, Andre´ JM, Crouzet G. Fibromuscular dysplasia of the cervico-cephalic arteries: Report of 70 cases. J Neuroradiol 1974;1:149-231. 12. Vega Molina J, Chiras J, Poirier B, Bories J. Fibromuscular dysplasia of the vertebral artery (angiographic features). J Neuroradiol 1985;12:123-134. 13. Corrin LS, Sandok BA, Houser OW. Cerebral ischemic events in patients with carotid artery fibromuscular dysplasia. Arch Neurol 1981;38:616-618. 14. Wells RP, Smith RR. Fibromuscular dysplasia of the internal carotid artery: A long-term follow-up. Neurosurgery 1982; 10:39-43. 15. Moreau P, Albat B, Thevenet A. Fibromuscular dysplasia of the internal carotid artery: Long-term surgical results. J Cardiovasc Surg 1993;34:465-472. 16. Effeney DJ, Ehrenfeld WK, Stoney RJ, Wylie EJ. Fibromuscular dysplasia of the internal carotid artery. World J Surg 1979;3:179-186. 17. Stanley JC, Fry WJ, Seeger JF, Hoffman GL, Gabrielsen TO. Extracranial internal carotid and vertebral artery fibrodysplasia. Arch Surg 1974;109:215-522. 18. Schievink WI, Bjo¨rnsson J, Parisi JE, Prakash UBS. Arterial fibromuscular dysplasia associated with severe alpha 1-antitrypsin deficiency. Mayo Clin Proc 1994;69:1040-1043.
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19. Kieffer E, Bahnini A, Koskas F. Aberrant subclavian artery: Surgical treatment in thirty-three adult patients. J Vasc Surg 1994;19:100-111. 20. Chambers J, Neale M, Appleberg M. Fibromuscular hyperplasia in an aberrant subclavian artery and neurogenic thoracic outlet syndrome: An unusual combination. J Vasc Surg 1994;20:834-848. 21. George B, Zerah M, Mourier KL, Gelbert F, Reizine D. Ruptured intracranial aneurysms: The influence of sex and fibromuscular dysplasia upon prognosis. Acta Neurochir 1989;97:26-30. 22. George B, Mourier KL, Gelbert F, Reizine D, Raggueneau JL. Vascular abnormalities in the neck associated with intracranial aneurysms. Neurosurgery 1989;24:499-508. 23. Maiuri F, Gallicchio B, Gangemi M, Briganti F, Iaconetta G, Corriero G. Fibromuscular dysplasia of the carotid arteries: Clinical and radiological considerations. Clin Neurol Neurosurg 1988;90:57-60. 24. Bahnini A, Chiche L, Koskas F, Kieffer E. Dysplasie fibromusculaire des arte`res a` destine´e ce´re´brale. In: Kieffer E, Godeau P, eds. Maladies Arte´rielles Non Athe´roscle´reuses de l’Adulte. Paris: AERCV, 1994, pp 355-367. 25. Mettinger KL, Ericson K. Fibromuscular dysplasia and the brain: Observations on angiographic, clinical and genetic characteristics. Stroke 1982;13:46-52. 26. Stewart MT, Moritz MW, Smith RB, Fulenwider JT, Perdue GD. The natural history of carotid fibromuscular dysplasia. J Vasc Surg 1986;3:305-310. 27. 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. 28. Van Den Hoven RW, Mali WPTH, Theodorides T. Transluminal dilatation of internal carotid artery in fibromuscular dysplasia: A case history. Angiology 1988;39:272-275. 29. Florio F, D’Angelo V, Nardella M, Balzano S, Catapano G, Cammisa M. Fibromuscular dysplasia of the internal carotid artery: Percutaneous transluminal angioplasty. Radiol Med 1992;84:796-801. 30. Jooma R, Bradshaw JR, Griffith HB. Intimal dissection following percutaneous transluminal carotid angioplasty for fibromuscular dysplasia. Neuroradiology 1985;27:181-182. 31. The´ron J, Courtheoux P, Alachkar F, Maiza D. Techniques endovasculaires de revascularisation ce´re´brale. J Mal Vasc 1990;15:245-256. 32. Motarjeme A, Gordon GI. Percutaneous transluminal angioplasty of the brachiocephalic vessels: Guidelines for therapy. Int Angiol 1993;12:260-269. 33. Brown MM. Balloon angioplasty for cerebrovascular disease. Neurological Res 1992;14(Suppl):159-163. 34. Kachel R. Percutaneous transluminal angioplasty (PTA) of supra-aortic arteries especially of the carotid and vertebral artery: An alternative to vascular surgery? J Mal Vasc 1993; 18:254-257.
INTRODUCTION Fibromuscular disease (FMD) is a common feature on renal arteries but it is rarely responsible for occlusive disease of extracranial arteries supplying the brain.1 FMD of the internal carotid artery is observed in less than 2.5% of patients who undergo angiography for evaluation of cerebrovascular disFrom the Service de Chirurgie Vasculaire, Groupe Hospitalier Pitie´-Salpe´trie`re, Paris, France. Presented at the Annual Meeting of the Societe´ de Chirurgie Vasculaire de Langue Franc¸aise, Bruges, Belgium, June 1-3, 1995. Correspondence to: A. Bahnini, MD, Service de Chirurgie Vasculaire, Groupe Hospitalier Pitie´-Salpe´trie`re, 45-83 boulevard de l’hoˆpital, 75651 Paris Cedex 13, France. 496
ease.2 This condition is more common than fibrodysplastic lesions of the vertebral arteries.2 The pathogenesis of the disease is unclear but a strong female predominance suggests a relationship with hormonal factors.2 While the natural history and outcome of the disease is not well documented, it is generally agreed that FMD may lead to neurologic complications and surgical treatment is usually undertaken in symptomatic patients.3 In this report, we describe our series of 70 patients who underwent surgery for occlusive FMD of the carotid or vertebral artery during an 18-year period.
PATIENTS AND METHODS From September 1976 to December 1994, 70 patients with occlusive FMD involving extracranial ar-
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Table I. Clinical manifestations in 70 patients with FMD of arteries supplying the brain Clinical manifestations
n
%
Isolated carotid symptoms Isolated VBI symptoms Carotid and VBI symptoms Headache or bruit Total Carotid TIA Carotid stroke Vertebrobasilar TIA Vertebrobasilar stroke
32 20 12 6 70 25 19 29 3
45.5 28.5 17.0 9 100 36 27 41 4
FMD, fibromuscular dysplasia; VBI, vertebrobasilar insufficiency; TIA, transient ischemic attack.
teries supplying the brain underwent surgery at the Department of Vascular Surgery of Pitie´-Salpe´trie`re University Hospital. There were 62 women (89%) and eight men (11%) with a mean age of 61.0 ± 14.5 years (range: 7 to 82 years). A total of 78 procedures were performed on 89 dysplastic arteries. Previously reported isolated dysplastic aneurysms and cases of coiling or kinking4-6 were not included in this series. Sixty-four patients (91%) presented previous focal neurologic ischemic symptoms. Six patients had no neurologic symptoms but complained of headaches and bruits. Neurologic symptoms are listed in Table I. Of 44 patients with carotid symptoms, four had bilateral symptoms. Twelve patients had both carotid and vertebral symptoms either successively or concomitantly. Twenty-five patients had experienced one or more transient ischemic attacks (TIA) in carotid territory including 18 hemispheric and seven ocular (transient amaurosis) events. Nineteen patients had presented stroke due to carotid artery disease including 13 hemispheric and six ocular events. Thirty-two patients had vertebrobasilar insufficiency (VBI) with clinical manifestation including vertigo, diplopia, or balance or postural derangement. Of these 32 patients, three had presented a vertebrobasilar stroke. In all, 22 patients (31%) recovered from stroke usually with minimal sequelae. In nine of these patients, CTscan documented cerebral infarctions. Thirteen patients (19%) presented with angina. Four had a history of myocardial infarction and one presented a crescendo angina requiring coronary artery bypass of grafting. Thirty-one patients (44%) had hypertension (>160/95 mmHg) including six that did not respond to medical treatment. All patients underwent semi-selective or selective arteriography of the four vessels supplying the
brain as well as duplex ultrasonography. In most patients, assessment of the renal arteries was also performed. No complications were observed during work-up procedures. Only occlusive FMD that generated the ‘‘string of beads’’ pattern, tubular stenosis, or focal stenosis on arteriographic images were taken into account for this study (Fig. 1). FMD involved the internal carotid artery in 65 patients (93%), unilaterally in 36 patients and bilaterally in 29 patients. Of these 65 patients, five presented unilateral carotid artery occlusion. In 18 cases, FMD of the internal carotid artery was associated with significant lengthening of the vessel with formation of a coil or a kink distal to the stenosis. FMD involved the vertebral artery in 32 patients (46%), unilaterally in 18 cases and bilaterally in 14 cases. The lesion was associated with lengthening and kinking in 16 cases. Twenty-seven patients presented FMD of both the carotid and vertebral arteries (Table II). One patient also presented bilateral involvement of the external carotid arteries. Ten patients (14%) presented FMD at other sites. One patient presented FMD of both subclavian arteries. Nine patients (13%) presented FMD of the renal arteries including five bilaterally. All of these patients had hypertension including four that did not respond to medical treatment. Four patients (6%) presented FMD of the visceral arteries (celiac artery in two cases, superior mesenteric artery in two cases, and splenic artery in one case). Of two patients with FMD of the external iliac arteries, one had bilateral involvement. Eighteen patients (26%) presented one or more associated atherosclerotic lesions. The site of atherosclerosis was the internal carotid artery in 12 cases, the vertebral artery in five cases, and the subclavian artery in eight cases. Five patients presented an occlusion of the subclavian artery. One patient presented an aortic arch aneurysm and two patients presented bilateral iliofemoral occlusive lesions. Arteriography allowed diagnosis of intracranial artery aneurysm in four patients. The site of aneurysm was the intrapetrous internal carotid artery in two cases, a pericallosal artery in one case, and a middle cerebral artery in one case. Four patients presented an uncomplicated aberrant subclavian artery. Five patients had previously undergone vascular procedures. In three cases, previous treatment consisted of endarterectomy for atherosclerotic stenosis of the contralateral internal carotid artery. In one case, resection with vein graft reconstruction had been performed for dysplastic aneurysm of the contralateral internal carotid artery. The youngest patient in this series had undergone percutaneous transluminal angioplasty for revascularization of
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Fig. 1. Arteriography showing fibrodysplastic stenosis of the left internal carotid artery with the characteristic ‘‘string of beads’’ pattern. Fig. 2. Arteriography showing satisfactory anatomical result 103 months after graduated intraluminal dilatation of the carotid artery and carotid-to-vertebral artery vein bypass.
Table II. Distribution of occlusive FMD in 27 patients with carotid and vertebral involvement Fibrodysplastic lesions
n = 70
%
1 carotid 2 carotid 1 carotid 2 carotid Total
5 9 4 9 27
7 13 6 13 39
artery + 1 vertebral artery arteries + 1 vertebral artery artery + 2 vertebral arteries arteries + 2 vertebral arteries
both renal arteries and of the superior mesenteric artery. Seventy-eight procedures were performed on 95 arteries including 89 that were dysplastic. The internal carotid artery was involved in 77 cases with the lesion being located on the right in 38 cases and left in 39 cases. The vertebral artery was involved in 18 cases with the lesion being located on the right in eight cases and on the left in 10 cases. Of these 18 cases, six vertebral arteries were not dysplastic but were revascularized at the same time as the dysplastic carotid artery. The underlying lesion in these six cases was atherosclerotic stenosis in three patients, kinking in two patients, and an abnormal level of entry of the artery into the transverse foramen that resulted in position-induced extrinsic compression in one patient. Revascularization involved one (n = 39) or both (n = 13) carotid arteries in 52 patients, one isolated vertebral artery in six
patients, and both carotid and vertebral arteries in 12 patients (Table III). Of the 13 patients (19%) in whom bilateral carotid artery revascularization was performed, five underwent single-staged procedures. They had nine graduated intraluminal dilatations of the internal carotid artery and one ligature of a dilated stump proximal to fibrodysplastic occlusion of the internal carotid artery. Eight other patients underwent double-staged procedures on a 3-week to 4-month period. Graduated intraluminal dilatation of the internal carotid artery was performed in 15 cases, alone in nine cases, and in association with another procedure in six cases (endarterectomy in three cases, resection-anastomosis in two cases, and redundancy correction in one case). In one case, exposure of the intrapetrous internal carotid artery allowed management of distal FMD by placement of a vein graft from the carotid artery bifurcation. One patient in this group also underwent vein bypass between the common carotid artery and the distal ipsilateral vertebral artery. Fifty-seven patients (81%) underwent unilateral revascularization involving an internal carotid artery in 51 cases and a vertebral artery in 17 cases. Of the 51 carotid artery procedures, graduated intraluminal dilatation was performed in 43 cases, alone in 22 cases and in association with another procedure in 21 cases (endarterectomy in 10 cases, resection anastomosis in two, shortening plasty in four, patch-angioplasty in four, and embolectomy
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Table III. Distribution of operated arteries supplying the brain in 70 patients with fibromuscular disease Patients
Arteries
FMD
Arteries operated
n
%
n
%
n
%
Unilateral carotid artery Bilateral carotid arteries Isolated vertebral artery Carotid + vertebral arteries Total
39 13 6 12 70
56 18.5 8.5 17 100
39 26 6 24 95
41 27.5 6.5 25 100
39 26 6 18 89
44 29 7 20 100
in one). Five patients underwent bypass between the carotid bifurcation and the distal internal carotid artery at the level of the C1. In four of these cases a saphenous vein graft was used. In the remaining case a superficial femoral artery autograft was used, this artery being replaced by a saphenous vein graft. The distal approach was used via the preor retro-jugular territory with successive dissection of the 12th and 9th cranial nerves, division of the digastric muscle, the occipital artery, and the styloid muscles, and resection of styloid process in order to reach the internal carotid artery at the base of the skull. One patient underwent ligation of the carotid artery for an internal carotid artery aneurysm distal to fibrodysplastic stenosis. One patient had isolated endarterectomy for an atherosclerotic lesion associated with minimal FMD. One patient had resection anastomosis for a short accessible dysplastic lesion. In 17 patients, vertebral artery revascularization was performed: alone in 6 patients and in association with carotid reconstruction in 11 patients (Fig. 2). Eight vein bypasses to the distal segment of the vertebral artery were made from the common carotid artery in six cases, the internal carotid artery in one case, and the ipsilateral subclavian artery in one case. In nine cases, the first segment of the vertebral artery was transposed to the common carotid artery in five cases, the subclavian artery in one case. Distal vertebral artery was transposed to the internal carotid artery in three cases. Overall, 77 procedures were performed on the internal carotid artery including 67 graduated intraluminal dilatations (27 in association with another procedure), six bypasses, two ligatures, one endarterectomy, and one isolated resectionanastomosis. All but two of the dilatation procedures were done surgically using Bakes metallic dilators of increasing diameter from 2.5 to 5 mm. Two dilatations were performed surgically using a balloon angioplasty catheter. In one of these cases, adjuvant metallic dilatation was required. No cases of perforation were observed during any dilatation procedure in this series. Eighteen vertebral arteries
were revascularized by bypass in nine cases and transposition in nine cases. Four patients with poorly controlled hypertension underwent concomitant surgery for FMD of the renal artery. The procedure consisted of renal autotransplantation in one case, aortorenal bypass using a superficial femoral artery autograft in two cases, and left splenorenal artery anastomosis in one case. Of these four patients, two underwent treatment for FMD of the external iliac arteries either by metallic graduated intraluminal dilatation or by iliofemoral venous bypass. All procedures were performed under general anesthesia without shunting. Early anatomic control was performed by intraoperative arteriography or angioscopy, or by duplex ultrasonography and/ or arteriography before discharge from hospital.
RESULTS Early Results There was one early postoperative death (1.4%) due to ipsilateral hemispheric hemorrhagic stroke following carotid dilatation. This patient had undergone surgery on the contralateral internal carotid artery 4 months earlier. Two patients (2.8%) presented nonlethal stroke and six presented TIA (8.5%). Of the two nonlethal strokes, one was a sequelae hemispheric event that occurred after early thrombosis of a carotidovertebral bypass performed simultaneously with carotidocarotid bypass. This patient recovered with only minimal sequelae in the upper extremity. The other nonlethal stroke was a vertebrobasilar event that occurred following a postoperative arteriographic control. This patient recovered fully within a few days. Five of the six TIAs involved territories supplied by the carotid artery: four were hemispheric (including one transient aggravation of a pre-existing deficit), and one was ocular. The remaining TIA was a vertebrobasilar event that occurred after early occlusion of a transposed vertebral artery. Early occlusion after vertebral revascularization
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Fig. 3. Actuarial survival curve for 70 patients that underwent surgical revascularization for occlusive fibrodysplastic lesions of arteries supplying the brain. The 5% confidence interval is indicated between the two thin lines.
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Fig. 4. Actuarial stroke-free survival curve for 78 revascularization procedures performed for occlusive fibrodysplastic lesions of arteries supplying the brain. The 5% confidence interval is indicated between the two thin lines.
was observed in three cases and led to one nonlethal stroke, one TIA, and one asymptomatic occlusion. All three cases involved the distal vertebral artery (two vein bypasses and one transposition into the internal carotid artery). Unilateral hearing loss was observed in one patient in whom the intrapetrous approach to the carotid artery had been used. Deafness was associated with paralysis of the facial nerve which regressed within 3 months. Transient paresis of cranial nerves (VII, IX, and XII) or Horner syndrome were observed in three other patients after posterior infraparotid approach.
Late Results Sixty-two patients have a mean follow-up of 86.2 ± 54.4 months (range: 2 to 184 months). In this group, 58 patients (94%) have undergone late duplex ultrasonography and/or arteriography (Fig. 2). Seven patients died during follow-up. The cause of death was unknown in one case, cancer in three cases, acute ischemia of the lower extremity in one case, heart disease in one case, and stroke in one case. The cause of stroke was unclear since it occurred 7 months postoperatively despite satisfactory anatomic control findings a few months earlier. Actuarial survival rates at five and 10 years (including operative mortality) were 96.4 ± 5.0% and 82.1 ± 14.9%, respectively (Fig. 3). Five patients presented nonlethal neurologic events during follow-up: stroke in two cases, TIA in one case, and persistence of preoperative transient amaurosis in one case. The first stroke occurred in a
Fig. 5. Actuarial primary patency curve for 78 revascularization procedures performed for occlusive fibrodysplastic lesions of arteries supplying the brain. The 5% confidence interval is indicated between the two thin lines.
patient with poor physical status in whom FMD of the contralateral carotid artery could not be treated and led to occlusion at 19 months. The second stroke occurred at 27 months in a patient with cardiac arrhythmia due to atrial fibrillation. The arteries supplying the brain were normal in this patient. Actuarial probability of stroke-free survival at 5 and 10 years (including postoperative strokes) was 94.2 ± 5.6% and 88.6 ± 10.3%, respectively (Fig. 4). The two late postoperative ipsilateral TIAs occurred at 19 and 37 months and could not be attributed to a specific cause. Of 32 patients who presented VBI, 25 were cured or significantly improved. Symptoms recurred in three of these patients, including a patient with
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early thrombosis of the vertebral revascularization. In one patient VBI was unchanged. In the remaining six patients, including two patients that died, clinical outcome was not specified. Asymptomatic occlusion of a distal carotid-tovertebral artery bypass occurred in one patient during the 4th postoperative month. No other late changes were observed. Overall actuarial primary patency rates of reconstructed carotid and vertebral arteries at 5 and 10 years were 94.3 ± 5.5% (Fig. 5). Six patients underwent one or more surgical procedures during follow-up. None of these procedures involved an already-treated dysplastic artery. The procedure consisted of four endarterectomies for atherosclerotic stenosis of the contralateral carotid artery, two distal carotid-to-vertebral artery bypasses (one for atherosclerotic stenosis and the other for position-induced extrinsic compression), one renal autotransplantation with contralateral nephrectomy, one repair of an aortic arch aneurysm, and one aortobiiliac bypass. One patient required neurosurgical repair of a middle cerebral artery aneurysm in the 3rd postoperative month. One patient has developed FMD of a contralateral carotid artery at 103 months and is scheduled for surgery.
DISCUSSION This study describes late clinical and anatomic results in an 18-year series of 70 patients that underwent surgery of occlusive FMD of arteries supplying the brain. Since the graduated intraluminal dilatation technique was used in most patients, histologic data were usually not available and diagnosis of FMD was based mainly on the angiographic imaging showing the ‘‘string of beads’’ pattern (Fig. 1).7 This feature, considered pathognomonic of FMD, usually corresponds to medial dysplasia which accounts for 90% of obstructive fibrodysplastic lesions. Tubular stenosis and focal stenosis account for the remaining 10% of lesions.8 The exact incidence of FMD involving arteries supplying the brain is unclear. Although less common than renal arteries, involvement of extracranial arteries has been reported in 2.5% to 6.8% of patients undergoing carotid artery arteriography.9 Involvement of the internal carotid artery is more frequent than involvement of the vertebral artery.10 However this series, like previous studies in which all four vessels supplying the brain were routinely studied,11,12 shows a high proportion (46%) of vertebral lesions (Fig. 6) occurring alone or in association with carotid lesions. Our series also confirms the previously reported female predomi-
Fig. 6. Arteriography showing fibrodysplastic stenosis of a distal vertebral artery with characteristic redundant length.
nance13,14 and the younger age of patients with fibrodysplastic lesions as compared to those presenting atherosclerotic lesions.11,14 In this regard, it should be noted that Moreau et al.15 reported a series of 58 patients including 23 men in which there were nine fibrodysplastic dissections and seven aneurysms, thus suggesting a different distribution according to sex for these lesions. The youngest patient in this series (a 7-year-old male) presented multiple severe dysplastic lesions. This observation raises doubt on the hypothesis implicating mechanical and hormonal factors in the pathogenesis of FMD.8 One such hypothesis states that FMD may result from unusual stresses acting on a longer than normal segment of arterial wall with few branches and that has a poor medial blood supply from vasa vasorum.16 It has also been speculated that hormonal-dependent medial ischemic damage could lead to disruption of the internal elastic lamina.17 Recently severe alpha-1 antitrypsin deficiency has been implicated in the pathogenesis of FMD,18 thus providing an explanation for the
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occurrence of multiple arterial lesions, particularly in young patients. Ten patients in this series presented a total of 24 occlusive fibrodysplastic lesions at various sites, i.e., the renal, visceral, external iliac, and subclavian arteries. Since arterial hypertension is usually the only symptom associated with these lesions, diagnosis requires complete arteriography. Using this technique we discovered an aberrant subclavian artery (ASA) in four patients. To our knowledge the association between FMD and ASA is uncommon and none of the 33 patients who underwent surgery for ASA in our 1994 series19 presented this combination. However, it should be noted that, although FMD rarely involves the subclavian artery,11 Chambers et al. reported an isolated fibrodysplastic lesion involving an ASA.20 Patients with FMD must also be routinely screened for intracranial aneurysm, which is a common cause of severe symptoms or complications due to rupture.15,21 The incidence of the association between obstructive FMD and aneurysms ranges from 3% to 50% and may raise the indication for neurosurgery or interventional neuroradiology.10,22,23 Of the four patients that presented intracranial aneurysm in our series, neurosurgery was performed in only one case. The presence of intracranial arterial lesions must be taken into account in the interpretation of symptoms. It can be difficult to determine the role of FMD in neurologic symptoms. In many cases, lesions of arteries to the brain are asymptomatic and discovered only coincidentally during assessment of FMD in other sites, particularly the renal arteries.24,25 Diagnosis may be suggested by headaches, pulsatile tinnitus, and cervical bruit detected either upon auscultation or by the patient himself (six patients in our series). Nevertheless, 31% of our patients had stroke and others had TIA. The mechanism underlying neurologic events due to FMD remains unclear. 2 Possible explanations include emboli from fibrino-cruoric material contained between the fibrous diaphragms, relative hypoperfusion distal to the stenosis, neurologic manifestations of hypertension in patients that do not respond to medical treatment, or of occlusive or aneurysmal intracranial dysplastic lesions.16,17 While preventive treatment for thromboembolism is widely prescribed, there is no etiologic treatment for FMD.24 Despite the proposal of Effeney et al.3 no prospective multicenter study is presently available concerning the natural history of FMD of arteries supplying the brain. Little data has been published concerning the outcome of the FMD in unoperated patients13,14,26 and no anatomic and neurologic criteria have been proposed to
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stage the progression of FMD lesions. However, it seems reasonable to speculate that obstructive lesions are progressive. Two findings of the present series support this conclusion, i.e., the finding at 103 months after the operation of progression of a mild contralateral carotid artery lesion and the occurrence of a lethal stroke in a patient with a previously noted carotid lesion that could not be repaired due to the patient’s poor physical status. Thus, though sometimes considered benign,26 FMD can lead to complications ranging from TIA to lethal stroke. As recommended by Effeney et al.3 surgical repair seems justified in symptomatic patients with accessible lesions provided the surgical group has the necessary experience to insure durable operative repair and long-lasting benefits from repair with minimal risk. Surgical graduated intraluminal dilatation is the most widely used procedure for FMD lesions.9 It can be used to treat distal lesions with a low risk of embolism since back bleeding following removal of the dilatator allows to wash free possible intimal fragments or thrombi.1 Use of a surgical approach for dilatation allows association of carotid endarterectomy, angioplasty, and resection-anastomosis if necessary to shorten the artery. We have little experience with operative balloon dilatation as performed by Smith et al.27 The theoretical advantage of this method is the application of a radial force against the arterial wall rather than a longitudinal shear force, thereby making intimal damage less likely and thus lowering the risk of perforation. Regarding the risk of perforation and dissection, we recommend arteriographic control immediately after dilatation. Long-term angiographic findings generally demonstrate perfect remodeling of the artery even if findings immediately after dilatation show residual minor ragged defects (Fig. 7).1 The increasing use of endoluminal revascularization techniques has led some groups to propose percutaneous transluminal angioplasty (PTA) using a balloon catheter for FMD of the carotid artery.28-32 This technique has been widely used for FMD of the renal arteries and seems applicable to arteries supplying the brain depending on the skill of the operator. However, redundancy coils and kinks are high-risk factors for injury during placement of the guidewire and balloon catheter.27 In the present series, these abnormalities were present in 18 carotid arteries and 16 vertebral arteries and as a result PTA would not have been indicated. The risk for stroke due to embolism of fibrino-cruoric fragments contained in the fibrous diaphragms cannot be ruled out and intimal dissection is inevitable.33,34 Although most dissections are limited to the zone of
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Fig. 7. A Postoperative arteriography showing residual minor ragged defects in an internal carotid artery immediately after progressive dilatation associated with a transposition of the vertebral artery into the common carotid artery. B Arteriography of the same artery 1 month later showing complete remodeling of the internal carotid artery.
angioplasty, cases requiring surgical repair have been reported.30 The triple coaxial catheter with an occlusive balloon described by Theron et al.31 theoretically prevents migration and allows aspiration of intimal fragments. However, placement of this device is difficult and is at risk of hemodynamic complications due to occlusion.33 Because of insufficient follow-up and low number of reported cases, it is presently impossible to draw any conclusions regarding the efficiency of PTA for treatment of FMD of arteries supplying the brain. The rate of restenosis, which is estimated to be 15% per year after dilatation of atherosclerotic lesions of the carotid artery,32,33 has not been determined for FMD. Nor has the benefit of stenting in this location been documented. Conversely, PTA is useful for treatment of FMD of renal or visceral arteries as shown by the successful treatment of one patient in this series. In our opinion, occurrence of severe hypertension is an indication for single-stage revascularization of the renal and carotid arteries. The rationale for this approach is to prevent the risk of cerebral hypovascularization if only renal artery lesions are corrected and cerebral hypervascularization if only carotid artery lesions are repaired. However, in four patients presenting severe hypertension in this series, PTA of the renal arteries was not feasible for anatomical reasons and conventional surgery was performed. The simultaneous performance of these two procedures did not increase the incidence of complications. On the other hand, the combined repair of the distal vertebral artery with revascularization of a fibrodysplastic carotid artery was associated with an increase in postoperative anatomic
and neurologic complications. Because of the limited number of such patients, it is difficult to state whether this increased morbidity is related to the multiple involvement of arteries supplying the brain, or to the combination of these two cerebral revascularization procedures. Based upon this observation, we believe that patients may, in some occasions, benefit from surgical refrain or postponed treatment of vertebral artery lesions. This recommendation is supported by the fact that recurrence of occlusion in distal vertebral artery remains asymptomatic in 50% of cases. In conclusion, although the natural history of occlusive fibromuscular dysplasia of arteries supplying the brain remains poorly documented, there is strong evidence that, like atherosclerotic lesions, these lesions lead to potentially serious neurologic complications. Despite the absence of a randomized prospective study, the results of this series suggest that surgery improves neurologic symptoms, particularly in patients with VBI, and achieves shortand long-term prevention of stroke. In this series, operative morbidity and lasting anatomical results are in accordance with those reported in patients with atherosclerotic lesions. These results suggest that surgery should be performed in symptomatic patients with occlusive FMD of the arteries supplying the brain.
REFERENCES 1. Ehrenfeld WK, Wylie EJ. Fibromuscular dysplasia of the internal carotid artery: Surgical management. Arch Surg 1974; 109:676-681.
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