From the Society for Clinical Vascular Surgery
Surgical and medical management of extracranial carotid artery aneurysms Grant T. Fankhauser, MD,a William M. Stone, MD,a Richard J. Fowl, MD,a Mark E. O’Donnell, MD,a Thomas C. Bower, MD,b Fredric B. Meyer, MD,b and Samuel R. Money, MD, MBA,a Phoenix, Ariz; and Rochester, Minn Objective: Extracranial carotid artery aneurysms (ECCAs) are extremely rare with limited information about management options. Our purpose was to review our institution’s experience with ECCAs during 15 years and to discuss the presentation and treatment of these aneurysms. Methods: A retrospective review of patients diagnosed with ECCAs from 1998 to 2012 was performed. Symptoms, risk factors, etiology, diagnostic methods, treatments, and outcomes were reviewed. Results: During the study period, 141 aneurysms were diagnosed in 132 patients (mean age, 61 years; 69 men). There were 116 (82%) pseudoaneurysms and 25 (18%) true aneurysms; 69 (49%) aneurysms were asymptomatic, whereas 72 (52%) had symptoms (28 painless masses; 10 transient ischemic attacks; 10 vision symptoms; 9 ruptures; 8 strokes; 4 painful mass; 1 dysphagia; 1 tongue weakness; 1 bruit). Causes of true aneurysms included fibromuscular dysplasia in 15 patients, Ehlers-Danlos syndrome in three, Marfan syndrome in one, and uncharacterized connective tissue diseases in two. Of 25 true aneurysms, 11 (44%) were symptomatic; 15 (60%) true aneurysms underwent open surgical treatment, whereas 10 (40%) were managed nonoperatively. Postoperative complications included one stroke during a mean followup of 31 months (range, 0-166 months). No aneurysms managed nonoperatively required intervention during a mean follow-up of 77 months (range, 1-115 months). Of 116 pseudoaneurysms, 60 (52%) were symptomatic; 33 (29%) pseudoaneurysms underwent open surgery, 18 (15%) underwent endovascular intervention, and 65 (56%) were managed medically. Pseudoaneurysm after endarterectomy (28 patients; 24%) presented at a mean of 82 months from the surgical procedure. Mean follow-up for all aneurysms was 33.9 months. One (0.7%) aneurysm-related death occurred (rupture treated palliatively). No patient undergoing nonoperative management suffered death or major morbidity related to the aneurysm. Nonoperative management was more common in asymptomatic patients (71%) than in symptomatic patients (31%). Conclusions: ECCAs are uncommon and may be manifested with varying symptoms. All segments of the carotid artery are susceptible, although the internal is most commonly affected. Open surgical intervention was more common in patients with symptoms and with true aneurysms. Patients with pseudoaneurysms were more likely to undergo endovascular intervention. Nonoperative treatment is safe in selected patients. (J Vasc Surg 2015;61:389-93.)
In 1805, Sir Astley Cooper ligated the common carotid artery in an attempt to treat an aneurysm of the artery. The surgery was successful but the patient died 48 hours later.1 Dimtza performed the first successful carotid aneurysm excision in 1952 using an end-to-end anastomosis.2 Beall et al were the first to report the use of a prosthetic graft to replace the carotid for aneurysmal disease in 1959.3 Today, open surgical, endovascular, and
From the Division of Vascular Surgery, Mayo Clinic Arizona, Phoenixa; and the Division of Vascular Surgery, Mayo Clinic, Rochester.b Author conflict of interest: none. Presented at a plenary session of the Forty-first Annual Symposium of the Society for Clinical Vascular Surgery, Miami, Fla, March 12-16, 2013. Reprint requests: Samuel R. Money, MD, Division of Vascular Surgery, Mayo Clinic Arizona, 5777 E Mayo Blvd, Phoenix, AZ 85054 (e-mail: [email protected]). The editors and reviewers of this article have no relevant financial relationships to disclose per the JVS policy that requires reviewers to decline review of any manuscript for which they may have a conflict of interest. 0741-5214 Copyright Ó 2015 by the Society for Vascular Surgery. http://dx.doi.org/10.1016/j.jvs.2014.07.092
nonoperative options are available to treat extracranial carotid artery aneurysms (ECCAs). Aneurysms of the extracranial carotid artery are rare and account for less than 1% of all arterial aneurysms.4-7 In the literature, the most common location is the common carotid artery near the bifurcation. The mid to distal internal carotid artery is the second most common location.8 Atherosclerosis is the most common cause, especially in older patients, but trauma, fibromuscular dysplasia, prior surgery, congenital defects, infection, and radiation can all predispose to aneurysmal degeneration.5,8 Large series of the management of ECCAs in the era of endovascular intervention are rare. Herein we present our institution’s experience with the surgical and medical management of ECCAs during the past 15 years and discuss the presentation and treatment of these aneurysms. METHODS After Institutional Review Board approval, a retrospective review of all patients in the Mayo Clinic System diagnosed with ECCA from January 1, 1998, through June 389
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Table I. Presentation, treatment, and follow-up of extracranial carotid artery aneurysms (ECCAs)
Number Mean age, years (P ¼ .08) Age range Gender Men (c2, P ¼ .10) Women Bilateral Symptoms Mass Pain Bleed Stroke/transient ischemic attack Other Treatment Open surgery Endovascular Medical Mean follow-up, months Follow-up range, months
True aneurysms
Pseudoaneurysms
25 67 37-91
116 60 19-95
8 15 2 11 6 2
(35) (65) (8) (44) (24) (8) 0 3 (12)
61 48 7 60 20 2 9 13
(56) (44) (6) (52) (17) (2) (8) (11)
0 (0)
16 (14)
15 (60) 0 (0) 10 (40) 31 0-167
33 (28) 18 (16) 65 (56) 30 0-153
Table II. Endovascular interventions on extracranial carotid pseudoaneurysms
Total aneurysms treated endovascularly Covered stent Uncovered stent with aneurysm coiling Carotid sacrifice/embolization
No.
Percentage
18 4 11 3
100 22 61 17
Table III. Medical treatment of extracranial carotid artery aneurysms (ECCAs) No. Total aneurysms treated medically (no intervention) Aspirin 325 mg Aspirin 81 mg Aspirin 81 mg and clopidogrel 75 mg Clopidogrel 75 mg Warfarin Warfarin and aspirin 81 mg Serial imaging and close follow-up
75 3 40 4 1 7 1 19
Percentage 100 4 53.3 5.3 1.3 9.3 1.3 25.3
Data are presented as number (%) unless otherwise indicated.
30, 2012, was performed. The need for informed consent was waived because of the retrospective nature of the study. This consecutive series included patients at three distinct geographic locations: Rochester, Minnesota; Jacksonville, Florida; and Phoenix, Arizona. Medical records of all patients were reviewed and included radiology reports, clinical notes, and operative reports. Patient demographic information, medical and surgical history, aneurysm size, causes, symptoms, medical and surgical treatments, operative details, and complications were recorded. Follow-up was recorded with clinical notes and repeated imaging. The distinction between true aneurysms and pseudoaneurysms was determined clinically or radiographically by the physicians involved in the care of the patients. When discrepancies arose regarding aneurysm classification, the etiology, pathology reports, and radiographic images were reviewed by the authors. Indications for intervention included symptoms, suspected infection, increasing aneurysm size, and size. Strict size cutoffs were not used; the treating clinicians made determinations about size and the need for intervention on the basis of etiology, aneurysm location, and aneurysm morphology. Basic demographic information and aneurysm characteristics were recorded. When measurements were not documented in the record, one of the authors of this report reviewed the images and calculated measurements. Open surgical intervention was typically performed under general anesthesia. Shunts and electroencephalographic monitoring were used selectively at the surgeon’s discretion. Endovascular procedures were typically performed under conscious sedation unless hemodynamic instability mandated general anesthesia. Complications including bleeding, infection, cranial nerve injury, stroke,
and death were recorded. Statistical analysis was conducted by t-tests and c2 analysis with Microsoft Excel. RESULTS During the 15-year study period, 141 ECCAs in 132 patients seeking treatment at the Mayo Clinic were identified and included for review (Table I). The mean age was 61 years (range, 19-95 years), and 69 patients (52%) were men. Bilateral aneurysms were present in nine patients (7%). Diagnosis was made by magnetic resonance imaging of 61 aneurysms (43%), by computed tomography of 40 (28%), by ultrasound examination of 29 (21%), by angiography of nine (6.5%), and with clinical evidence of rupture but no imaging of two (1.5%). Of these aneurysms, 114 (81%) involved the internal carotid, 11 (8%) the common carotid, 15 (10%) the bifurcation, and 1 (1%) the external carotid. There were 116 (82%) pseudoaneurysms and 25 (18%) true aneurysms; 72 aneurysms (52%) were manifested with symptoms (28 painless mass; 10 transient ischemic attacks; 10 vision symptoms; 9 ruptures; 8 strokes; 4 painful mass; 1 dysphagia; 1 tongue weakness; 1 bruit). Intervention was undertaken in 66 aneurysms, 48 by open surgery and 18 by endovascular intervention. Endovascular interventions included covered stents, uncovered stents with aneurysm coiling, and carotid sacrifice (Table II). Distal embolic protection devices were used at the provider’s discretion. When carotid embolization was considered during endovascular intervention, a balloon occlusion test was performed before embolization. Seventy-five aneurysms were treated nonoperatively; medical therapy included aspirin, anticoagulation, or serial imaging as determined by the treating clinician (Table III).
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Mean follow-up for all aneurysms was 33.9 months. One (0.7%) aneurysm-related death occurred (rupture treated palliatively). No patient undergoing nonoperative treatment suffered death or major morbidity related to the aneurysm. One pseudoaneurysm diagnosed in a 77-year-old and treated nonoperatively with aspirin 81 mg demonstrated a small amount of growth during a 9-year follow-up period but was not operated on because of the patient’s age and slow growth of the aneurysm. Nonoperative treatment was more common in asymptomatic patients (71%) than in symptomatic patients (31%) and in patients whose aneurysms demonstrated stability before consultation at our institution. True aneurysms. Of 25 true aneurysms, 11 (44%) were manifested with symptoms. The average diameter of true aneurysms causing symptoms was 22.8 mm compared with 12.9 mm in asymptomatic aneurysms; 15 (60%) true aneurysms (average diameter, 21.2 mm) underwent open surgical treatment, whereas 10 (40%) were treated nonoperatively (average diameter, 12.0 mm). Surgical procedures included 14 (93%) aneurysmectomies with reconstruction (seven end-to-end anastomoses, four saphenous interpositions, three prosthetic interpositions) and one (7%) aneurysmorrhaphy. Postoperative complications included one stroke during a mean follow-up of 31 months (range, 0-166 months). The stroke occurred 8 hours postoperatively. At exploration, there was considerable thrombus lining the polytetrafluoroethylene graft (W. L. Gore & Associates, Newark, Del). The graft was excised, and the artery was reconstructed with saphenous vein. The patient had no longterm sequelae. No aneurysms treated nonoperatively progressed to need treatment during a mean follow-up of 77 months (range, 1-115 months). The possible cause of true aneurysms was fibromuscular dysplasia in 15 patients, EhlersDanlos syndrome in three, Marfan syndrome in one, and uncharacterized connective tissue diseases in two. The aneurysms were attributed to these diseases when preoperative diagnoses were known, pathologic examination was consistent with the disease, or postoperative testing revealed the presence of the disease. Some pathologic specimens demonstrated characteristics of connective tissue disease that were not specific for fibromuscular dysplasia, Ehlers-Danlos syndrome, or Marfan syndrome. These were classified as uncharacterized. Other true aneurysms without identifiable sources were attributed to idiopathic causes but could have been influenced by hypertension, dyslipidemia, or genetics. Pseudoaneurysms. Of 116 pseudoaneurysms, 60 (52%) were symptomatic. Aneurysms causing symptoms had an average diameter of 17.1 mm compared with an average of 10.5 mm in asymptomatic pseudoaneurysms (P < .01). Thirty-three (29%) pseudoaneurysms (average diameter, 20.9 mm) underwent open surgery, 18 (15%) pseudoaneurysms (average diameter, 14.5 mm) underwent endovascular intervention, and 65 (56%) pseudoaneurysms (average diameter, 10.2 mm) were managed medically; 42 (65%) aneurysms managed medically were treated with
Fankhauser et al 391
antiplatelet agents (35 single-agent, five dual-agent), and seven (11%) were treated with anticoagulation. Pseudoaneurysms at the site of prior endarterectomy accounted for 28 (24%) of all pseudoaneurysms. Pseudoaneurysm after endarterectomy presented at a mean of 82 months from the time of surgery. All of the affected arteries were originally patched (79% Dacron, 7% saphenous vein, 4% bovine pericardium, 10% unknown patch). Seventeen (61%) pseudoaneurysms (average diameter, 24.4 mm) at the site of prior endarterectomy were treated surgically, four (14%) were treated endovascularly (average diameter, 26.8 mm), and seven (25%) were treated medically (average diameter, 15.8 mm). Two pseudoaneurysms caused by infection of a prosthetic patch used during endarterectomy were treated with patch resection and saphenous reconstruction. Trauma accounted for 13 pseudoaneurysms (11%). Three (23%) traumatic pseudoaneurysms with acute presentation underwent open surgical intervention (preoperative imaging not available), and three (23%) with delayed presentation underwent endovascular treatment (average diameter, 13.3 mm). The remaining seven (54%) traumatic pseudoaneurysms (average diameter, 8.3 mm) underwent medical management, five with aspirin therapy and two with observation alone because of the small size of the aneurysms. One traumatic pseudoaneurysm treated surgically was re-explored because of bleeding on postoperative day 2. For the remaining pseudoaneurysms, when trauma or prior intervention was not clearly responsible, the source was attributed to idiopathic causes. DISCUSSION ECCAs are uncommon and occur in a broad range of patients from many causes. The patient populations susceptible to trauma and congenital connective tissue diseases are different from those with atherosclerotic aneurysms or pseudoaneurysm at endarterectomy sites. Each patient population and etiology presents its own challenges. Determining the exact cause of aneurysm formation remains a challenge.4,9 The most common underlying cause of ECCA is atherosclerosis, which in past series has been the leading factor in 37% to 42% of aneurysms.10,11 Trauma has accounted for 35% to 51% of aneurysms in some series,12,13 whereas pseudoaneurysms at prior endarterectomy sites have accounted for 26% to 57% of aneurysms in other series.11,14 The patient population of an institution affects the mean age at presentation. Those centers that see more trauma tend to have a lower mean age at presentation. Our mean age of 61 years is a reflection of a balance between younger patients with trauma or connective tissue diseases and older patients with atherosclerosis or prior endarterectomy. Disorders of connective tissue can cause a number of vascular complications. The pattern of organ system involvement and physiology of vascular disease can often be traced to a single extracellular matrix component.15 Diseases shown to affect the carotid arteries include Marfan
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syndrome, Ehlers-Danlos syndrome, osteogenesis imperfecta, and pseudoxanthoma elasticum.16,17 Polycystic kidney disease and neurofibromatosis, although not technically connective tissue diseases, can also cause carotid artery disease.18,19 Common arterial pathologic change related to these diseases includes dissections, aneurysms, and occlusive disease. When a predisposing disease is suspected in a patient with a carotid aneurysm, further investigation is warranted and should include family history, pathology consultation, and imaging of other affected arterial beds. Genetic testing and counseling should be considered. Open surgical intervention is the standard treatment for aneurysms caused by these diseases, but endovascular intervention may play a role. These patients are at an increased risk of arterial dissection, aneurysm recurrence, and aneurysm expansion.15 Open surgical intervention has been a first-line treatment since Cooper’s initial operation in 1805. The methods have obviously changed, but even with the increasing availability of endovascular options, open surgical repair remains a viable option. Garg et al point out the five basic options for open surgical intervention: aneurysm clipping, excision with primary anastomosis, excision with interposition graft, extracranial-intracranial bypass, and carotid ligation.12 Ligation carries up to a 25% risk of stroke and 20% mortality rate,20 so it tends to be used only as a last resort. In our series, endovascular intervention was used only in the treatment of pseudoaneurysms. This was mainly due to the belief that the causes of the pseudoaneurysms were self-limited and could be addressed endovascularly, whereas the causes of true aneurysms (including connective tissue disease) were ongoing and could lead to further aneurysmal degeneration if treated endovascularly. There was a trend for more endovascular intervention in more recent cases. Open surgical intervention was favored when symptoms occurred, especially mass effect or bleeding. Both covered and bare metal stents have been used to treat ECCAs. Bare metal stents can be used alone or combined with aneurysm sac coiling through the stents. Li et al have proposed criteria that would tend to favor an endovascular approach: aneurysms of the distal cervical internal carotid or hostile necks due to prior surgery or radiation.13 In our series, the choice between open and endovascular intervention was more dependent on the type of aneurysm than on the location. Several series have reported favorable midterm results after endovascular intervention.13,21 Historically, ECCAs were diagnosed when symptoms such as cerebrovascular events, cervical masses, or pain developed. More recently, the diagnosis of asymptomatic aneurysms has increased with more frequent use of crosssectional imaging. In our series, 49% of aneurysms were asymptomatic and discovered incidentally during imaging. Prior studies have reported up to 50% of patients presenting with neurologic symptoms such as stroke or transient ischemic attack.14,22,23 The strength of our series is in both the total number of ECCAs and the varieties of treatment, including medical therapy with observation. Other large series have focused
on intervention alone without an observation cohort.14,24 The weaknesses of our series include its retrospective nature, without predefined diagnostic, treatment, or follow-up algorithms, and the heterogeneity of aneurysms inherent in a large, retrospective review across distinct geographic areas. Nonetheless, it is clear from this series that ECCAs can be successfully and safely treated by both open and endovascular means and that properly selected ECCAs can be treated with medical therapy and observation. CONCLUSIONS ECCAs are uncommon and may be manifested with varying or no symptoms. All segments of the carotid artery are susceptible, although the internal is most commonly affected. Open surgical intervention was more common in patients with symptoms, true aneurysms, and larger aneurysms. Patients with pseudoaneurysms were more likely to undergo endovascular intervention than were patients with true aneurysms. Nonoperative treatment is safe in selected patients and tends to occur in smaller aneurysms. AUTHOR CONTRIBUTIONS Conception and design: GF, WS, SM Analysis and interpretation: GF, WS, MO, SM Data collection: GF Writing the article: GF, WS, RF, SM Critical revision of the article: GF, WS, RF, MO, TB, FM, SM Final approval of the article: GF, WS, RF, MO, TB, FM, SM Statistical analysis: GF Obtained funding: Not applicable Overall responsibility: SM REFERENCES 1. Brock RC. Astley Cooper and carotid artery ligation. Guys Hosp Rep 1968;117:219-24. 2. Dimtza A. Aneurysm of the carotid arteries: report of two cases. Angiology 1956;7:218-27. 3. Beall AC, Crawford ES, Cooley DA. Extracranial aneurysms of the carotid artery. Postgrad Med 1962;32:93-102. 4. Faggioli GL, Freyrie A, Stella A, Pedrini L, Gargiulo M, Tarantini S, et al. Extracranial internal carotid artery aneurysms: results of a surgical series with long-term follow-up. J Vasc Surg 1996;23:587-94; discussion: 594-5. 5. van Sambeek MR, Segeren CM, van Dijk LC, van Essen JA, Dippel DW, van Urk H. Endovascular repair of an extracranial internal carotid artery aneurysm complicated by heparin-induced thrombocytopenia and thrombosis. J Endovasc Ther 2000;7:353-8. 6. Moreau P, Albat B, Thevenet A. Surgical treatment of extracranial internal carotid artery aneurysm. Ann Vasc Surg 1994;8:409-16. 7. McCollum CH, Wheeler WG, Noon GP, DeBakey ME. Aneurysms of the extracranial carotid artery. Twenty-one years’ experience. Am J Surg 1979;137:196-200. 8. Rittenhouse EA, Radke HM, Sumner DS. Carotid artery aneurysm. Review of the literature and report of a case with rupture into the oropharynx. Arch Surg 1972;105:786-9. 9. Stewart MT, Moritz MW, Smith RB 3rd, Fulenwider JT, Perdue GD. The natural history of carotid fibromuscular dysplasia. J Vasc Surg 1986;3:305-10.
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10. Zhang Q, Duan ZQ, Xin SJ, Wang XW, Dong YT. Management of extracranial carotid artery aneurysms: 17 years’ experience. Eur J Vasc Endovasc Surg 1999;18:162-5. 11. Srivastava SD, Eagleton MJ, O’Hara P, Kashyap VS, Sarac T, Clair D. Surgical repair of carotid artery aneurysms: a 10-year, single-center experience. Ann Vasc Surg 2010;24:100-5. 12. Garg K, Rockman CB, Lee V, Maldonado TS, Jacobowitz GR, Adelman MA, et al. Presentation and management of carotid artery aneurysms and pseudoaneurysms. J Vasc Surg 2012;55:1618-22. 13. Li Z, Chang G, Yao C, Guo L, Liu Y, Wang M, et al. Endovascular stenting of extracranial carotid artery aneurysm: a systematic review. Eur J Vasc Endovasc Surg 2011;42:419-26. 14. El-Sabrout R, Cooley DA. Extracranial carotid artery aneurysms: Texas Heart Institute experience. J Vasc Surg 2000;31:702-12. 15. Schievink WI, Michels VV, Piepgras DG. Neurovascular manifestations of heritable connective tissue disorders. A review. Stroke 1994;25: 889-903. 16. Royce PM, Steinmann BU, editors. Connective tissue and its heritable disorders: molecular, genetic, and medical aspects. New York: WileyLiss; 1993. 17. Beighton P, editor. McKusick’s heritable disorders of connective tissue. 5th ed. St. Louis: CV Mosby; 1993.
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18. Schrier RW, Gottschalk CW, editors. Diseases of the kidney. Boston, MA: Little, Brown; 1993. 19. Riccardi V. Neurofibromatosis: phenotype, natural history and pathogenesis. Baltimore, MD: Johns Hopkins University Press; 1992. 20. McCann RL. Basic data related to peripheral artery aneurysms. Ann Vasc Surg 1990;4:411-4. 21. Zhou W, Lin PH, Bush RL, Peden E, Guerrero MA, Terramani T, et al. Carotid artery aneurysm: evolution of management over two decades. J Vasc Surg 2006;43:493-6; discussion: 497. 22. Attigah N, Kulkens S, Zausig N, Hansmann J, Ringleb P, Hakimi M, et al. Surgical therapy of extracranial carotid artery aneurysms: long-term results over a 24-year period. Eur J Vasc Endovasc Surg 2009;37:127-33. 23. Radak D, Davidovic L, Vukobratov V, Ilijevski N, Kostic D, Maksimovic Z, et al. Carotid artery aneurysms: Serbian multicentric study. Ann Vasc Surg 2007;21:23-9. 24. Szopinski P, Ciostek P, Kielar M, Myrcha P, Pleban E, Noszczyk W. A series of 15 patients with extracranial carotid artery aneurysms: surgical and endovascular treatment. Eur J Vasc Endovasc Surg 2005;29: 256-61.
Submitted Feb 11, 2014; accepted Jul 25, 2014.
Surgical and medical management of extracranial carotid artery aneurysms Grant T. Fankhauser, MD,a William M. Stone, MD,a Richard J. Fowl, MD,a Mark E. O’Donnell, MD,a Thomas C. Bower, MD,b Fredric B. Meyer, MD,b and Samuel R. Money, MD, MBA,a Phoenix, Ariz; and Rochester, Minn Objective: Extracranial carotid artery aneurysms (ECCAs) are extremely rare with limited information about management options. Our purpose was to review our institution’s experience with ECCAs during 15 years and to discuss the presentation and treatment of these aneurysms. Methods: A retrospective review of patients diagnosed with ECCAs from 1998 to 2012 was performed. Symptoms, risk factors, etiology, diagnostic methods, treatments, and outcomes were reviewed. Results: During the study period, 141 aneurysms were diagnosed in 132 patients (mean age, 61 years; 69 men). There were 116 (82%) pseudoaneurysms and 25 (18%) true aneurysms; 69 (49%) aneurysms were asymptomatic, whereas 72 (52%) had symptoms (28 painless masses; 10 transient ischemic attacks; 10 vision symptoms; 9 ruptures; 8 strokes; 4 painful mass; 1 dysphagia; 1 tongue weakness; 1 bruit). Causes of true aneurysms included fibromuscular dysplasia in 15 patients, Ehlers-Danlos syndrome in three, Marfan syndrome in one, and uncharacterized connective tissue diseases in two. Of 25 true aneurysms, 11 (44%) were symptomatic; 15 (60%) true aneurysms underwent open surgical treatment, whereas 10 (40%) were managed nonoperatively. Postoperative complications included one stroke during a mean followup of 31 months (range, 0-166 months). No aneurysms managed nonoperatively required intervention during a mean follow-up of 77 months (range, 1-115 months). Of 116 pseudoaneurysms, 60 (52%) were symptomatic; 33 (29%) pseudoaneurysms underwent open surgery, 18 (15%) underwent endovascular intervention, and 65 (56%) were managed medically. Pseudoaneurysm after endarterectomy (28 patients; 24%) presented at a mean of 82 months from the surgical procedure. Mean follow-up for all aneurysms was 33.9 months. One (0.7%) aneurysm-related death occurred (rupture treated palliatively). No patient undergoing nonoperative management suffered death or major morbidity related to the aneurysm. Nonoperative management was more common in asymptomatic patients (71%) than in symptomatic patients (31%). Conclusions: ECCAs are uncommon and may be manifested with varying symptoms. All segments of the carotid artery are susceptible, although the internal is most commonly affected. Open surgical intervention was more common in patients with symptoms and with true aneurysms. Patients with pseudoaneurysms were more likely to undergo endovascular intervention. Nonoperative treatment is safe in selected patients. (J Vasc Surg 2015;61:389-93.)
In 1805, Sir Astley Cooper ligated the common carotid artery in an attempt to treat an aneurysm of the artery. The surgery was successful but the patient died 48 hours later.1 Dimtza performed the first successful carotid aneurysm excision in 1952 using an end-to-end anastomosis.2 Beall et al were the first to report the use of a prosthetic graft to replace the carotid for aneurysmal disease in 1959.3 Today, open surgical, endovascular, and
From the Division of Vascular Surgery, Mayo Clinic Arizona, Phoenixa; and the Division of Vascular Surgery, Mayo Clinic, Rochester.b Author conflict of interest: none. Presented at a plenary session of the Forty-first Annual Symposium of the Society for Clinical Vascular Surgery, Miami, Fla, March 12-16, 2013. Reprint requests: Samuel R. Money, MD, Division of Vascular Surgery, Mayo Clinic Arizona, 5777 E Mayo Blvd, Phoenix, AZ 85054 (e-mail: [email protected]). The editors and reviewers of this article have no relevant financial relationships to disclose per the JVS policy that requires reviewers to decline review of any manuscript for which they may have a conflict of interest. 0741-5214 Copyright Ó 2015 by the Society for Vascular Surgery. http://dx.doi.org/10.1016/j.jvs.2014.07.092
nonoperative options are available to treat extracranial carotid artery aneurysms (ECCAs). Aneurysms of the extracranial carotid artery are rare and account for less than 1% of all arterial aneurysms.4-7 In the literature, the most common location is the common carotid artery near the bifurcation. The mid to distal internal carotid artery is the second most common location.8 Atherosclerosis is the most common cause, especially in older patients, but trauma, fibromuscular dysplasia, prior surgery, congenital defects, infection, and radiation can all predispose to aneurysmal degeneration.5,8 Large series of the management of ECCAs in the era of endovascular intervention are rare. Herein we present our institution’s experience with the surgical and medical management of ECCAs during the past 15 years and discuss the presentation and treatment of these aneurysms. METHODS After Institutional Review Board approval, a retrospective review of all patients in the Mayo Clinic System diagnosed with ECCA from January 1, 1998, through June 389
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Table I. Presentation, treatment, and follow-up of extracranial carotid artery aneurysms (ECCAs)
Number Mean age, years (P ¼ .08) Age range Gender Men (c2, P ¼ .10) Women Bilateral Symptoms Mass Pain Bleed Stroke/transient ischemic attack Other Treatment Open surgery Endovascular Medical Mean follow-up, months Follow-up range, months
True aneurysms
Pseudoaneurysms
25 67 37-91
116 60 19-95
8 15 2 11 6 2
(35) (65) (8) (44) (24) (8) 0 3 (12)
61 48 7 60 20 2 9 13
(56) (44) (6) (52) (17) (2) (8) (11)
0 (0)
16 (14)
15 (60) 0 (0) 10 (40) 31 0-167
33 (28) 18 (16) 65 (56) 30 0-153
Table II. Endovascular interventions on extracranial carotid pseudoaneurysms
Total aneurysms treated endovascularly Covered stent Uncovered stent with aneurysm coiling Carotid sacrifice/embolization
No.
Percentage
18 4 11 3
100 22 61 17
Table III. Medical treatment of extracranial carotid artery aneurysms (ECCAs) No. Total aneurysms treated medically (no intervention) Aspirin 325 mg Aspirin 81 mg Aspirin 81 mg and clopidogrel 75 mg Clopidogrel 75 mg Warfarin Warfarin and aspirin 81 mg Serial imaging and close follow-up
75 3 40 4 1 7 1 19
Percentage 100 4 53.3 5.3 1.3 9.3 1.3 25.3
Data are presented as number (%) unless otherwise indicated.
30, 2012, was performed. The need for informed consent was waived because of the retrospective nature of the study. This consecutive series included patients at three distinct geographic locations: Rochester, Minnesota; Jacksonville, Florida; and Phoenix, Arizona. Medical records of all patients were reviewed and included radiology reports, clinical notes, and operative reports. Patient demographic information, medical and surgical history, aneurysm size, causes, symptoms, medical and surgical treatments, operative details, and complications were recorded. Follow-up was recorded with clinical notes and repeated imaging. The distinction between true aneurysms and pseudoaneurysms was determined clinically or radiographically by the physicians involved in the care of the patients. When discrepancies arose regarding aneurysm classification, the etiology, pathology reports, and radiographic images were reviewed by the authors. Indications for intervention included symptoms, suspected infection, increasing aneurysm size, and size. Strict size cutoffs were not used; the treating clinicians made determinations about size and the need for intervention on the basis of etiology, aneurysm location, and aneurysm morphology. Basic demographic information and aneurysm characteristics were recorded. When measurements were not documented in the record, one of the authors of this report reviewed the images and calculated measurements. Open surgical intervention was typically performed under general anesthesia. Shunts and electroencephalographic monitoring were used selectively at the surgeon’s discretion. Endovascular procedures were typically performed under conscious sedation unless hemodynamic instability mandated general anesthesia. Complications including bleeding, infection, cranial nerve injury, stroke,
and death were recorded. Statistical analysis was conducted by t-tests and c2 analysis with Microsoft Excel. RESULTS During the 15-year study period, 141 ECCAs in 132 patients seeking treatment at the Mayo Clinic were identified and included for review (Table I). The mean age was 61 years (range, 19-95 years), and 69 patients (52%) were men. Bilateral aneurysms were present in nine patients (7%). Diagnosis was made by magnetic resonance imaging of 61 aneurysms (43%), by computed tomography of 40 (28%), by ultrasound examination of 29 (21%), by angiography of nine (6.5%), and with clinical evidence of rupture but no imaging of two (1.5%). Of these aneurysms, 114 (81%) involved the internal carotid, 11 (8%) the common carotid, 15 (10%) the bifurcation, and 1 (1%) the external carotid. There were 116 (82%) pseudoaneurysms and 25 (18%) true aneurysms; 72 aneurysms (52%) were manifested with symptoms (28 painless mass; 10 transient ischemic attacks; 10 vision symptoms; 9 ruptures; 8 strokes; 4 painful mass; 1 dysphagia; 1 tongue weakness; 1 bruit). Intervention was undertaken in 66 aneurysms, 48 by open surgery and 18 by endovascular intervention. Endovascular interventions included covered stents, uncovered stents with aneurysm coiling, and carotid sacrifice (Table II). Distal embolic protection devices were used at the provider’s discretion. When carotid embolization was considered during endovascular intervention, a balloon occlusion test was performed before embolization. Seventy-five aneurysms were treated nonoperatively; medical therapy included aspirin, anticoagulation, or serial imaging as determined by the treating clinician (Table III).
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Mean follow-up for all aneurysms was 33.9 months. One (0.7%) aneurysm-related death occurred (rupture treated palliatively). No patient undergoing nonoperative treatment suffered death or major morbidity related to the aneurysm. One pseudoaneurysm diagnosed in a 77-year-old and treated nonoperatively with aspirin 81 mg demonstrated a small amount of growth during a 9-year follow-up period but was not operated on because of the patient’s age and slow growth of the aneurysm. Nonoperative treatment was more common in asymptomatic patients (71%) than in symptomatic patients (31%) and in patients whose aneurysms demonstrated stability before consultation at our institution. True aneurysms. Of 25 true aneurysms, 11 (44%) were manifested with symptoms. The average diameter of true aneurysms causing symptoms was 22.8 mm compared with 12.9 mm in asymptomatic aneurysms; 15 (60%) true aneurysms (average diameter, 21.2 mm) underwent open surgical treatment, whereas 10 (40%) were treated nonoperatively (average diameter, 12.0 mm). Surgical procedures included 14 (93%) aneurysmectomies with reconstruction (seven end-to-end anastomoses, four saphenous interpositions, three prosthetic interpositions) and one (7%) aneurysmorrhaphy. Postoperative complications included one stroke during a mean follow-up of 31 months (range, 0-166 months). The stroke occurred 8 hours postoperatively. At exploration, there was considerable thrombus lining the polytetrafluoroethylene graft (W. L. Gore & Associates, Newark, Del). The graft was excised, and the artery was reconstructed with saphenous vein. The patient had no longterm sequelae. No aneurysms treated nonoperatively progressed to need treatment during a mean follow-up of 77 months (range, 1-115 months). The possible cause of true aneurysms was fibromuscular dysplasia in 15 patients, EhlersDanlos syndrome in three, Marfan syndrome in one, and uncharacterized connective tissue diseases in two. The aneurysms were attributed to these diseases when preoperative diagnoses were known, pathologic examination was consistent with the disease, or postoperative testing revealed the presence of the disease. Some pathologic specimens demonstrated characteristics of connective tissue disease that were not specific for fibromuscular dysplasia, Ehlers-Danlos syndrome, or Marfan syndrome. These were classified as uncharacterized. Other true aneurysms without identifiable sources were attributed to idiopathic causes but could have been influenced by hypertension, dyslipidemia, or genetics. Pseudoaneurysms. Of 116 pseudoaneurysms, 60 (52%) were symptomatic. Aneurysms causing symptoms had an average diameter of 17.1 mm compared with an average of 10.5 mm in asymptomatic pseudoaneurysms (P < .01). Thirty-three (29%) pseudoaneurysms (average diameter, 20.9 mm) underwent open surgery, 18 (15%) pseudoaneurysms (average diameter, 14.5 mm) underwent endovascular intervention, and 65 (56%) pseudoaneurysms (average diameter, 10.2 mm) were managed medically; 42 (65%) aneurysms managed medically were treated with
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antiplatelet agents (35 single-agent, five dual-agent), and seven (11%) were treated with anticoagulation. Pseudoaneurysms at the site of prior endarterectomy accounted for 28 (24%) of all pseudoaneurysms. Pseudoaneurysm after endarterectomy presented at a mean of 82 months from the time of surgery. All of the affected arteries were originally patched (79% Dacron, 7% saphenous vein, 4% bovine pericardium, 10% unknown patch). Seventeen (61%) pseudoaneurysms (average diameter, 24.4 mm) at the site of prior endarterectomy were treated surgically, four (14%) were treated endovascularly (average diameter, 26.8 mm), and seven (25%) were treated medically (average diameter, 15.8 mm). Two pseudoaneurysms caused by infection of a prosthetic patch used during endarterectomy were treated with patch resection and saphenous reconstruction. Trauma accounted for 13 pseudoaneurysms (11%). Three (23%) traumatic pseudoaneurysms with acute presentation underwent open surgical intervention (preoperative imaging not available), and three (23%) with delayed presentation underwent endovascular treatment (average diameter, 13.3 mm). The remaining seven (54%) traumatic pseudoaneurysms (average diameter, 8.3 mm) underwent medical management, five with aspirin therapy and two with observation alone because of the small size of the aneurysms. One traumatic pseudoaneurysm treated surgically was re-explored because of bleeding on postoperative day 2. For the remaining pseudoaneurysms, when trauma or prior intervention was not clearly responsible, the source was attributed to idiopathic causes. DISCUSSION ECCAs are uncommon and occur in a broad range of patients from many causes. The patient populations susceptible to trauma and congenital connective tissue diseases are different from those with atherosclerotic aneurysms or pseudoaneurysm at endarterectomy sites. Each patient population and etiology presents its own challenges. Determining the exact cause of aneurysm formation remains a challenge.4,9 The most common underlying cause of ECCA is atherosclerosis, which in past series has been the leading factor in 37% to 42% of aneurysms.10,11 Trauma has accounted for 35% to 51% of aneurysms in some series,12,13 whereas pseudoaneurysms at prior endarterectomy sites have accounted for 26% to 57% of aneurysms in other series.11,14 The patient population of an institution affects the mean age at presentation. Those centers that see more trauma tend to have a lower mean age at presentation. Our mean age of 61 years is a reflection of a balance between younger patients with trauma or connective tissue diseases and older patients with atherosclerosis or prior endarterectomy. Disorders of connective tissue can cause a number of vascular complications. The pattern of organ system involvement and physiology of vascular disease can often be traced to a single extracellular matrix component.15 Diseases shown to affect the carotid arteries include Marfan
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syndrome, Ehlers-Danlos syndrome, osteogenesis imperfecta, and pseudoxanthoma elasticum.16,17 Polycystic kidney disease and neurofibromatosis, although not technically connective tissue diseases, can also cause carotid artery disease.18,19 Common arterial pathologic change related to these diseases includes dissections, aneurysms, and occlusive disease. When a predisposing disease is suspected in a patient with a carotid aneurysm, further investigation is warranted and should include family history, pathology consultation, and imaging of other affected arterial beds. Genetic testing and counseling should be considered. Open surgical intervention is the standard treatment for aneurysms caused by these diseases, but endovascular intervention may play a role. These patients are at an increased risk of arterial dissection, aneurysm recurrence, and aneurysm expansion.15 Open surgical intervention has been a first-line treatment since Cooper’s initial operation in 1805. The methods have obviously changed, but even with the increasing availability of endovascular options, open surgical repair remains a viable option. Garg et al point out the five basic options for open surgical intervention: aneurysm clipping, excision with primary anastomosis, excision with interposition graft, extracranial-intracranial bypass, and carotid ligation.12 Ligation carries up to a 25% risk of stroke and 20% mortality rate,20 so it tends to be used only as a last resort. In our series, endovascular intervention was used only in the treatment of pseudoaneurysms. This was mainly due to the belief that the causes of the pseudoaneurysms were self-limited and could be addressed endovascularly, whereas the causes of true aneurysms (including connective tissue disease) were ongoing and could lead to further aneurysmal degeneration if treated endovascularly. There was a trend for more endovascular intervention in more recent cases. Open surgical intervention was favored when symptoms occurred, especially mass effect or bleeding. Both covered and bare metal stents have been used to treat ECCAs. Bare metal stents can be used alone or combined with aneurysm sac coiling through the stents. Li et al have proposed criteria that would tend to favor an endovascular approach: aneurysms of the distal cervical internal carotid or hostile necks due to prior surgery or radiation.13 In our series, the choice between open and endovascular intervention was more dependent on the type of aneurysm than on the location. Several series have reported favorable midterm results after endovascular intervention.13,21 Historically, ECCAs were diagnosed when symptoms such as cerebrovascular events, cervical masses, or pain developed. More recently, the diagnosis of asymptomatic aneurysms has increased with more frequent use of crosssectional imaging. In our series, 49% of aneurysms were asymptomatic and discovered incidentally during imaging. Prior studies have reported up to 50% of patients presenting with neurologic symptoms such as stroke or transient ischemic attack.14,22,23 The strength of our series is in both the total number of ECCAs and the varieties of treatment, including medical therapy with observation. Other large series have focused
on intervention alone without an observation cohort.14,24 The weaknesses of our series include its retrospective nature, without predefined diagnostic, treatment, or follow-up algorithms, and the heterogeneity of aneurysms inherent in a large, retrospective review across distinct geographic areas. Nonetheless, it is clear from this series that ECCAs can be successfully and safely treated by both open and endovascular means and that properly selected ECCAs can be treated with medical therapy and observation. CONCLUSIONS ECCAs are uncommon and may be manifested with varying or no symptoms. All segments of the carotid artery are susceptible, although the internal is most commonly affected. Open surgical intervention was more common in patients with symptoms, true aneurysms, and larger aneurysms. Patients with pseudoaneurysms were more likely to undergo endovascular intervention than were patients with true aneurysms. Nonoperative treatment is safe in selected patients and tends to occur in smaller aneurysms. AUTHOR CONTRIBUTIONS Conception and design: GF, WS, SM Analysis and interpretation: GF, WS, MO, SM Data collection: GF Writing the article: GF, WS, RF, SM Critical revision of the article: GF, WS, RF, MO, TB, FM, SM Final approval of the article: GF, WS, RF, MO, TB, FM, SM Statistical analysis: GF Obtained funding: Not applicable Overall responsibility: SM REFERENCES 1. Brock RC. Astley Cooper and carotid artery ligation. Guys Hosp Rep 1968;117:219-24. 2. Dimtza A. Aneurysm of the carotid arteries: report of two cases. Angiology 1956;7:218-27. 3. Beall AC, Crawford ES, Cooley DA. Extracranial aneurysms of the carotid artery. Postgrad Med 1962;32:93-102. 4. Faggioli GL, Freyrie A, Stella A, Pedrini L, Gargiulo M, Tarantini S, et al. Extracranial internal carotid artery aneurysms: results of a surgical series with long-term follow-up. J Vasc Surg 1996;23:587-94; discussion: 594-5. 5. van Sambeek MR, Segeren CM, van Dijk LC, van Essen JA, Dippel DW, van Urk H. Endovascular repair of an extracranial internal carotid artery aneurysm complicated by heparin-induced thrombocytopenia and thrombosis. J Endovasc Ther 2000;7:353-8. 6. Moreau P, Albat B, Thevenet A. Surgical treatment of extracranial internal carotid artery aneurysm. Ann Vasc Surg 1994;8:409-16. 7. McCollum CH, Wheeler WG, Noon GP, DeBakey ME. Aneurysms of the extracranial carotid artery. Twenty-one years’ experience. Am J Surg 1979;137:196-200. 8. Rittenhouse EA, Radke HM, Sumner DS. Carotid artery aneurysm. Review of the literature and report of a case with rupture into the oropharynx. Arch Surg 1972;105:786-9. 9. Stewart MT, Moritz MW, Smith RB 3rd, Fulenwider JT, Perdue GD. The natural history of carotid fibromuscular dysplasia. J Vasc Surg 1986;3:305-10.
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10. Zhang Q, Duan ZQ, Xin SJ, Wang XW, Dong YT. Management of extracranial carotid artery aneurysms: 17 years’ experience. Eur J Vasc Endovasc Surg 1999;18:162-5. 11. Srivastava SD, Eagleton MJ, O’Hara P, Kashyap VS, Sarac T, Clair D. Surgical repair of carotid artery aneurysms: a 10-year, single-center experience. Ann Vasc Surg 2010;24:100-5. 12. Garg K, Rockman CB, Lee V, Maldonado TS, Jacobowitz GR, Adelman MA, et al. Presentation and management of carotid artery aneurysms and pseudoaneurysms. J Vasc Surg 2012;55:1618-22. 13. Li Z, Chang G, Yao C, Guo L, Liu Y, Wang M, et al. Endovascular stenting of extracranial carotid artery aneurysm: a systematic review. Eur J Vasc Endovasc Surg 2011;42:419-26. 14. El-Sabrout R, Cooley DA. Extracranial carotid artery aneurysms: Texas Heart Institute experience. J Vasc Surg 2000;31:702-12. 15. Schievink WI, Michels VV, Piepgras DG. Neurovascular manifestations of heritable connective tissue disorders. A review. Stroke 1994;25: 889-903. 16. Royce PM, Steinmann BU, editors. Connective tissue and its heritable disorders: molecular, genetic, and medical aspects. New York: WileyLiss; 1993. 17. Beighton P, editor. McKusick’s heritable disorders of connective tissue. 5th ed. St. Louis: CV Mosby; 1993.
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18. Schrier RW, Gottschalk CW, editors. Diseases of the kidney. Boston, MA: Little, Brown; 1993. 19. Riccardi V. Neurofibromatosis: phenotype, natural history and pathogenesis. Baltimore, MD: Johns Hopkins University Press; 1992. 20. McCann RL. Basic data related to peripheral artery aneurysms. Ann Vasc Surg 1990;4:411-4. 21. Zhou W, Lin PH, Bush RL, Peden E, Guerrero MA, Terramani T, et al. Carotid artery aneurysm: evolution of management over two decades. J Vasc Surg 2006;43:493-6; discussion: 497. 22. Attigah N, Kulkens S, Zausig N, Hansmann J, Ringleb P, Hakimi M, et al. Surgical therapy of extracranial carotid artery aneurysms: long-term results over a 24-year period. Eur J Vasc Endovasc Surg 2009;37:127-33. 23. Radak D, Davidovic L, Vukobratov V, Ilijevski N, Kostic D, Maksimovic Z, et al. Carotid artery aneurysms: Serbian multicentric study. Ann Vasc Surg 2007;21:23-9. 24. Szopinski P, Ciostek P, Kielar M, Myrcha P, Pleban E, Noszczyk W. A series of 15 patients with extracranial carotid artery aneurysms: surgical and endovascular treatment. Eur J Vasc Endovasc Surg 2005;29: 256-61.
Submitted Feb 11, 2014; accepted Jul 25, 2014.
