- Email: [email protected]
Neurofibromatosis Type 1–Associated Extracranial Vertebral Artery Aneurysm Complicated by Vertebral Arteriovenous Fistula After Rupture: Case Report and Literature Review
Case Report
Neurofibromatosis Type 1eAssociated Extracranial Vertebral Artery Aneurysm Complicated by Vertebral Arteriovenous Fistula After Rupture: Case Report and Literature Review Atsuhito Uneda, Kenta Suzuki, Shuichi Okubo, Koji Hirashita, Masatoshi Yunoki, Kimihiro Yoshino
Key words Aneurysm - Arteriovenous fistula - Neurofibromatosis type 1 - Vertebral artery - von Recklinghausen disease -
Abbreviations and Acronyms AVF: Arteriovenous fistula NF1: Neurofibromatosis type 1 Department of Neurosurgery, Kagawa Rosai Hospital, Marugame, Kagawa, Japan To whom correspondence should be addressed: Atsuhito Uneda, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2016). http://dx.doi.org/10.1016/j.wneu.2016.09.036 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2016 Elsevier Inc. All rights reserved.
INTRODUCTION Neurofibromatosis type 1 (NF1) is an autosomal dominant familial disorder with an incidence of approximately 1 in 3000e4000 individuals.1,2 Vascular abnormalities associated with NF1 reportedly occur in 0.4%e6.4% of patients3-5 and most commonly involve the aorta and renal arteries.6 Both extracranial vertebral artery aneurysm and vertebral arteriovenous fistula (AVF) are relatively rare, and in the majority of cases occur in response to trauma involving the craniocervical region.7,8 Nontraumatic causes include hypertension, infection, inflammatory disease, and inherited disorders, such as Marfan syndrome, EhlerseDanlos syndrome, and NF1.9-12 Craniocervical vascular abnormalities are uncommon manifestations of NF1. Those reported to date include stenosis, occlusion, aneurysm, and AVF,6 whereas extracranial vertebral artery aneurysm is rare.9,10,13-31 Patients with extracranial vertebral artery aneurysm typically present with radiculopathy, neck pain or
- BACKGROUND:
Extracranial vertebral artery aneurysm related to neurofibromatosis type 1 (NF1) is rare. Aneurysmal rupture typically induces such symptoms as cervical hematoma, hemothorax, and hypotension. Here we report a case of ruptured extracranial vertebral artery aneurysm in a patient with NF1 who, rather than cervical hematoma, hemothorax, or hypotension, developed a vertebral arteriovenous fistula (AVF) after aneurysm rupture.
- CASE
DESCRIPTION: A 35-year-old woman with a family history of NF1 presented with sudden-onset right neck and shoulder pain. Computed tomography angiography showed a right extracranial vertebral artery aneurysm. She had neither a cervical hematoma nor hypotension; however, angiography showed an AVF secondary to aneurysmal rupture. The patient was treated with endovascular coil embolization to prevent re-rupture. Postoperatively, her right neck and shoulder pain improved, and she was discharged without further neurologic deficits.
- CONCLUSIONS:
This patient’s clinical course suggests that if there is minimal bleeding from an NF1-associated ruptured extracranial vertebral artery aneurysm, then typical symptoms, such as cervical hematoma, hemothorax, and hypotension, may be absent. Thus, ruptured extracranial vertebral artery aneurysm should be considered in the differential diagnosis of patients with NF1 with sudden-onset radiculopathy, even in the absence of typical symptoms. The detection of a vertebral AVF provides a useful clue to the diagnosis of aneurysm rupture in such cases.
neck mass, and—in those with rupture— cervical hematoma, hemothorax, or hypotension. There have only been 2 reported cases of extracranial vertebral artery aneurysm associated with NF1 in which the AVF was detected at the same time as the aneurysm.28,29 Here we report a patient with NF1 who presented with a ruptured extracranial vertebral artery aneurysm, the sole manifestation of which was a vertebral AVF rather than the more common symptoms of cervical hematoma, hemothorax or hypotension. To the best of our knowledge, this is the first description of a patient with a ruptured extracranial vertebral artery aneurysm associated with NF1 in whom these symptoms were absent. We discuss our findings in the context of a literature review
WORLD NEUROSURGERY -: ---, MONTH 2016
of NF1-associated extracranial vertebral artery aneurysms. CASE REPORT A 35-year-old woman with a paternal family history of NF1 presented to our hospital complaining of severe right neck and shoulder pain that had begun suddenly after a bout of intense coughing starting 5 days earlier. She was fully conscious, and clinical examination revealed no evidence of cervical hematoma, no cervical bruit, and normal blood pressure. Multiple fibromas and café au lait spots were visible on her chest and abdomen. Radiologic Findings Cervical T2-weighted magnetic resonance imaging showed a round hypointense
www.WORLDNEUROSURGERY.org
1.E1
CASE REPORT ATSUHITO UNEDA ET AL.
EXTRACRANIAL VA ANEURYSM AND VERTEBRAL AVF ASSOCIATED WITH NF1
Figure 1. (A) Axial T2-weighted magnetic resonance imaging showing a hypointense mass compressing the right C3 nerve root. (B) Neck 3-dimensional computed tomography angiography showing an aneurysm of 15 mm diameter in the C3eC4 segment of the right cervical vertebral artery. (C) Axial computed tomography scan showing enlargement of the C3eC4 intravertebral foramen owing to bony erosion by the aneurysm. (D) A lateral view obtained on right vertebral angiography showing an aneurysm in the C3eC4 segment of the right cervical vertebral artery and a right vertebral arteriovenous fistula draining into the spinal venous system. (E) Anteroposterior view on left vertebral artery angiography showing retrograde filling of the right distal vertebral artery and aneurysm.
mass compressing the right third cervical nerve root (Figure 1A). A flow void inside the mass suggested a vascular lesion. Three-dimensional computed tomography angiography of the neck revealed a right cervical vertebral artery aneurysm at the level of C3eC4 with a diameter of 15 mm (Figure 1B). Enlargement of the C3eC4 intravertebral foramen owing to bony erosion by the aneurysm was also observed (Figure 1C). The patient’s symptoms were attributed
to radiculopathy of the right C3 nerve root. At 4 days after admission, the patient underwent right vertebral angiography via the right femoral artery. The aneurysm in the right cervical vertebral artery at the C3eC4 segment and a vertebral AVF that had likely developed subsequent to aneurysmal rupture were identified (Figure 1D). A 5-Fr ENVOY guiding catheter (Codman, Miami, Florida, USA) was advanced into the proximal
right vertebral artery via the right femoral artery, followed by a Scepter XC balloon catheter (Microvention, Tustin, California, USA), as far as the C5eC6 intervertebral space. A balloon occlusion test of the proximal right cervical vertebral artery was performed for 15 minutes. Left vertebral angiography from a 4-Fr diagnostic catheter placed in the left vertebral artery via the left femoral artery showed the right distal vertebral artery and the aneurysm in retrograde (Figure 1E). The
Figure 2. (A) Lateral view on preoperative right vertebral angiography showing the spontaneous occlusion of the distal portion of the aneurysm, with the major portion of the aneurysm and the vertebral arteriovenous fistula (AVF) still visualized. (B) Anteroposterior view on preoperative left vertebral angiography showing the right distal vertebral artery in retrograde, without visualization of the aneurysm or AVF. (C) Anteroposterior view on postoperative right vertebral angiography confirming successful occlusion of the cervical vertebral artery aneurysm and AVF. (Left) Precontrast. (Right) Subtracted. (D) Lateral view on postoperative right vertebral angiography. (Left) Precontrast. (Right) Subtracted.
1.E2
www.SCIENCEDIRECT.com
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2016.09.036
Case
Age (years)/ Sex
Author (year)
Side
Level
Symptoms
Ruptured or Unruptured
AVF
Outcome and Follow-Up
Treatment
1
Schubiger and Yasargil (1978)13
50/Male
Left
C2eC6
Radiculopathy
Unruptured
Direct surgery
GR
2
Pentecost et al. (1981)14
1/Female
Left
Th1
Limited neck movement, arm weakness
Unruptured
Observation
SD (intraoperative bleeding of other aneurysm)
3
Detwiler et al. (1987)15
52/Female
Left
C2
Neck mass, neck pain, bruits
Unruptured
Endovascular (balloon)
GR
4
Negoro et al. (1990)16
47/Male
Left
C1
Neck pain, cervical hematoma
Ruptured
Endovascular (balloon)
GR
5
Muhonen et al. (1991)
52/Female
Left
C2
Neck mass, neck pain, arm weakness
Unruptured
Endovascular (balloon)
GR
6
Schievink and Piepgras (1991)18
43/Female
Left
C7
No symptoms
Unruptured
Observation
GR
7
Ohkata et al. (1994)19
48/Female
Left
C4eC7
Radiculopathy
Unruptured
Direct surgery
GR
8
Horsley et al. (1997)20
56/Female
Left
C5eC7
Neck pain, arm paresthesias, neck mass
Ruptured
Endovascular (coil)
GR
17
Hoffmann et al. (1998)
59/Male
Right
C6
None
Unruptured
Observation
GR
10
Ushikoshi et al. (1999)22
40/Female
Left
C1
Occipitalgia, cervical hematoma
Ruptured
Secondary AVF at the same site 11 years later
Endovascular (balloon)
GR
11
Miyazaki et al. (2004)23
52/Female
Left
C5eC7
Radiculopathy, hypotension, altered consciousness, hemothorax
Ruptured
Endovascular (balloon), direct surgery
D
12
Arai et al. (2007)24
38/Male
Left
NR
Chest pain, dizziness, vomiting, hemothorax
Ruptured
Untreated
D
13
Hieda et al. (2007)25
36/Female
Left
Ostium of vertebral artery
Back pain, chest pain, dyspnea, hypotension, hemothorax, coma
Ruptured
Endovascular (coil, NBCA)
D
14
Hiramatsu et al. (2007)26
67/Male
Left
Proximal segment of vertebral artery (V1)
Dizziness
Unruptured
Endovascular (coil)
GR
15
Pereira et al. (2007)9
Endovascular (balloon)
GR
16
14/Female
Right
C5eC6
Radiculopathy
Unruptured
10
18/Female
Right
C5eC6
Radiculopathy
Unruptured
Endovascular (coil)
GR
27
Peyre et al. (2007) Horie et al. (2008)
30/Female
Right
C6eC7
Radiculopathy
Unruptured
Endovascular (coil, balloon)
GR
18
Higa et al. (2010)28
60/Female
Left
NR
Cervical hematoma, stridor, respiratory failure
Ruptured
þ
Endovascular (coil)
SD (after 3 months, ventilator-dependent)
19
Morvan et al. (2011)29
36/Female
Left
C3eC4
Headache, neck pain, vomiting, subarachnoid hemorrhage
Ruptured
þ
Endovascular (coil, stent)
NR
AVF, arteriovenous fistula; D, death; GR, good recovery; NR, not reported; SD, severely disabled. Continues
CASE REPORT
1.E3
17
EXTRACRANIAL VA ANEURYSM AND VERTEBRAL AVF ASSOCIATED WITH NF1
www.WORLDNEUROSURGERY.org
9
21
ATSUHITO UNEDA ET AL.
WORLD NEUROSURGERY -: ---, MONTH 2016
Table 1. Reported Cases of Extracranial Vertebral Artery Aneurysm Associated With NF1, Including Our Case
CASE REPORT ATSUHITO UNEDA ET AL.
EXTRACRANIAL VA ANEURYSM AND VERTEBRAL AVF ASSOCIATED WITH NF1
1.E4
Endovascular (coil) þ
GR
Direct surgery, endovascular (stent)
GR
Endovascular (coil)
AVF, arteriovenous fistula; D, death; GR, good recovery; NR, not reported; SD, severely disabled.
Ruptured C3eC4 Right 35/Female 22
Present case
C8 32/Male 21
Gouaillier-Vulcain et al. (2014)31
Left
Radiculopathy
Unruptured Radiculopathy
Ruptured Neck pain, cervical hematoma, radiculopathy C6 Right 31/Male Hiramatsu et al. (2012)30 20
Author (year) Case
Table 1. Continued
Age (years)/ Sex
Side
Level
Symptoms
Ruptured or Unruptured
AVF
Treatment
GR
Outcome and Follow-Up
patient reported no neurologic deficits during occlusion.
www.SCIENCEDIRECT.com
Treatment At 6 days after admission, the patient underwent endovascular coil embolization to prevent re-rupture of the aneurysm. A 7-Fr Optimo balloon catheter (Tokai Medical Products, Kasugai, Japan) was placed via the right femoral artery into the proximal right vertebral artery. Preoperative right vertebral angiography from a 7-Fr Optimo balloon catheter showed spontaneous occlusion of the distal portion of the aneurysm, but the major portion of the aneurysm and the vertebral AVF were still evident (Figure 2A). Left vertebral angiography from a 4-Fr diagnostic catheter placed via the left femoral artery into the left vertebral artery showed the right distal vertebral artery in retrograde, without visualization of the aneurysm or the AVF (Figure 2B). An Excelsior SL-10 microcatheter (Stryker Neurovascular, Fremont, California, USA) was inserted through the Optimo balloon catheter, so that its tip lay within the aneurysmal cavity. Endovascular trapping with 10 Target XL detachable coils (Stryker), and 5 Orbit Galaxy detachable coils (Codman) was performed from the distal aneurysmal neck to the proximal vertebral artery. Neither the aneurysm nor the AVF could be visualized during postoperative angiography of the right vertebral artery (Figure 2C and D). Postoperative angiography of the left vertebral artery demonstrated adequate flow in the basilar artery and retrograde flow into the right vertebral artery, without visualization of the aneurysm or AVF. Postoperative Course and Follow-up The patient reported an improvement in her right neck and shoulder pain, and experienced no further neurologic deficits. She was discharged on aspirin 100 mg once daily and clopidogrel 75 mg once daily. Follow-up angiography performed 3 months after surgery confirmed no recurrence of the right cervical vertebral artery aneurysm or AVF. DISCUSSION NF1, also known as von Recklinghausen disease, is an autosomal dominant familial
disorder caused by mutations of the NF1 gene, located on the long arm of chromosome 17 (17q11.2).32 Neurofibromin, the protein product of the NF1 gene, functions in part as a negative regulator of the p21 Ras proto-oncogene.32 The loss of neurofibromin expression results in increased mitogenic signaling and thus increased cell growth, which in turn facilitates tumor formation.32 Vascular abnormalities associated with NF1 are rare and may reflect disruption of the vascular maintenance and repair regulated by neurofibromin.33 In a literature search, we found 22 cases of extracranial vertebral artery aneurysm associated with NF1 (Table 1).9,10,13-31 Rupture occurred in 10 of these cases, as in our patient, whereas rupture was not reported in 12 cases. The mean age at diagnosis was 41 years (range, 1e67 years). The majority of aneurysms occurred on the left side (16:6) and in women (15:7). Patients typically presented with radiculopathy, neck pain, or neck mass; in those with rupture, cervical hematoma, hemothorax, or hypotension was the characteristic presenting symptom. More than 30 cases of vertebral AVF associated with NF1 have been reported to date,28,34 whereas vertebral AVF combined with extracranial vertebral artery aneurysm associated with NF1 is very unusual. A literature review uncovered only 3 other cases (Table 1). Including our patient, the aneurysm ruptured in all 4 cases, and the AVF was detected in the extracranial vertebral artery at the same time as the aneurysm in 3 cases (including ours).28,29 In 1 patient, the vertebral AVF developed at the site of the aneurysm 11 years after rupture.22 Deans et al.35 suggested 2 mechanisms by which an AVF might arise in a patient with NF1, either by rupture of a preexisting extracranial vertebral artery aneurysm into the vertebral venous plexus, or congenitally as a manifestation of mesodermal dysplasia.35 Alternatively, a flow-related aneurysm-like dilatation of vertebral artery might arise proximal to a preexisting AVF.35 In aneurysmal rupture leading to AVF, the onset of symptoms is generally acute,28,29 whereas in flowrelated aneurysm-like dilatation of the artery proximal to the AVF, symptoms are usually progressive.35 In our patient, typical symptoms of rupture, especially cervical hematoma or
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2016.09.036
CASE REPORT ATSUHITO UNEDA ET AL.
hypotension, were absent, likely because bleeding was not extensive; instead, a vertebral AVF was seen on angiography. Its appearance, together with the sudden onset of severe right neck and shoulder pain after a bout of intense coughing, was interpreted as a sign of aneurysmal rupture, and thus endovascular coil embolization to prevent re-rupture was performed. Patients with NF1 complicated by extracranial vertebral artery aneurysm have been treated surgically (n ¼ 2), with endovascular therapy (n ¼ 14), with both (n ¼ 2), and conservatively (n ¼ 4) (Table 1). Endovascular treatment of a ruptured aneurysm is minimally invasive and of short surgical duration; however, if only the proximal parent artery is occluded, the aneurysm may persist, with recanalization by retrograde flow from the opposite vertebral artery.26 In our patient, flow was high in the fistula; the distal portion of the aneurysm occluded spontaneously, but the major portion of the aneurysm and the vertebral AVF could still be visualized. Thus, endovascular trapping of the aneurysm and proximal vertebral artery was performed, which resulted in successful occlusion of the AVF. The outcomes of patients with aneurysmal ruptures are very poor if bleeding extends into the thoracic cavity.23-25 Of the 10 patients with rupture described in the literature, 4 died or were severely disabled thereafter (Table 1). Therefore, the goal of treatment must be to stop bleeding promptly and prevent re-rupture. CONCLUSION Rupture of an NF1-associated extracranial vertebral artery aneurysm without ensuing cervical hematoma, hemothorax, or hypotension is rare. In our patient, the absence of these symptoms likely can be explained by the relative lack of bleeding after rupture. The differential diagnosis of sudden radiculopathy in a patient with NF1 should include rupture of an extracranial vertebral artery aneurysm, even in the absence of cervical hematoma, hemothorax, or hypotension. In such cases, detection of a vertebral AVF provides a useful clue as to the diagnosis of aneurysmal rupture.
EXTRACRANIAL VA ANEURYSM AND VERTEBRAL AVF ASSOCIATED WITH NF1
REFERENCES 1. Neurofibromatosis. Conference statement, National Institutes of Health Consensus Development Conference. Arch Neurol. 1988;45:575-578. 2. Friedman JM. Epidemiology of neurofibromatosis type 1. Am J Med Genet. 1999;89:1-6. 3. Friedman JM, Arbiser J, Epstein JA, Gutmann DH, Huot SJ, Lin AE, et al. Cardiovascular disease in neurofibromatosis 1: report of the NF1 Cardiovascular Task Force. Genet Med. 2002;4:105-111. 4. Hamilton SJ, Friedman JM. Insights into the pathogenesis of neurofibromatosis 1 vasculopathy. Clin Genet. 2000;58:341-344. 5. Lin AE, Birch PH, Korf BR, Tenconi R, Niimura M, Poyhonen M, et al. Cardiovascular malformations and other cardiovascular abnormalities in neurofibromatosis 1. Am J Med Genet. 2000;95:108-117. 6. Oderich GS, Sullivan TM, Bower TC, Gloviczki P, Miller DV, Babovic-Vuksanovic D, et al. Vascular abnormalities in patients with neurofibromatosis syndrome type I: clinical spectrum, management, and results. J Vasc Surg. 2007;46:475-484. 7. Morasch MD, Phade SV, Naughton P, GarciaToca M, Escobar G, Berguer R. Primary extracranial vertebral artery aneurysms. Ann Vasc Surg. 2013;27:418-423. 8. Vinchon M, Laurian C, George B, D’Arrigo G, Reizine D, Aymard A, et al. Vertebral arteriovenous fistulas: a study of 49 cases and review of the literature. Cardiovasc Surg. 1994;2:359-369.
neurofibromatosis. Endovascular treatment by detachable balloon. Neuroradiology. 1990;31: 533-536. 17. Muhonen MG, Godersky JC, VanGilder JC. Cerebral aneurysms associated with neurofibromatosis. Surg Neurol. 1991;36:470-475. 18. Schievink WI, Piepgras DG. Cervical vertebral artery aneurysms and arteriovenous fistulae in neurofibromatosis type 1: case reports. Neurosurgery. 1991;29:760-765. 19. Ohkata N, Ikota T, Tashiro T, Okamoto K. A case of multiple extracranial vertebral artery aneurysms associated with neurofibromatosis. No Shinkei Geka. 1994;22:637-641 [in Japanese]. 20. Horsley M, Taylor TK, Sorby WA. Tractioninduced rupture of an extracranial vertebral artery aneurysm associated with neurofibromatosis. A case report. Spine (Phila Pa 1976). 1997;22:225-227. 21. Hoffmann KT, Hosten N, Liebig T, Schwarz K, Felix R. Giant aneurysm of the vertebral artery in neurofibromatosis type 1: report of a case and review of the literature. Neuroradiology. 1998;40: 245-248. 22. Ushikoshi S, Goto K, Uda K, Ogata N, Takeno Y. Vertebral arteriovenous fistula that developed in the same place as a previous ruptured aneurysm: a case report. Surg Neurol. 1999;51:168-173. 23. Miyazaki T, Ohta F, Daisu M, Hoshii Y. Extracranial vertebral artery aneurysm ruptured into the thoracic cavity with neurofibromatosis type 1: case report. Neurosurgery. 2004;54:1517-1520 [discussion: 1520-1521].
9. Pereira VM, Geiprasert S, Krings T, Caldas JG, Toulgoat F, Ozanne A, et al. Extracranial vertebral artery involvement in neurofibromatosis type I: report of four cases and literature review. Interv Neuroradiol. 2007;13:315-328.
24. Arai K, Sanada J, Kurozumi A, Watanabe T, Matsui O. Spontaneous hemothorax in neurofibromatosis treated with percutaneous embolization. Cardiovasc Intervent Radiol. 2007;30:477-479.
10. Peyre M, Ozanne A, Bhangoo R, Pereira V, Tadié M, Lasjaunias P, et al. Pseudotumoral presentation of a cervical extracranial vertebral artery aneurysm in neurofibromatosis type 1: case report. Neurosurgery. 2007;61:E658 [discussion: E658].
25. Hieda M, Toyota N, Kakizawa H, Hirai N, Tachikake T, Yahiro Y, et al. Endovascular therapy for massive haemothorax caused by ruptured extracranial vertebral artery aneurysm with neurofibromatosis type 1. Br J Radiol. 2007;80: e81-e84.
11. Schievink WI. Cerebrovascular involvement in Ehlers-Danlos syndrome. Curr Treat Options Cardiovasc Med. 2004;6:231-236.
26. Hiramatsu H, Negoro M, Hayakawa M, Sadatou A, Irie K, Uemura A, et al. Extracranial vertebral artery aneurysm associated with neurofibromatosis type 1: a case report. Interv Neuroradiol. 2007; 13(Suppl 1):90-93.
12. Schievink WI, Michels VV, Piepgras DG. Neurovascular manifestations of heritable connective tissue disorders: a review. Stroke. 1994;25:889-903. 13. Schubiger O, Yasargil MG. Extracranial vertebral aneurysm with neurofibromatosis. Neuroradiology. 1978;15:171-173. 14. Pentecost M, Stanley P, Takahashi M, Isaacs H Jr. Aneurysms of the aorta and subclavian and vertebral arteries in neurofibromatosis. Am J Dis Child. 1981;135:475-477. 15. Detwiler K, Godersky JC, Gentry L. Pseudoaneurysm of the extracranial vertebral artery: case report. J Neurosurg. 1987;67:935-939. 16. Negoro M, Nakaya T, Terashima K, Sugita K. Extracranial vertebral artery aneurysm with
WORLD NEUROSURGERY -: ---, MONTH 2016
27. Horie N, Morikawa M, Kitagawa N, Nakamoto M, Nagata I. Successful endovascular occlusion of an aneurysm of the cervical vertebral artery associated with neurofibromatosis-1. Acta Neurochir (Wien). 2008;150:847-848. 28. Higa G, Pacanowski JP Jr, Jeck DT, Goshima KR, León LR Jr. Vertebral artery aneurysms and cervical arteriovenous fistulae in patients with neurofibromatosis 1. Vascular. 2010;18:166-177. 29. Morvan T, de Broucker F, de Broucker T. Subarachnoid hemorrhage in neurofibromatosis type 1: case report of extracranial cerebral aneurysm rupture into a meningocele. J Neuroradiol. 2011;38: 125-128.
www.WORLDNEUROSURGERY.org
1.E5
CASE REPORT ATSUHITO UNEDA ET AL.
30. Hiramatsu H, Matsui S, Yamashita S, Kamiya M, Yamashita T, Akai K, et al. Ruptured extracranial vertebral artery aneurysm associated with neurofibromatosis type 1. Case report. Neurol Med Chir (Tokyo). 2012;52:446-449. 31. Gouaillier-Vulcain F, Maurel B, Marchand E, Martinez R, Picquet J, Enon B. Successful hybrid management of a left vertebral artery aneurysm secondary to type 1 neurofibromatosis. Ann Vasc Surg. 2014;28:1936.e1-1936.e4. 32. Viskochil D. Genetics of neurofibromatosis 1 and the NF1 gene. J Child Neurol. 2002;17:562-570 [discussion: 571-572, 646-651].
1.E6
www.SCIENCEDIRECT.com
EXTRACRANIAL VA ANEURYSM AND VERTEBRAL AVF ASSOCIATED WITH NF1
33. Riccardi VM. The vasculopathy of NF1 and histogenesis control genes. Clin Genet. 2000;58:345-347. 34. Gao P, Chen Y, Zhang H, Zhang P, Ling F. Vertebral arteriovenous fistulae (AVF) in neurofibromatosis type 1: a report of two cases. Turk Neurosurg. 2013;23:289-293. 35. Deans WR, Bloch S, Leibrock L, Berman BM, Skultety FM. Arteriovenous fistula in patients with neurofibromatosis. Radiology. 1982;144:103-107.
commercial or financial relationships that could be construed as a potential conflict of interest. Received 17 June 2016; accepted 8 September 2016 Citation: World Neurosurg. (2016). http://dx.doi.org/10.1016/j.wneu.2016.09.036 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2016 Elsevier Inc. All rights reserved.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2016.09.036
Neurofibromatosis Type 1eAssociated Extracranial Vertebral Artery Aneurysm Complicated by Vertebral Arteriovenous Fistula After Rupture: Case Report and Literature Review Atsuhito Uneda, Kenta Suzuki, Shuichi Okubo, Koji Hirashita, Masatoshi Yunoki, Kimihiro Yoshino
Key words Aneurysm - Arteriovenous fistula - Neurofibromatosis type 1 - Vertebral artery - von Recklinghausen disease -
Abbreviations and Acronyms AVF: Arteriovenous fistula NF1: Neurofibromatosis type 1 Department of Neurosurgery, Kagawa Rosai Hospital, Marugame, Kagawa, Japan To whom correspondence should be addressed: Atsuhito Uneda, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2016). http://dx.doi.org/10.1016/j.wneu.2016.09.036 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2016 Elsevier Inc. All rights reserved.
INTRODUCTION Neurofibromatosis type 1 (NF1) is an autosomal dominant familial disorder with an incidence of approximately 1 in 3000e4000 individuals.1,2 Vascular abnormalities associated with NF1 reportedly occur in 0.4%e6.4% of patients3-5 and most commonly involve the aorta and renal arteries.6 Both extracranial vertebral artery aneurysm and vertebral arteriovenous fistula (AVF) are relatively rare, and in the majority of cases occur in response to trauma involving the craniocervical region.7,8 Nontraumatic causes include hypertension, infection, inflammatory disease, and inherited disorders, such as Marfan syndrome, EhlerseDanlos syndrome, and NF1.9-12 Craniocervical vascular abnormalities are uncommon manifestations of NF1. Those reported to date include stenosis, occlusion, aneurysm, and AVF,6 whereas extracranial vertebral artery aneurysm is rare.9,10,13-31 Patients with extracranial vertebral artery aneurysm typically present with radiculopathy, neck pain or
- BACKGROUND:
Extracranial vertebral artery aneurysm related to neurofibromatosis type 1 (NF1) is rare. Aneurysmal rupture typically induces such symptoms as cervical hematoma, hemothorax, and hypotension. Here we report a case of ruptured extracranial vertebral artery aneurysm in a patient with NF1 who, rather than cervical hematoma, hemothorax, or hypotension, developed a vertebral arteriovenous fistula (AVF) after aneurysm rupture.
- CASE
DESCRIPTION: A 35-year-old woman with a family history of NF1 presented with sudden-onset right neck and shoulder pain. Computed tomography angiography showed a right extracranial vertebral artery aneurysm. She had neither a cervical hematoma nor hypotension; however, angiography showed an AVF secondary to aneurysmal rupture. The patient was treated with endovascular coil embolization to prevent re-rupture. Postoperatively, her right neck and shoulder pain improved, and she was discharged without further neurologic deficits.
- CONCLUSIONS:
This patient’s clinical course suggests that if there is minimal bleeding from an NF1-associated ruptured extracranial vertebral artery aneurysm, then typical symptoms, such as cervical hematoma, hemothorax, and hypotension, may be absent. Thus, ruptured extracranial vertebral artery aneurysm should be considered in the differential diagnosis of patients with NF1 with sudden-onset radiculopathy, even in the absence of typical symptoms. The detection of a vertebral AVF provides a useful clue to the diagnosis of aneurysm rupture in such cases.
neck mass, and—in those with rupture— cervical hematoma, hemothorax, or hypotension. There have only been 2 reported cases of extracranial vertebral artery aneurysm associated with NF1 in which the AVF was detected at the same time as the aneurysm.28,29 Here we report a patient with NF1 who presented with a ruptured extracranial vertebral artery aneurysm, the sole manifestation of which was a vertebral AVF rather than the more common symptoms of cervical hematoma, hemothorax or hypotension. To the best of our knowledge, this is the first description of a patient with a ruptured extracranial vertebral artery aneurysm associated with NF1 in whom these symptoms were absent. We discuss our findings in the context of a literature review
WORLD NEUROSURGERY -: ---, MONTH 2016
of NF1-associated extracranial vertebral artery aneurysms. CASE REPORT A 35-year-old woman with a paternal family history of NF1 presented to our hospital complaining of severe right neck and shoulder pain that had begun suddenly after a bout of intense coughing starting 5 days earlier. She was fully conscious, and clinical examination revealed no evidence of cervical hematoma, no cervical bruit, and normal blood pressure. Multiple fibromas and café au lait spots were visible on her chest and abdomen. Radiologic Findings Cervical T2-weighted magnetic resonance imaging showed a round hypointense
www.WORLDNEUROSURGERY.org
1.E1
CASE REPORT ATSUHITO UNEDA ET AL.
EXTRACRANIAL VA ANEURYSM AND VERTEBRAL AVF ASSOCIATED WITH NF1
Figure 1. (A) Axial T2-weighted magnetic resonance imaging showing a hypointense mass compressing the right C3 nerve root. (B) Neck 3-dimensional computed tomography angiography showing an aneurysm of 15 mm diameter in the C3eC4 segment of the right cervical vertebral artery. (C) Axial computed tomography scan showing enlargement of the C3eC4 intravertebral foramen owing to bony erosion by the aneurysm. (D) A lateral view obtained on right vertebral angiography showing an aneurysm in the C3eC4 segment of the right cervical vertebral artery and a right vertebral arteriovenous fistula draining into the spinal venous system. (E) Anteroposterior view on left vertebral artery angiography showing retrograde filling of the right distal vertebral artery and aneurysm.
mass compressing the right third cervical nerve root (Figure 1A). A flow void inside the mass suggested a vascular lesion. Three-dimensional computed tomography angiography of the neck revealed a right cervical vertebral artery aneurysm at the level of C3eC4 with a diameter of 15 mm (Figure 1B). Enlargement of the C3eC4 intravertebral foramen owing to bony erosion by the aneurysm was also observed (Figure 1C). The patient’s symptoms were attributed
to radiculopathy of the right C3 nerve root. At 4 days after admission, the patient underwent right vertebral angiography via the right femoral artery. The aneurysm in the right cervical vertebral artery at the C3eC4 segment and a vertebral AVF that had likely developed subsequent to aneurysmal rupture were identified (Figure 1D). A 5-Fr ENVOY guiding catheter (Codman, Miami, Florida, USA) was advanced into the proximal
right vertebral artery via the right femoral artery, followed by a Scepter XC balloon catheter (Microvention, Tustin, California, USA), as far as the C5eC6 intervertebral space. A balloon occlusion test of the proximal right cervical vertebral artery was performed for 15 minutes. Left vertebral angiography from a 4-Fr diagnostic catheter placed in the left vertebral artery via the left femoral artery showed the right distal vertebral artery and the aneurysm in retrograde (Figure 1E). The
Figure 2. (A) Lateral view on preoperative right vertebral angiography showing the spontaneous occlusion of the distal portion of the aneurysm, with the major portion of the aneurysm and the vertebral arteriovenous fistula (AVF) still visualized. (B) Anteroposterior view on preoperative left vertebral angiography showing the right distal vertebral artery in retrograde, without visualization of the aneurysm or AVF. (C) Anteroposterior view on postoperative right vertebral angiography confirming successful occlusion of the cervical vertebral artery aneurysm and AVF. (Left) Precontrast. (Right) Subtracted. (D) Lateral view on postoperative right vertebral angiography. (Left) Precontrast. (Right) Subtracted.
1.E2
www.SCIENCEDIRECT.com
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2016.09.036
Case
Age (years)/ Sex
Author (year)
Side
Level
Symptoms
Ruptured or Unruptured
AVF
Outcome and Follow-Up
Treatment
1
Schubiger and Yasargil (1978)13
50/Male
Left
C2eC6
Radiculopathy
Unruptured
Direct surgery
GR
2
Pentecost et al. (1981)14
1/Female
Left
Th1
Limited neck movement, arm weakness
Unruptured
Observation
SD (intraoperative bleeding of other aneurysm)
3
Detwiler et al. (1987)15
52/Female
Left
C2
Neck mass, neck pain, bruits
Unruptured
Endovascular (balloon)
GR
4
Negoro et al. (1990)16
47/Male
Left
C1
Neck pain, cervical hematoma
Ruptured
Endovascular (balloon)
GR
5
Muhonen et al. (1991)
52/Female
Left
C2
Neck mass, neck pain, arm weakness
Unruptured
Endovascular (balloon)
GR
6
Schievink and Piepgras (1991)18
43/Female
Left
C7
No symptoms
Unruptured
Observation
GR
7
Ohkata et al. (1994)19
48/Female
Left
C4eC7
Radiculopathy
Unruptured
Direct surgery
GR
8
Horsley et al. (1997)20
56/Female
Left
C5eC7
Neck pain, arm paresthesias, neck mass
Ruptured
Endovascular (coil)
GR
17
Hoffmann et al. (1998)
59/Male
Right
C6
None
Unruptured
Observation
GR
10
Ushikoshi et al. (1999)22
40/Female
Left
C1
Occipitalgia, cervical hematoma
Ruptured
Secondary AVF at the same site 11 years later
Endovascular (balloon)
GR
11
Miyazaki et al. (2004)23
52/Female
Left
C5eC7
Radiculopathy, hypotension, altered consciousness, hemothorax
Ruptured
Endovascular (balloon), direct surgery
D
12
Arai et al. (2007)24
38/Male
Left
NR
Chest pain, dizziness, vomiting, hemothorax
Ruptured
Untreated
D
13
Hieda et al. (2007)25
36/Female
Left
Ostium of vertebral artery
Back pain, chest pain, dyspnea, hypotension, hemothorax, coma
Ruptured
Endovascular (coil, NBCA)
D
14
Hiramatsu et al. (2007)26
67/Male
Left
Proximal segment of vertebral artery (V1)
Dizziness
Unruptured
Endovascular (coil)
GR
15
Pereira et al. (2007)9
Endovascular (balloon)
GR
16
14/Female
Right
C5eC6
Radiculopathy
Unruptured
10
18/Female
Right
C5eC6
Radiculopathy
Unruptured
Endovascular (coil)
GR
27
Peyre et al. (2007) Horie et al. (2008)
30/Female
Right
C6eC7
Radiculopathy
Unruptured
Endovascular (coil, balloon)
GR
18
Higa et al. (2010)28
60/Female
Left
NR
Cervical hematoma, stridor, respiratory failure
Ruptured
þ
Endovascular (coil)
SD (after 3 months, ventilator-dependent)
19
Morvan et al. (2011)29
36/Female
Left
C3eC4
Headache, neck pain, vomiting, subarachnoid hemorrhage
Ruptured
þ
Endovascular (coil, stent)
NR
AVF, arteriovenous fistula; D, death; GR, good recovery; NR, not reported; SD, severely disabled. Continues
CASE REPORT
1.E3
17
EXTRACRANIAL VA ANEURYSM AND VERTEBRAL AVF ASSOCIATED WITH NF1
www.WORLDNEUROSURGERY.org
9
21
ATSUHITO UNEDA ET AL.
WORLD NEUROSURGERY -: ---, MONTH 2016
Table 1. Reported Cases of Extracranial Vertebral Artery Aneurysm Associated With NF1, Including Our Case
CASE REPORT ATSUHITO UNEDA ET AL.
EXTRACRANIAL VA ANEURYSM AND VERTEBRAL AVF ASSOCIATED WITH NF1
1.E4
Endovascular (coil) þ
GR
Direct surgery, endovascular (stent)
GR
Endovascular (coil)
AVF, arteriovenous fistula; D, death; GR, good recovery; NR, not reported; SD, severely disabled.
Ruptured C3eC4 Right 35/Female 22
Present case
C8 32/Male 21
Gouaillier-Vulcain et al. (2014)31
Left
Radiculopathy
Unruptured Radiculopathy
Ruptured Neck pain, cervical hematoma, radiculopathy C6 Right 31/Male Hiramatsu et al. (2012)30 20
Author (year) Case
Table 1. Continued
Age (years)/ Sex
Side
Level
Symptoms
Ruptured or Unruptured
AVF
Treatment
GR
Outcome and Follow-Up
patient reported no neurologic deficits during occlusion.
www.SCIENCEDIRECT.com
Treatment At 6 days after admission, the patient underwent endovascular coil embolization to prevent re-rupture of the aneurysm. A 7-Fr Optimo balloon catheter (Tokai Medical Products, Kasugai, Japan) was placed via the right femoral artery into the proximal right vertebral artery. Preoperative right vertebral angiography from a 7-Fr Optimo balloon catheter showed spontaneous occlusion of the distal portion of the aneurysm, but the major portion of the aneurysm and the vertebral AVF were still evident (Figure 2A). Left vertebral angiography from a 4-Fr diagnostic catheter placed via the left femoral artery into the left vertebral artery showed the right distal vertebral artery in retrograde, without visualization of the aneurysm or the AVF (Figure 2B). An Excelsior SL-10 microcatheter (Stryker Neurovascular, Fremont, California, USA) was inserted through the Optimo balloon catheter, so that its tip lay within the aneurysmal cavity. Endovascular trapping with 10 Target XL detachable coils (Stryker), and 5 Orbit Galaxy detachable coils (Codman) was performed from the distal aneurysmal neck to the proximal vertebral artery. Neither the aneurysm nor the AVF could be visualized during postoperative angiography of the right vertebral artery (Figure 2C and D). Postoperative angiography of the left vertebral artery demonstrated adequate flow in the basilar artery and retrograde flow into the right vertebral artery, without visualization of the aneurysm or AVF. Postoperative Course and Follow-up The patient reported an improvement in her right neck and shoulder pain, and experienced no further neurologic deficits. She was discharged on aspirin 100 mg once daily and clopidogrel 75 mg once daily. Follow-up angiography performed 3 months after surgery confirmed no recurrence of the right cervical vertebral artery aneurysm or AVF. DISCUSSION NF1, also known as von Recklinghausen disease, is an autosomal dominant familial
disorder caused by mutations of the NF1 gene, located on the long arm of chromosome 17 (17q11.2).32 Neurofibromin, the protein product of the NF1 gene, functions in part as a negative regulator of the p21 Ras proto-oncogene.32 The loss of neurofibromin expression results in increased mitogenic signaling and thus increased cell growth, which in turn facilitates tumor formation.32 Vascular abnormalities associated with NF1 are rare and may reflect disruption of the vascular maintenance and repair regulated by neurofibromin.33 In a literature search, we found 22 cases of extracranial vertebral artery aneurysm associated with NF1 (Table 1).9,10,13-31 Rupture occurred in 10 of these cases, as in our patient, whereas rupture was not reported in 12 cases. The mean age at diagnosis was 41 years (range, 1e67 years). The majority of aneurysms occurred on the left side (16:6) and in women (15:7). Patients typically presented with radiculopathy, neck pain, or neck mass; in those with rupture, cervical hematoma, hemothorax, or hypotension was the characteristic presenting symptom. More than 30 cases of vertebral AVF associated with NF1 have been reported to date,28,34 whereas vertebral AVF combined with extracranial vertebral artery aneurysm associated with NF1 is very unusual. A literature review uncovered only 3 other cases (Table 1). Including our patient, the aneurysm ruptured in all 4 cases, and the AVF was detected in the extracranial vertebral artery at the same time as the aneurysm in 3 cases (including ours).28,29 In 1 patient, the vertebral AVF developed at the site of the aneurysm 11 years after rupture.22 Deans et al.35 suggested 2 mechanisms by which an AVF might arise in a patient with NF1, either by rupture of a preexisting extracranial vertebral artery aneurysm into the vertebral venous plexus, or congenitally as a manifestation of mesodermal dysplasia.35 Alternatively, a flow-related aneurysm-like dilatation of vertebral artery might arise proximal to a preexisting AVF.35 In aneurysmal rupture leading to AVF, the onset of symptoms is generally acute,28,29 whereas in flowrelated aneurysm-like dilatation of the artery proximal to the AVF, symptoms are usually progressive.35 In our patient, typical symptoms of rupture, especially cervical hematoma or
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2016.09.036
CASE REPORT ATSUHITO UNEDA ET AL.
hypotension, were absent, likely because bleeding was not extensive; instead, a vertebral AVF was seen on angiography. Its appearance, together with the sudden onset of severe right neck and shoulder pain after a bout of intense coughing, was interpreted as a sign of aneurysmal rupture, and thus endovascular coil embolization to prevent re-rupture was performed. Patients with NF1 complicated by extracranial vertebral artery aneurysm have been treated surgically (n ¼ 2), with endovascular therapy (n ¼ 14), with both (n ¼ 2), and conservatively (n ¼ 4) (Table 1). Endovascular treatment of a ruptured aneurysm is minimally invasive and of short surgical duration; however, if only the proximal parent artery is occluded, the aneurysm may persist, with recanalization by retrograde flow from the opposite vertebral artery.26 In our patient, flow was high in the fistula; the distal portion of the aneurysm occluded spontaneously, but the major portion of the aneurysm and the vertebral AVF could still be visualized. Thus, endovascular trapping of the aneurysm and proximal vertebral artery was performed, which resulted in successful occlusion of the AVF. The outcomes of patients with aneurysmal ruptures are very poor if bleeding extends into the thoracic cavity.23-25 Of the 10 patients with rupture described in the literature, 4 died or were severely disabled thereafter (Table 1). Therefore, the goal of treatment must be to stop bleeding promptly and prevent re-rupture. CONCLUSION Rupture of an NF1-associated extracranial vertebral artery aneurysm without ensuing cervical hematoma, hemothorax, or hypotension is rare. In our patient, the absence of these symptoms likely can be explained by the relative lack of bleeding after rupture. The differential diagnosis of sudden radiculopathy in a patient with NF1 should include rupture of an extracranial vertebral artery aneurysm, even in the absence of cervical hematoma, hemothorax, or hypotension. In such cases, detection of a vertebral AVF provides a useful clue as to the diagnosis of aneurysmal rupture.
EXTRACRANIAL VA ANEURYSM AND VERTEBRAL AVF ASSOCIATED WITH NF1
REFERENCES 1. Neurofibromatosis. Conference statement, National Institutes of Health Consensus Development Conference. Arch Neurol. 1988;45:575-578. 2. Friedman JM. Epidemiology of neurofibromatosis type 1. Am J Med Genet. 1999;89:1-6. 3. Friedman JM, Arbiser J, Epstein JA, Gutmann DH, Huot SJ, Lin AE, et al. Cardiovascular disease in neurofibromatosis 1: report of the NF1 Cardiovascular Task Force. Genet Med. 2002;4:105-111. 4. Hamilton SJ, Friedman JM. Insights into the pathogenesis of neurofibromatosis 1 vasculopathy. Clin Genet. 2000;58:341-344. 5. Lin AE, Birch PH, Korf BR, Tenconi R, Niimura M, Poyhonen M, et al. Cardiovascular malformations and other cardiovascular abnormalities in neurofibromatosis 1. Am J Med Genet. 2000;95:108-117. 6. Oderich GS, Sullivan TM, Bower TC, Gloviczki P, Miller DV, Babovic-Vuksanovic D, et al. Vascular abnormalities in patients with neurofibromatosis syndrome type I: clinical spectrum, management, and results. J Vasc Surg. 2007;46:475-484. 7. Morasch MD, Phade SV, Naughton P, GarciaToca M, Escobar G, Berguer R. Primary extracranial vertebral artery aneurysms. Ann Vasc Surg. 2013;27:418-423. 8. Vinchon M, Laurian C, George B, D’Arrigo G, Reizine D, Aymard A, et al. Vertebral arteriovenous fistulas: a study of 49 cases and review of the literature. Cardiovasc Surg. 1994;2:359-369.
neurofibromatosis. Endovascular treatment by detachable balloon. Neuroradiology. 1990;31: 533-536. 17. Muhonen MG, Godersky JC, VanGilder JC. Cerebral aneurysms associated with neurofibromatosis. Surg Neurol. 1991;36:470-475. 18. Schievink WI, Piepgras DG. Cervical vertebral artery aneurysms and arteriovenous fistulae in neurofibromatosis type 1: case reports. Neurosurgery. 1991;29:760-765. 19. Ohkata N, Ikota T, Tashiro T, Okamoto K. A case of multiple extracranial vertebral artery aneurysms associated with neurofibromatosis. No Shinkei Geka. 1994;22:637-641 [in Japanese]. 20. Horsley M, Taylor TK, Sorby WA. Tractioninduced rupture of an extracranial vertebral artery aneurysm associated with neurofibromatosis. A case report. Spine (Phila Pa 1976). 1997;22:225-227. 21. Hoffmann KT, Hosten N, Liebig T, Schwarz K, Felix R. Giant aneurysm of the vertebral artery in neurofibromatosis type 1: report of a case and review of the literature. Neuroradiology. 1998;40: 245-248. 22. Ushikoshi S, Goto K, Uda K, Ogata N, Takeno Y. Vertebral arteriovenous fistula that developed in the same place as a previous ruptured aneurysm: a case report. Surg Neurol. 1999;51:168-173. 23. Miyazaki T, Ohta F, Daisu M, Hoshii Y. Extracranial vertebral artery aneurysm ruptured into the thoracic cavity with neurofibromatosis type 1: case report. Neurosurgery. 2004;54:1517-1520 [discussion: 1520-1521].
9. Pereira VM, Geiprasert S, Krings T, Caldas JG, Toulgoat F, Ozanne A, et al. Extracranial vertebral artery involvement in neurofibromatosis type I: report of four cases and literature review. Interv Neuroradiol. 2007;13:315-328.
24. Arai K, Sanada J, Kurozumi A, Watanabe T, Matsui O. Spontaneous hemothorax in neurofibromatosis treated with percutaneous embolization. Cardiovasc Intervent Radiol. 2007;30:477-479.
10. Peyre M, Ozanne A, Bhangoo R, Pereira V, Tadié M, Lasjaunias P, et al. Pseudotumoral presentation of a cervical extracranial vertebral artery aneurysm in neurofibromatosis type 1: case report. Neurosurgery. 2007;61:E658 [discussion: E658].
25. Hieda M, Toyota N, Kakizawa H, Hirai N, Tachikake T, Yahiro Y, et al. Endovascular therapy for massive haemothorax caused by ruptured extracranial vertebral artery aneurysm with neurofibromatosis type 1. Br J Radiol. 2007;80: e81-e84.
11. Schievink WI. Cerebrovascular involvement in Ehlers-Danlos syndrome. Curr Treat Options Cardiovasc Med. 2004;6:231-236.
26. Hiramatsu H, Negoro M, Hayakawa M, Sadatou A, Irie K, Uemura A, et al. Extracranial vertebral artery aneurysm associated with neurofibromatosis type 1: a case report. Interv Neuroradiol. 2007; 13(Suppl 1):90-93.
12. Schievink WI, Michels VV, Piepgras DG. Neurovascular manifestations of heritable connective tissue disorders: a review. Stroke. 1994;25:889-903. 13. Schubiger O, Yasargil MG. Extracranial vertebral aneurysm with neurofibromatosis. Neuroradiology. 1978;15:171-173. 14. Pentecost M, Stanley P, Takahashi M, Isaacs H Jr. Aneurysms of the aorta and subclavian and vertebral arteries in neurofibromatosis. Am J Dis Child. 1981;135:475-477. 15. Detwiler K, Godersky JC, Gentry L. Pseudoaneurysm of the extracranial vertebral artery: case report. J Neurosurg. 1987;67:935-939. 16. Negoro M, Nakaya T, Terashima K, Sugita K. Extracranial vertebral artery aneurysm with
WORLD NEUROSURGERY -: ---, MONTH 2016
27. Horie N, Morikawa M, Kitagawa N, Nakamoto M, Nagata I. Successful endovascular occlusion of an aneurysm of the cervical vertebral artery associated with neurofibromatosis-1. Acta Neurochir (Wien). 2008;150:847-848. 28. Higa G, Pacanowski JP Jr, Jeck DT, Goshima KR, León LR Jr. Vertebral artery aneurysms and cervical arteriovenous fistulae in patients with neurofibromatosis 1. Vascular. 2010;18:166-177. 29. Morvan T, de Broucker F, de Broucker T. Subarachnoid hemorrhage in neurofibromatosis type 1: case report of extracranial cerebral aneurysm rupture into a meningocele. J Neuroradiol. 2011;38: 125-128.
www.WORLDNEUROSURGERY.org
1.E5
CASE REPORT ATSUHITO UNEDA ET AL.
30. Hiramatsu H, Matsui S, Yamashita S, Kamiya M, Yamashita T, Akai K, et al. Ruptured extracranial vertebral artery aneurysm associated with neurofibromatosis type 1. Case report. Neurol Med Chir (Tokyo). 2012;52:446-449. 31. Gouaillier-Vulcain F, Maurel B, Marchand E, Martinez R, Picquet J, Enon B. Successful hybrid management of a left vertebral artery aneurysm secondary to type 1 neurofibromatosis. Ann Vasc Surg. 2014;28:1936.e1-1936.e4. 32. Viskochil D. Genetics of neurofibromatosis 1 and the NF1 gene. J Child Neurol. 2002;17:562-570 [discussion: 571-572, 646-651].
1.E6
www.SCIENCEDIRECT.com
EXTRACRANIAL VA ANEURYSM AND VERTEBRAL AVF ASSOCIATED WITH NF1
33. Riccardi VM. The vasculopathy of NF1 and histogenesis control genes. Clin Genet. 2000;58:345-347. 34. Gao P, Chen Y, Zhang H, Zhang P, Ling F. Vertebral arteriovenous fistulae (AVF) in neurofibromatosis type 1: a report of two cases. Turk Neurosurg. 2013;23:289-293. 35. Deans WR, Bloch S, Leibrock L, Berman BM, Skultety FM. Arteriovenous fistula in patients with neurofibromatosis. Radiology. 1982;144:103-107.
commercial or financial relationships that could be construed as a potential conflict of interest. Received 17 June 2016; accepted 8 September 2016 Citation: World Neurosurg. (2016). http://dx.doi.org/10.1016/j.wneu.2016.09.036 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2016 Elsevier Inc. All rights reserved.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2016.09.036