Revascularization of the internal carotid artery through the hypertrophied vasa vasorum in traumatic carotid-cavernous fistula previously treated by ligation of cervical carotid arteries: A case report
- Department of Neurosurgery, Neurological Institute of Thailand, Thailand.
- Department of Neuroradiology, Neurological Institute of Thailand, Thailand.
- Department of Radiology, Bumrungrad International Hospital, Bangkok, Thailand.
Prasert Iampreechakul, Department of Neurosurgery, Neurological Institute of Thailand, 312, Ratchawithi Road, Khwaeng Thung Phaya Thai, Bangkok, Thailand.
DOI:10.25259/SNI_450_2022Copyright: © 2022 Surgical Neurology International This is an open-access article distributed under the terms of the Creative Commons Attribution-Non Commercial-Share Alike 4.0 License, which allows others to remix, transform, and build upon the work non-commercially, as long as the author is credited and the new creations are licensed under the identical terms.
How to cite this article: Prasert Iampreechakul1, Korrapakc Wangtanaphat1, Punjama Lertbutsayanukul2, Somkiet Siriwimonmas3. Revascularization of the internal carotid artery through the hypertrophied vasa vasorum in traumatic carotid-cavernous fistula previously treated by ligation of cervical carotid arteries: A case report. 29-Jul-2022;13:324
How to cite this URL: Prasert Iampreechakul1, Korrapakc Wangtanaphat1, Punjama Lertbutsayanukul2, Somkiet Siriwimonmas3. Revascularization of the internal carotid artery through the hypertrophied vasa vasorum in traumatic carotid-cavernous fistula previously treated by ligation of cervical carotid arteries: A case report. 29-Jul-2022;13:324. Available from: https://surgicalneurologyint.com/surgicalint-articles/11754/
Background: Revascularization of the occluded internal carotid artery (ICA) through the vasa vasorum is exceedingly rare. Several previous studies hypothesized that the expansion of the vasa vasorum is associated with neovascularization related to the progression of atherosclerosis or plaque. The occurrence of reconstitution of the ICA through the vasa vasorum in traumatic carotid-cavernous fistula (TCCF) has rarely been reported.
Case Description: We described an extremely rare case of a 64-year-old woman who developed reconstitution of the occluded ICA through hypertrophied vasa vasorum supplying recurrent TCCF previously treated by ligation of the internal and external carotid arteries. Usual endovascular treatment may be challenging for this patient due to inaccessible route from the affected ICA through multiple small vessels. The patient was successfully treated with trapping procedure and obliteration the fistula using combined surgical and endovascular treatment.
Conclusion: We speculated that the hypertrophied vasa vasorum in TCCF may cause by a sequela of previous arterial injury, spontaneous recanalization of the occluded artery by the formation of vasa vasorum, and/or hypertrophy of the vasa vasorum due to the high flow of the fistula.
Keywords: Carotid artery ligation, Direct carotid-cavernous fistula, Trapping procedure, Traumatic carotid-cavernous fistula, Vasa vasorum
Following complete occlusion of the internal carotid artery (ICA), recanalization through the vasa vasorum is extremely rare.[
A 64-year-old woman was admitted to the local hospital due to seizure with transient loss of consciousness. She complained of headache and mild cognitive impairment for the past 1 year. Cranial computed tomography (CT) scan and magnetic resonance imaging revealed markedly dilatation of the left cavernous sinus (CS), sphenoparietal sinus, and cortical veins along left cerebral hemisphere. There was some venous wall calcification [
(a-d) Sequential axial images of non-contrast computed tomography scan, and (e and f) axial and (g) sagittal T2-weighted magnetic resonance images of the brain reveal markedly enlarged left sphenoparietal sinus and cortical veins along left cerebral hemisphere. There is some venous wall calcification. (h) Photograph of the patient’s left-sided neck in oblique view shows the previous surgical scar.
Cerebral angiography was performed before treatment. The left common carotid artery injection showed no existence of the external carotid artery, severe stenosis of the proximal ICA, and long segment of multiple small vascular channels, probably representing the revascularization of the left occluded ICA through vasa vasorum, at C3 to C4 vertebral level. There was a direct high-flow fistula between the cavernous segment of the left ICA and the CS with retrograde venous drainage into markedly dilated left sphenoparietal sinus, superficial middle cerebral vein, superior sagittal sinus through the vein of Trolard, and the left transverse sinus through the vein of Labbé [
Cerebral angiography before treatment. (a) Anteroposterior (AP) and (b) lateral views of the left common carotid artery, (c) AP view of the right internal carotid artery (ICA), and (d) lateral views of the left vertebral artery with (e) 3D reconstruction angiographic computerized tomography reveal the left direct high-flow carotid-cavernous fistula supplied by the contralateral ICA through the anterior communicating artery, vertebrobasilar system through posterior communicating artery, and ipsilateral ICA through multiple small vascular channels, representing the revascularization of the left ICA through vasa vasorum, at the level of C3-C4. The venous drainage exclusively drains into markedly dilated tortuous cortical veins along left cerebral hemisphere. There is no existence of the left external carotid artery.
3D reconstruction images in (a) anterior, (b) posterior, (c) right lateral, and (d) left lateral views, and maximum intensity projection reformatted images in (e) axial, (f) sagittal, and (g) coronal views of angiographic computerized tomography of the left common carotid artery clearly demonstrate multiple small serpiginous vessels, hypertrophied vasa vasorum, projecting over expected course of the internal carotid artery (ICA) with antegrade filling of the distal ICA.
The patient underwent balloon occlusion test before treatment and could tolerate the vessel occlusion. Under general anesthesia and heparinization, transarterial detachable balloon embolization was attempted but the detachable balloon catheter could not be advanced into the fistula through ACoA from the right ICA, and PCoA from the VA. Then, the microcatheter was navigated into the fistula through ACoA from the right ICA. The largest GDC coil was attempted to place into the fistula, but the retrograde shunt into the fistula was so great that the coils mass was unable and kept migrating into the large venous pouch. Subsequently, the microcatheter was advanced further into the petrous segment of the left ICA proximal to the fistula which was occluded with Axium Detachable coils (Medtronic, Minneapolis, Minnesota, USA). Then, transarterial coil embolization was attempted at left supraclinoid ICA, but it was failed. The decision was made to proceed with surgery by clipping of the left supraclinoid ICA distal to the fistula.
On the following day, the patient underwent the left frontotemporal craniotomy. Anterior clinoidectomy was subsequently performed because it was difficult to place the clip on the ICA due to the large arterialized venous pouch. The clinoidal segment of the left ICA was clipped by the fenestrated clip encircling the left optic nerve. In addition, the left ophthalmic artery was clipped by another clip. Postoperative course of the patient was uneventful.
One month after surgery, cerebral angiography was obtained and revealed the remaining of severe stenosis of the proximal ICA with associated vasa vasorum and reduction in shunt flow and size of the dilated draining vein along the left cerebral hemisphere. In addition, the fistula received additional supply from the contralateral ICA and left VA. Prowler Plus microcatheter (Codman Neurovascular, Raynham, MA, USA) was used over the Agility Steerable guidewire (0.016 soft, Codman Neurovascular, Raynham, MA, USA) was successfully advanced into the fistula through the small recanalized limen of the left ICA. Embolization was performed with multiple fibered interlocking detachable coils (Interlock-35, Boston Scientific, Natick, MA). Post embolization angiography showed nearly obliteration of the fistula. Post embolization course of the patient was uneventful. Follow-up cerebral angiography, obtained 1 year after the second embolization, confirmed no recurrence of the fistula [
Cerebral angiography obtained 1 year after treatment. (a) Anteroposterior (AP) and (b) lateral views of the left common carotid artery, (c) AP view of the right internal carotid artery, and (d) lateral views of the left vertebral artery injections confirm complete obliteration of the fistula.
The vasa vasorum is a network of microvessels located in the adventitia of vessel wall of mid-to large-sized arteries. It supplies oxygen and necessary nutrients to the adventitia and the outer media of the arterial wall. On the other hand, the intima and inner media are nourished by direct diffusion of blood nutrients from the arterial lumen.[
The network of vasa vasorum surrounding atherosclerotic plaque may originate from the superior thyroid, ascending pharyngeal, common carotid, internal carotid, and external carotid arteries and fills up into the more distal ICA beyond the occlusion site.[
Interestingly, when the ICA contains marked atherosclerotic plaque, the vasa vasorum may arise directly from lumen of the ICA distal to atherosclerotic plaque and pass inferiorly into network of the vasa vasorum.[
In non-arteriosclerotic cause, such as carotid artery dissecting aneurysm, and tumor, an occluded ICA might be recanalized through the vasa vasorum.[
Our case was the fourth case of TCCF supplied by the affected ICA through hypertrophied vasa vasorum. The patient underwent previous ligation of internal and external carotid arteries. We speculated that the fistula may remain persist or recur and the draining veins may reroute into cortical veins. Without other neurological symptoms and follow-up cerebral angiography, TCCF may sustain for more than 20 years until her seizure developed. The enormously draining veins and venous wall calcification may represent the presence of a long-standing fistula.
Following the occlusion of the ICA, revascularization of an occluded ICA may be explained by two possible mechanisms including luminal recanalization or reconstitution by a hypertrophied vasa vasorum, a source of collateral circulation.[
In our case, we speculated that the rete mirabile-like arterial lesions of the left subpetrosal cervical ICA may cause by a combination of few factors including a sequela of previous arterial injury, spontaneous recanalization of the occluded artery by the formation of vasa vasorum, and hypertrophy of the vasa vasorum due to the high flow of the fistula.
The preferred access to the CS is certainly the affected ICA by transarterial route. Patients harboring TCCF with the previous occlusion of the affected ICA could not be successfully treated by standard endovascular techniques alone. These such cases may be cured by combining a surgical approach and endovascular technique, as shown in our case. Other options for the management of recurrent TCCF after surgical occlusion of the affected ICA have been previously reported.[
It is well known that the proliferation or expansion of the vasa vasorum may occur during the progression of atherosclerosis. We reported the fourth case of recurrent TCCF developing the supply from the vasa vasorum after ligation of the affected ICA. We speculated that the hypertrophied vasa vasorum in TCCF may cause by a sequela of the previous arterial injury, spontaneous recanalization of the occluded artery by the formation of vasa vasorum, and/or hypertrophy of the vasa vasorum due to the high flow of the fistula. From our review, antegrade recanalization through the vasa vasorum may occur following parent artery occlusion by endovascular coiling or balloon.
The authors certify that they have obtained all appropriate patient consent.
There are no conflicts of interest.
1. Baik SK, Park J, Kim GC, Lee TH, Kim YS. Vascular response to the vasa vasorum in a carotid artery dissecting aneurysm. Acta Neurochir (Wien). 2009. 151: 1159-61
2. Bayer IM, Caniggia I, Adamson SL, Langille BL. Experimental angiogenesis of arterial vasa vasorum. Cell Tissue Res. 2002. 307: 303-13
3. Bo WJ, McKinney WM, Bowden RL. The origin and distribution of vasa vasorum at the bifurcation of the common carotid artery with atherosclerosis. Stroke. 1989. 20: 1484-7
4. Chng SM, Alvarez H, Marsot-Dupuch K, Mercier P, Lasjaunias P. “Duplicated” or “multiple” cervical internal carotid and vertebral arteries from fenestration, duplication and vasa vasorum to segmental rete. Interv Neuroradiol. 2004. 10: 301-7
5. Cho HJ, Roh HG, Chun YI, Moon CT, Chung HW, Kim HY. Hypertrophy of the vasa vasorum: Vascular response to the hungry brain. Neurologist. 2012. 18: 133-5
6. Coley SC, Pandya H, Hodgson TJ, Jeffree MA, Deasy NP. Endovascular trapping of traumatic carotid-cavernous fistulae. AJNR Am J Neuroradiol. 2003. 24: 1785-8
7. Colon GP, Deveikis JP, Dickinson LD. Revascularization of occluded internal carotid arteries by hypertrophied vasa vasorum: Report of four cases. Neurosurgery. 1999. 45: 634-7
8. Debrun GM, Nauta HJ, Miller NR, Drake CG, Heros RC, Ahn HS. Combining the detachable balloon technique and surgery in imaging carotid cavernous fistulae. Surg Neurol. 1989. 32: 3-10
9. Garcia-Cervigon E, Bien S, Laurent A, Weitzner I, Biondi A, Merland JJ. Treatment of a recurrent traumatic carotid-cavernous fistula: Vertebro-basilar approach after surgical occlusion of the internal carotid artery. Neuroradiology. 1988. 30: 355-7
10. Halbach VV, Higashida RT, Hieshima GB, Hardin CW. Direct puncture of the proximally occluded internal carotid artery for treatment of carotid cavernous fistulas. AJNR Am J Neuroradiol. 1989. 10: 151-4
11. Kapp JP, Pattisapu JR, Parker JL. Transarterial closure of persistent carotid-cavernous fistula after carotid ligation. Case report. J Neurosurg. 1984. 61: 402-4
12. Kemény V, Droste DW, Nabavi DG, Schulte-Altedorneburg G, Schuierer G, Ringelstein EB. Collateralization of an occluded internal carotid artery via a vas vasorum. Stroke. 1998. 29: 521-3
13. Martin MA, Marotta TR. Vasa vasorum: Another cause of the carotid string sign. AJNR Am J Neuroradiol. 1999. 20: 259-62
14. Meguro T, Muraoka K, Terada K, Hirotsune N, Nishino S. Recanalisation of the internal carotid artery via the vasa vasorum after coil occlusion. Br J Radiol. 2011. 84: e23-6
15. Numagami Y, Ezura M, Takahashi A, Yoshimoto T. Antegrade recanalization of completely embolized internal carotid artery after treatment of a giant intracavernous aneurysm: A case report. Surg Neurol. 1999. 52: 611-6
16. O’Reilly GV, Shillito J, Haykal HA, Kleefield J, Wang AM, Rumbaugh CL. Balloon occlusion of a recurrent carotid-cavernous fistula previously treated by carotid ligations. Neurosurgery. 1986. 19: 643-8
17. Sedding DG, Boyle EC, Demandt JAF, Sluimer JC, Dutzmann J, Haverich A. Vasa Vasorum angiogenesis: Key player in the initiation and progression of atherosclerosis and potential target for the treatment of cardiovascular disease. Front Immunol. 2018. 9: 706
18. Teng MM, Guo WY, Lee LS, Chang T. Direct puncture of the cavernous sinus for obliteration of a recurrent carotid-cavernous fistula. Neurosurgery. 1988. 23: 104-7