- Email: [email protected]
Trigeminal neuralgia due to arterialization of the superior petrosal vein in the context of dural or cerebral arteriovenous shunt
Accepted Manuscript Title: Trigeminal Neuralgia due to Arterialization of the Superior Petrosal Vein in the Context of Dural or Cerebral Arteriovenous Shunt Authors: Thomas Robert M.D Rapha¨el Blanc M.D, M.Sc Gabriele Ciccio M.D Stanislas Smajda M.D Hocine Redjem M.D Robert Fahed M.D Michel Piotin M.D PII: DOI: Reference:
S0303-8467(15)00279-6 http://dx.doi.org/doi:10.1016/j.clineuro.2015.08.004 CLINEU 4145
To appear in:
Clinical Neurology and Neurosurgery
Received date: Revised date: Accepted date:
5-7-2015 27-7-2015 6-8-2015
Please cite this article as: Robert T, Blanc R, Ciccio G, Smajda S, Redjem H, Fahed R, Piotin M, Trigeminal Neuralgia due to Arterialization of the Superior Petrosal Vein in the Context of Dural or Cerebral Arteriovenous Shunt, Clinical Neurology and Neurosurgery (2015), http://dx.doi.org/10.1016/j.clineuro.2015.08.004 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Trigeminal Neuralgia due to Arterialization of the Superior Petrosal Vein in the Context of Dural or Cerebral
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Arteriovenous Shunt Thomas Robert M.D, Raphaël Blanc M.D,M.Sc, Gabriele Ciccio M.D, Stanislas Smajda M.D, Hocine Redjem M.D, Robert Fahed M.D, Michel Piotin M.D.
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Department of Interventional Neuroradiology, Rothschild Foundation Hospital, Paris, France.
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Correspondence: Dr Thomas Robert, MD,
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Rothschild Foundation Hospital, 25 Rue Manin, 75019 Paris, France.
Fax: +33 1 48 62 25 44
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E-mail: [email protected]
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Tel: +33 7 81 30 52 66
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Objective Trigeminal neuralgia (TN) is a rare revealing symptom of dural or cerebral arteriovenous (AV) shunt. Few isolated cases have described the association between TN and arteriovenous shunt. We presented our experience concerning cerebral AV shunt revealed by a TN. Methods Between 2003 and 2013, 548 brain AV malformations (bAVM) and 268 dural AV fistulas (dAVF) were treated and a retrospective analysis identified 10 consecutive cases with TN. We reviewed their clinical and angiographic data and as well as their outcome after endovascular treatment. Results Among the 10 patients, 5 presented a bAVM and 5 a dAVF. TN was contralateral to the AV shunt in 2 cases (20%). The superior petrosal vein (SPV) was arterialized in all cases. An ectasia of the SPV which could explain a compression of the trigeminal nerve was found in two cases only (20%). It seems that a venous hyperpressure in the pontotrigeminal vein (tributary of the SPV) is responsible of the TN, rather than a compressive mechanism. Conclusions Contrary to other publications on this topic, we believe that the venous reflux into tributaries of the superior petrous vein (and in particular the ponto-trigeminal vein) seems to be the first mechanism of the TN rather that the nerve compression.
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Page 1 of 14
Running title: Trigeminal neuralgia secondary to arterialization of the superior petrosal vein.
Key Words: Arteriovenous malformation, Dural arteriovenous fistula, Trigeminal
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neuralgia, Superior petrous vein. ABBREVIATIONS: TN: Trigeminal neuralgia; bAVM: Brain Arteriovenous Malformation;
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dAVF: Dural Arteriovenous Fistula; AV: Arteriovenous; DREZ: Dorsal Root Entry Zone;
Disclosure of funding or financial support/industry affiliations:
an
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We have no conflict of interest.
Highlights
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Trigeminal neuralgia could be, in few cases, the symptom of a cerebral pathology.
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We analyze cases of trigeminal neuralgia secondary to brain arteriovenous malformation or dural arteriovenous fistula.
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Introduction
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The first etiology seems not to be the compression of the nerve but the venous reflux.
Trigeminal neuralgia (TN) is frequently idiopathic and, in few cases, the revealing symptom of a cerebral pathology.1 Dural and cerebral arteriovenous shunts are one of these pathologies but this circumstance is very rare.2 The association between trigeminal neuralgia and arteriovenous shunt of cerebrum or dura has been reported in few cases only.3-16 Isolated cases reported good pain reversibility after embolization,4, 7, 8, 10, 13, 15 surgery2, 5, 6 or radiotherapy.3, 11, 16 We report our cases of symptomatic trigeminal neuralgia secondary to brain arteriovenous malformation (bAVM) or dural arteriovenous fistula (DAVF) in order to understand the pathophysiology, the structure that compresses the nerve (in case of compression) and factors influencing the presence of the neuralgia.
Materials and Methods Patient Demographics
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From a prospectively gathered registry, we identified 548 patients with cerebral AVM and 268 patients with dural arteriovenous fistulas who were treated in our institution between 2003 and 2013.
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In this study, we retrospectively reviewed data from all the patients who suffered from trigeminal neuralgia, and we identified 10 consecutive cases. Demographic data were recorded for each patient including age, sex, clinical presentation and angiographic characteristics of the AV shunt.
Trigeminal Neuralgia Characteristics
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Each patient had a pre-treatment consultation with a neurologist who assessed the following characteristics of the trigeminal neuralgia: trigeminal territory, presence of a trigger zone, corneal reflex, potential hypoesthesia associated to the neuralgia, side of the neurological symptom, duration of the symptoms and the on-going medication.
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Arteriovenous Shunt Anatomy
Endovascular therapy
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Each patient had a radiologic assessment with cerebral magnetic resonance imaging (MRI) and six-vessels cerebral digital subtraction angiography (DSA). Two distinct pathologies were analyzed: brain arteriovenous malformation and dural arteriovenous fistula. In all cases, we noted angioarchitecture landmarks to understand the relation between the underlying vascular disease and the trigeminal neuralgia. We insisted on the analysis of the mechanisms involved in the trigeminal impairment (compression or venous reflux) and the vascular structures involved.
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All patients were treated by endovascular embolization performed under general anesthesia. After cerebral MRI and DSA were performed, the appropriate working projections for catheterization of the arterial supply of the AV shunt were recorded. Treatment options included parent artery occlusion or nidus embolization by cyanoacrylate synthetic glue (Glubran, GEM, Viareggio, Italy) or Onyx (ev3 Neurovascular, Irvine, CA, USA).
Clinical Evolution
Follow-up started at the time of the last embolization session and finished with the last visit or angiography. Angiographic follow-up after complete exclusion of an AVM consisted of one year and long term (5 years) DSA. For dAVF, only one control angiography was performed 6 months after the treatment to confirm the occlusion of the AV shunt. Neurological evaluation regarding the trigeminal neuralgia evolution was made between 6 and 12 months after the treatment. The presence of residual pain, its type and the prescription of an analgesic treatment were assessed.
Results 3
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Clinical Presentation
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Between 2003 and 2013, 10 patients (8 [80%] men, mean age = 37 years old) with dural or cerebral AV shunts revealed by a trigeminal neuralgia were treated in our departement. Patient baseline data and neuralgia types are described in Table 1. The facial pain was in the ophthalmic division (V1) of the TN in 3 cases (30%), the maxillary (V2) in 1 case (10%) and in the mandibular (V3) in 6 cases (60%). A trigger zone was noted in 6 cases (60%), particularly in V3 neuralgia, a loss of corneal reflex in 2 cases (20%) and an associated hypoesthesia in 2 other cases (20%). The symptoms were homolateral of the AV shunt in 80% of cases. The mean duration of symptoms was 26 months. Seven patients presented a drug-resistant pain and the three others had no specific analgesic medication. Five patients were treated by carbamazepine (from 800 to 1200 mg/day) and 2 patients received gabapentine (1200 mg/day) without pain relief.
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Angio-architecture of Brain Arteriovenous Malformations
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Five patients presented a bAVM with an identifiable nidus, which was located in the cerebellar hemisphere in 4 cases and in the vermis in one case. The nidus size was less than 30 mm in 2 cases and between 30 and 60 mm in 3 cases. Four nidi were diffuse and one was compact. The Spetzler-Martin grade 17 was 3 in 4 cases and 4 in 1 case. All the AVMs presented multiple arterial supplies (2-5), at least one of the superior cerebral arteries (SCA) was involved in every case and antero-inferior cerebellar arteries (AICA) were involved in 4 cases as well as the postero-inferior cerebellar arteries (PICA). Flowrelated arterial aneurysm was noted in 3 cases but without relation to the pons or the trigeminal nerve pathway. The venous drainage always involved the superior petrosal vein (Dandy’s vein). In 1 case of right cerebellar hemisphere AVM, the venous drainage impaired the lateral recess vein then the superior petrosal with large ectasia, which compressed the trigeminal nerve DREZ medially. In another case presenting a rightsided TN (figure 1), a large cerebellar hemisphere AVM located in the left side had a venous drainage by the left SPV, the left ponto-mesencephalic vein, the left basal vein with large reflux in the right SPV by the right ponto-mesencephalic vein and causing a contralateral TN. The remaining three cases had a venous drainage by the SPV without reflux but with hyperpressure in tributaries of this vein.
Anatomy of Dural Arteriovenous Fistulas The five other patients presented dural arteriovenous fistulas. The shunt was in the cerebellopontine cistern in 3 cases, the foramen magnum in 1 case and at the free margin of the tentorium in one case. The number of arterial feeders ranged between 2 and 5 with participation of the petrous branch of the middle meningeal artery and clival branches of meningo-hypophyseal trunk in the majority of the cases. Two fistulas had recruited feeders by the AICA and made then duro-pial fistulas. The three other cases were duro-arachnoidal fistulas. According to the classification of Lariboisière 18, 3 were grade 3 and 2 grade 4. The superior petrosal vein was arterialized in all the cases. In one case, the arterialized superior petrosal vein presented a large ectasia (figure 2) that created a major compression of the cisternal portion of the trigeminal nerve. Cystic rearrangements could be seen on pre-operative MR imaging. In another case with
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contralateral TN, a large venous reflux in the SPV could be seen. In the remaining cases, the venous drainage of the fistula increased venous pressure in the SPV.
Treatment of the Pathology
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All the patients were treated by endovascular therapy as a stand-alone treatment modality. All dAVF were cured after one embolization session and 6 month angiographic follow-up showed the durability of the exclusion of these fistulas. Four fistulas were treated with Onyx injection and the other case with glue. One patient presented perprocedural hemorrhage due to venous perforation and a transient cerebellar dysmetria was deplored. Thirteen embolization sessions were performed to treat the 5 patients with AVM (overall: 2.6 embolizations per patient; range: 2-5), and 25 arterial pedicles were navigated to catheterize the AVM nidus. Glue was used in 8 sessions and Onyx in 5. Three AVM nidi were completely occluded, one partially treated with subsequent major decreased venous reflux. The last patient with AVM presented a massive ponto-bulbar hemorrhage 24 hours after partial treatment and died. No other complications were noted.
Clinical Evolution
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The eight patients with complete reversibility of the arterialization of the superior petrosal vein remained pain-free after a mean follow-up of 11.4 months (range: 6-28). Analgesic therapy was interrupted in all patients. Two of them kept a hypoesthesia in the involved territory. The patient for whom a partial treatment of a cerebellar AVM was carried out presented a contralateral TN. After the second embolization session, which decreased significantly the venous reflux into the contralateral SPV, the TN disappeared (figure 1). Further nidal embolizations are planned for this patient to obtain a complete AVM cure.
Discussion
Idiopathic trigeminal neuralgia has an approximate incidence of 5/100 000 and affects generally patients between the 6th and 7th decades.1 Large surgical series2, 19, 20 of trigeminal neuralgia reported a correlation of TN and cerebro-meningeal AVM in 0.6 to 1.5% of cases. For example, Jannetta et al.2 presented only one case in his series of 4400 trigeminal neuralgia. Few isolated cases could be found in the literature reporting TN due to bAVM or dAVF. As we have found in our series, the characteristics of the TN for these patients are identical to those met in idiopathic TN. The mandibular portion of the nerve is frequently involved, a trigger zone is present in half of cases and associated clinical signs are infrequent (10-15%).1, 2, 10 The petrosal veins are divided into superior and inferior petrosal veins based on whether they enter the superior or inferior petrosal sinus.21 The figure 3 is a schematic representation of the relationship between the superior petrosal vein and his tributaries
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with the trigeminal nerve into the cerebello-pontine fissure. The superior petrosal vein is the main collecting vein of the anterolateral portion of posterior fossa structures. This vein receives the lateral anterior ponto-mesencephalic vein, transverse pontine veins, brachial veins, the vein of the horizontal cerebellar fissure and the vein of the lateral recess of the 4th ventricle.21, 22 Another small vein named the ponto-trigeminal vein drains the DREZ of the trigeminal nerve into the SPV.21 The SPV courses anterolaterally, parallel to the trigeminal nerve, to enter into the superior petrosal sinus passing posteriorly and usually superiorly to the trigeminal nerve.21, 22
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In the literature, the first case of brain AVM associated with a TN was described by Eisenbrey and Hegarty in 1956.23 Since this first description, we found in Pubmed database 22 cases of TN secondary to bAVM or dAVF. Most of them were isolated cases except for two small series6, 10. After analyzing these articles, we found 6 cases of cryptic AVM of the trigeminal nerve DREZ3, 14-16, 19, 20. The authors described the involvement of the DREZ nerve directly by the nidus and explained the symptomatology by compression. In 6 other cases4, 6, the AVM nidus were located in the cerebellum hemisphere, and were fed by a dilated superior cerebellar artery compressing the trigeminal nerve. In one case, the AVM was fed by the artery of the Rotundum foramen and this dilated feeding artery exerted the compression of the 2nd portion of the nerve. The authors argued that the Onyx embolization of the rotundum foramen artery was effective on the TN. In only 8 cases,5, 8-13 the venous drainage impaired the superior petrosal vein and was recognized to be responsible for the neuralgia. All authors hypothesized that the arterialized superior petrosal vein compressed the trigeminal nerve DREZ or could be irritating it by the pulsatility. No one evoked the hypothesis of a venous reflux into superior petrosal vein tributaries and, in particular, the pontotrigeminal vein. Only one case of trigeminal neuralgia contralateral to the AV shunt was described by Lu et al.8 where authors described the venous reflux into the contralateral superior petrosal vein but did not conclude that the reflux into the ponto-trigeminal vein could explain the neuralgia.
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In all the case reports on this topic, the authors explained the trigeminal neuralgia by direct involvement of the cysternal part of the trigeminal nerve or by its compression. These two hypotheses cannot explain why contralateral involvement could be possible and why the retrograde flow into the latero-mesencephalic vein increases the risk to develop trigeminal neuralgia. We think that the arterialization of the SPV may produce venous hyperpression into the ponto-trigeminal vein, which is a direct tributary of the SPV, and explains the presence of the neuralgia. The treatment by endovascular embolization of such cases was reported in only 6 cases4, 8, 10, 13. In all cases, the trigeminal neuralgia disappeared after significant decreased in flow in the SPS. In our series of 10 cases, the improvement of the symptomatology was the rule after endovascular therapy.
Conclusion
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Acknowledgements
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Authors have no conflict of interest to declare for his paper.
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BAVM and dAVF are rarely revealed by trigeminal neuralgia, only in 0.6-1.5% of cases. The clinical characteristics of the neuralgia are identical to the idiopathic type in case of AV shunt. Whatever the modality of the treatment chosen, the flow decreasing in the SPV determines the cure of the symptoms. The main etiology of the TN seems to be the venous reflux into tributaries of the SPV (and in particular the ponto-trigeminal vein) rather than a direct compression of the nerve.
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References
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Katusic S, Williams DB, Beard CM, Bergstralh EJ, Kurland LT. Epidemiology and clinical features of idiopathic trigeminal neuralgia and glossopharyngeal neuralgia: similarities and differences, Rochester, Minnesota, 1945-1984. Neuroepidemiology. 1991;10(5-6):276-281. McLaughlin MR, Jannetta PJ, Clyde BL, Subach BR, Comey CH, Resnick DK. Microvascular decompression of cranial nerves: lessons learned after 4400 operations. Journal of neurosurgery. Jan 1999;90(1):1-8. Anderson WS, Wang PP, Rigamonti D. Case of microarteriovenous malformationinduced trigeminal neuralgia treated with radiosurgery. The journal of headache and pain. Sep 2006;7(4):217-221. Athanasiou TC, Nair S, Coakham HB, Lewis TT. Arteriovenous malformation presenting with trigeminal neuralgia and treated with endovascular coiling. Neurology India. Jun 2005;53(2):247-248. Ferroli P, Acerbi F, Broggi M, Broggi G. Arteriovenous micromalformation of the trigeminal root: intraoperative diagnosis with indocyanine green videoangiography: case report. Neurosurgery. Sep 2010;67(3 Suppl Operative):onsE309-310; discussion onsE310. Garcia-Pastor C, Lopez-Gonzalez F, Revuelta R, Nathal E. Trigeminal neuralgia secondary to arteriovenous malformations of the posterior fossa. Surgical neurology. Aug 2006;66(2):207-211; discussion 211. Levitt MR, Ramanathan D, Vaidya SS, Hallam DK, Ghodke BV. Endovascular palliation of AVM-associated intractable trigeminal neuralgia via embolization of the artery of the foramen rotundum. Pain medicine. Dec 2011;12(12):1824-1830. Lu X, Qin X, Ni L, Chen J, Xu F. Tentorial dural arteriovenous fistula manifesting as contralateral trigeminal neuralgia: resolution after transarterial Onyx embolization. BMJ case reports. 2013;2013. Lucas Cde P, Zabramski JM. Dural arteriovenous fistula of the transverse-sigmoid sinus causing trigeminal neuralgia. Acta neurochirurgica. Dec 2007;149(12):1249-1253; discussion 1253. Machet A, Aggour M, Estrade L, Chays A, Pierot L. Trigeminal neuralgia related to arteriovenous malformation of the posterior fossa: three case reports and a review of the literature. Journal of neuroradiology. Journal de neuroradiologie. Mar 2012;39(1):64-69. Matsushige T, Nakaoka M, Ohta K, Yahara K, Okamoto H, Kurisu K. Tentorial dural arteriovenous malformation manifesting as trigeminal neuralgia treated by stereotactic radiosurgery: A case report. Surgical neurology. Nov 2006;66(5):519523; discussion 523. Rahme R, Ali Y, Slaba S, Samaha E. Dural arteriovenous malformation: an unusual cause of trigeminal neuralgia. Acta neurochirurgica. 2007;149(9):937-941; discussion 941. Simon SD, Yao TL, Rosenbaum BP, Reig A, Mericle RA. Resolution of trigeminal neuralgia after palliative embolization of a cerebellopontine angle arteriovenous malformation. Central European neurosurgery. Aug 2009;70(3):161-163. Sumioka S, Kondo A, Tanabe H, Yasuda S. Intrinsic arteriovenous malformation embedded in the trigeminal nerve of a patient with trigeminal neuralgia. Neurologia medico-chirurgica. 2011;51(9):639-641.
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Wanke I, Dietrich U, Oppel F, Puchner MJ. Endovascular treatment of trigeminal neuralgia caused by arteriovenous malformation: is surgery really necessary? Zentralblatt fur Neurochirurgie. Nov 2005;66(4):213-216. Yip V, Michael BD, Nahser HC, Smith D. Arteriovenous malformation: a rare cause of trigeminal neuralgia identified by magnetic resonance imaging with constructive interference in steady state sequences. QJM : monthly journal of the Association of Physicians. Sep 2012;105(9):895-898. Spetzler RF, Martin NA. A proposed grading system for arteriovenous malformations. Journal of neurosurgery. Oct 1986;65(4):476-483. Cognard C, Gobin YP, Pierot L, et al. Cerebral dural arteriovenous fistulas: clinical and angiographic correlation with a revised classification of venous drainage. Radiology. Mar 1995;194(3):671-680. Tsubaki S, Fukushima T, Tamagawa T, et al. Parapontine trigeminal cryptic angiomas presenting as trigeminal neuralgia. Journal of neurosurgery. Sep 1989;71(3):368-374. Edwards RJ, Clarke Y, Renowden SA, Coakham HB. Trigeminal neuralgia caused by microarteriovenous malformations of the trigeminal nerve root entry zone: symptomatic relief following complete excision of the lesion with nerve root preservation. Journal of neurosurgery. Oct 2002;97(4):874-880. Rhoton AA. Rhoton: cranial anatomy and surgical approaches: Lippincott Williams and Wilkins; 2007. Yasargil MG. Microsurgery, vol I. New York: Thieme; 1988. Eisenbrey.AB., Hegarty.W.M. Trigeminal neuralgia and arteriovenous aneurysm of the cerebellopontine angle. Journal of neurosurgery. 1956;13(6):647-649.
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Figure Legends
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Figure 1: Illustrative case 1. A 29-year-old female with a right-sided trigeminal neuralgia presented a left cerebellar hemisphere AVM. Axial (a) and coronal (b) MR in FLAIR weighted-imaging showing the diffuse nidus with an enlarged draining vein in the cerebello-pontine angle. Antero-posterior projections DSA with injection of the left vertebral artery before (c) and after (d) the second embolization session demonstrating the decreasing of the venous reflux into the contralateral superior petrosal vein. Since this embolization, the patient is pain-free.
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Figure 2: Illustrative case 2. A 42-year-old male presenting a left-sided trigeminal neuralgia. Pre-operative MR in axial T2 WI (a) showed venous ectasia in the cerebellopontine angle with major compression to the trigeminal nerve (white arrows). Edema of the left middle cerebellar peduncle (white arrowhead) was also visible in axial FLAIR (b). After gadolinium injection (c), the ectasia could be seen without thrombosis. The course of the trigeminal nerve could be followed (white arrows on c). 6 vessels DSA (d,e and f) showed a dural fistula of the cerebello-pontine fissure fed by the petrous branch of the left MMA and the left meningo-hypophyseal trunk. The venous drainage could be appreciated in the figure 2d, and is drained by the SPV and the contralateral superior petrosal sinus through pontine vein. The working projection after micro-catheterism of the petrous branch of the MMA (g) demonstrated a high-flow into the venous ectasia. The injection of Onyx by the MMA (h) went through the venous ectasia and the draining vein. The control DSA in lateral projection after injection of the left common carotid artery (i) confirmed the complete obliteration of the arteriovenous shunt. Since this embolization, the patient is pain-free.
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Figure 3: Schematic representation of venous anatomy within the ambient cistern. Anterior view of the left cerebello-pontine fissure showing the closed relationship between the trigeminal nerve, the ponto-trigeminal vein and the superior petrosal vein. 1: Basal vein of Rosenthal. 2: Latero-mesencephalic vein. 3: Trigeminal nerve. 4: Superior petrosal vein. 5: Vein of the horizontal cerebellar fissure. 6: Lateral recess vein. 7: Ponto-trigeminal vein and trans-pontine vein.
Table 1: Demographic data and trigeminal neuralgia description. Variable Male Mean age (range) Trigeminal territory V1 V2 V3 Trigger Zone Loss of Corneal Reflex Associated Hypoesthesia Side
n=10 8 (80%) 37 (25-56) 3 1 6 6 2 2
(30%) (10%) (60%) (60%) (20%) (20%)
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Homolateral to the shunt Contralateral to the shunt Duration of Symptoms (months) Treatment No Carbamazepine Gabapentine
8 (80%) 2 (20%) 25.9 (1-120)
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3 (30%) 5 (50%) 2 (20%)
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S0303-8467(15)00279-6 http://dx.doi.org/doi:10.1016/j.clineuro.2015.08.004 CLINEU 4145
To appear in:
Clinical Neurology and Neurosurgery
Received date: Revised date: Accepted date:
5-7-2015 27-7-2015 6-8-2015
Please cite this article as: Robert T, Blanc R, Ciccio G, Smajda S, Redjem H, Fahed R, Piotin M, Trigeminal Neuralgia due to Arterialization of the Superior Petrosal Vein in the Context of Dural or Cerebral Arteriovenous Shunt, Clinical Neurology and Neurosurgery (2015), http://dx.doi.org/10.1016/j.clineuro.2015.08.004 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Trigeminal Neuralgia due to Arterialization of the Superior Petrosal Vein in the Context of Dural or Cerebral
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Arteriovenous Shunt Thomas Robert M.D, Raphaël Blanc M.D,M.Sc, Gabriele Ciccio M.D, Stanislas Smajda M.D, Hocine Redjem M.D, Robert Fahed M.D, Michel Piotin M.D.
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Department of Interventional Neuroradiology, Rothschild Foundation Hospital, Paris, France.
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Correspondence: Dr Thomas Robert, MD,
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Rothschild Foundation Hospital, 25 Rue Manin, 75019 Paris, France.
Fax: +33 1 48 62 25 44
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E-mail: [email protected]
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Tel: +33 7 81 30 52 66
Ac ce p
te
Objective Trigeminal neuralgia (TN) is a rare revealing symptom of dural or cerebral arteriovenous (AV) shunt. Few isolated cases have described the association between TN and arteriovenous shunt. We presented our experience concerning cerebral AV shunt revealed by a TN. Methods Between 2003 and 2013, 548 brain AV malformations (bAVM) and 268 dural AV fistulas (dAVF) were treated and a retrospective analysis identified 10 consecutive cases with TN. We reviewed their clinical and angiographic data and as well as their outcome after endovascular treatment. Results Among the 10 patients, 5 presented a bAVM and 5 a dAVF. TN was contralateral to the AV shunt in 2 cases (20%). The superior petrosal vein (SPV) was arterialized in all cases. An ectasia of the SPV which could explain a compression of the trigeminal nerve was found in two cases only (20%). It seems that a venous hyperpressure in the pontotrigeminal vein (tributary of the SPV) is responsible of the TN, rather than a compressive mechanism. Conclusions Contrary to other publications on this topic, we believe that the venous reflux into tributaries of the superior petrous vein (and in particular the ponto-trigeminal vein) seems to be the first mechanism of the TN rather that the nerve compression.
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Page 1 of 14
Running title: Trigeminal neuralgia secondary to arterialization of the superior petrosal vein.
Key Words: Arteriovenous malformation, Dural arteriovenous fistula, Trigeminal
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neuralgia, Superior petrous vein. ABBREVIATIONS: TN: Trigeminal neuralgia; bAVM: Brain Arteriovenous Malformation;
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dAVF: Dural Arteriovenous Fistula; AV: Arteriovenous; DREZ: Dorsal Root Entry Zone;
Disclosure of funding or financial support/industry affiliations:
an
us
We have no conflict of interest.
Highlights
M
Trigeminal neuralgia could be, in few cases, the symptom of a cerebral pathology.
d
We analyze cases of trigeminal neuralgia secondary to brain arteriovenous malformation or dural arteriovenous fistula.
Ac ce p
Introduction
te
The first etiology seems not to be the compression of the nerve but the venous reflux.
Trigeminal neuralgia (TN) is frequently idiopathic and, in few cases, the revealing symptom of a cerebral pathology.1 Dural and cerebral arteriovenous shunts are one of these pathologies but this circumstance is very rare.2 The association between trigeminal neuralgia and arteriovenous shunt of cerebrum or dura has been reported in few cases only.3-16 Isolated cases reported good pain reversibility after embolization,4, 7, 8, 10, 13, 15 surgery2, 5, 6 or radiotherapy.3, 11, 16 We report our cases of symptomatic trigeminal neuralgia secondary to brain arteriovenous malformation (bAVM) or dural arteriovenous fistula (DAVF) in order to understand the pathophysiology, the structure that compresses the nerve (in case of compression) and factors influencing the presence of the neuralgia.
Materials and Methods Patient Demographics
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From a prospectively gathered registry, we identified 548 patients with cerebral AVM and 268 patients with dural arteriovenous fistulas who were treated in our institution between 2003 and 2013.
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In this study, we retrospectively reviewed data from all the patients who suffered from trigeminal neuralgia, and we identified 10 consecutive cases. Demographic data were recorded for each patient including age, sex, clinical presentation and angiographic characteristics of the AV shunt.
Trigeminal Neuralgia Characteristics
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Each patient had a pre-treatment consultation with a neurologist who assessed the following characteristics of the trigeminal neuralgia: trigeminal territory, presence of a trigger zone, corneal reflex, potential hypoesthesia associated to the neuralgia, side of the neurological symptom, duration of the symptoms and the on-going medication.
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Arteriovenous Shunt Anatomy
Endovascular therapy
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Each patient had a radiologic assessment with cerebral magnetic resonance imaging (MRI) and six-vessels cerebral digital subtraction angiography (DSA). Two distinct pathologies were analyzed: brain arteriovenous malformation and dural arteriovenous fistula. In all cases, we noted angioarchitecture landmarks to understand the relation between the underlying vascular disease and the trigeminal neuralgia. We insisted on the analysis of the mechanisms involved in the trigeminal impairment (compression or venous reflux) and the vascular structures involved.
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All patients were treated by endovascular embolization performed under general anesthesia. After cerebral MRI and DSA were performed, the appropriate working projections for catheterization of the arterial supply of the AV shunt were recorded. Treatment options included parent artery occlusion or nidus embolization by cyanoacrylate synthetic glue (Glubran, GEM, Viareggio, Italy) or Onyx (ev3 Neurovascular, Irvine, CA, USA).
Clinical Evolution
Follow-up started at the time of the last embolization session and finished with the last visit or angiography. Angiographic follow-up after complete exclusion of an AVM consisted of one year and long term (5 years) DSA. For dAVF, only one control angiography was performed 6 months after the treatment to confirm the occlusion of the AV shunt. Neurological evaluation regarding the trigeminal neuralgia evolution was made between 6 and 12 months after the treatment. The presence of residual pain, its type and the prescription of an analgesic treatment were assessed.
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Clinical Presentation
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Between 2003 and 2013, 10 patients (8 [80%] men, mean age = 37 years old) with dural or cerebral AV shunts revealed by a trigeminal neuralgia were treated in our departement. Patient baseline data and neuralgia types are described in Table 1. The facial pain was in the ophthalmic division (V1) of the TN in 3 cases (30%), the maxillary (V2) in 1 case (10%) and in the mandibular (V3) in 6 cases (60%). A trigger zone was noted in 6 cases (60%), particularly in V3 neuralgia, a loss of corneal reflex in 2 cases (20%) and an associated hypoesthesia in 2 other cases (20%). The symptoms were homolateral of the AV shunt in 80% of cases. The mean duration of symptoms was 26 months. Seven patients presented a drug-resistant pain and the three others had no specific analgesic medication. Five patients were treated by carbamazepine (from 800 to 1200 mg/day) and 2 patients received gabapentine (1200 mg/day) without pain relief.
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Angio-architecture of Brain Arteriovenous Malformations
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Five patients presented a bAVM with an identifiable nidus, which was located in the cerebellar hemisphere in 4 cases and in the vermis in one case. The nidus size was less than 30 mm in 2 cases and between 30 and 60 mm in 3 cases. Four nidi were diffuse and one was compact. The Spetzler-Martin grade 17 was 3 in 4 cases and 4 in 1 case. All the AVMs presented multiple arterial supplies (2-5), at least one of the superior cerebral arteries (SCA) was involved in every case and antero-inferior cerebellar arteries (AICA) were involved in 4 cases as well as the postero-inferior cerebellar arteries (PICA). Flowrelated arterial aneurysm was noted in 3 cases but without relation to the pons or the trigeminal nerve pathway. The venous drainage always involved the superior petrosal vein (Dandy’s vein). In 1 case of right cerebellar hemisphere AVM, the venous drainage impaired the lateral recess vein then the superior petrosal with large ectasia, which compressed the trigeminal nerve DREZ medially. In another case presenting a rightsided TN (figure 1), a large cerebellar hemisphere AVM located in the left side had a venous drainage by the left SPV, the left ponto-mesencephalic vein, the left basal vein with large reflux in the right SPV by the right ponto-mesencephalic vein and causing a contralateral TN. The remaining three cases had a venous drainage by the SPV without reflux but with hyperpressure in tributaries of this vein.
Anatomy of Dural Arteriovenous Fistulas The five other patients presented dural arteriovenous fistulas. The shunt was in the cerebellopontine cistern in 3 cases, the foramen magnum in 1 case and at the free margin of the tentorium in one case. The number of arterial feeders ranged between 2 and 5 with participation of the petrous branch of the middle meningeal artery and clival branches of meningo-hypophyseal trunk in the majority of the cases. Two fistulas had recruited feeders by the AICA and made then duro-pial fistulas. The three other cases were duro-arachnoidal fistulas. According to the classification of Lariboisière 18, 3 were grade 3 and 2 grade 4. The superior petrosal vein was arterialized in all the cases. In one case, the arterialized superior petrosal vein presented a large ectasia (figure 2) that created a major compression of the cisternal portion of the trigeminal nerve. Cystic rearrangements could be seen on pre-operative MR imaging. In another case with
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contralateral TN, a large venous reflux in the SPV could be seen. In the remaining cases, the venous drainage of the fistula increased venous pressure in the SPV.
Treatment of the Pathology
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All the patients were treated by endovascular therapy as a stand-alone treatment modality. All dAVF were cured after one embolization session and 6 month angiographic follow-up showed the durability of the exclusion of these fistulas. Four fistulas were treated with Onyx injection and the other case with glue. One patient presented perprocedural hemorrhage due to venous perforation and a transient cerebellar dysmetria was deplored. Thirteen embolization sessions were performed to treat the 5 patients with AVM (overall: 2.6 embolizations per patient; range: 2-5), and 25 arterial pedicles were navigated to catheterize the AVM nidus. Glue was used in 8 sessions and Onyx in 5. Three AVM nidi were completely occluded, one partially treated with subsequent major decreased venous reflux. The last patient with AVM presented a massive ponto-bulbar hemorrhage 24 hours after partial treatment and died. No other complications were noted.
Clinical Evolution
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The eight patients with complete reversibility of the arterialization of the superior petrosal vein remained pain-free after a mean follow-up of 11.4 months (range: 6-28). Analgesic therapy was interrupted in all patients. Two of them kept a hypoesthesia in the involved territory. The patient for whom a partial treatment of a cerebellar AVM was carried out presented a contralateral TN. After the second embolization session, which decreased significantly the venous reflux into the contralateral SPV, the TN disappeared (figure 1). Further nidal embolizations are planned for this patient to obtain a complete AVM cure.
Discussion
Idiopathic trigeminal neuralgia has an approximate incidence of 5/100 000 and affects generally patients between the 6th and 7th decades.1 Large surgical series2, 19, 20 of trigeminal neuralgia reported a correlation of TN and cerebro-meningeal AVM in 0.6 to 1.5% of cases. For example, Jannetta et al.2 presented only one case in his series of 4400 trigeminal neuralgia. Few isolated cases could be found in the literature reporting TN due to bAVM or dAVF. As we have found in our series, the characteristics of the TN for these patients are identical to those met in idiopathic TN. The mandibular portion of the nerve is frequently involved, a trigger zone is present in half of cases and associated clinical signs are infrequent (10-15%).1, 2, 10 The petrosal veins are divided into superior and inferior petrosal veins based on whether they enter the superior or inferior petrosal sinus.21 The figure 3 is a schematic representation of the relationship between the superior petrosal vein and his tributaries
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with the trigeminal nerve into the cerebello-pontine fissure. The superior petrosal vein is the main collecting vein of the anterolateral portion of posterior fossa structures. This vein receives the lateral anterior ponto-mesencephalic vein, transverse pontine veins, brachial veins, the vein of the horizontal cerebellar fissure and the vein of the lateral recess of the 4th ventricle.21, 22 Another small vein named the ponto-trigeminal vein drains the DREZ of the trigeminal nerve into the SPV.21 The SPV courses anterolaterally, parallel to the trigeminal nerve, to enter into the superior petrosal sinus passing posteriorly and usually superiorly to the trigeminal nerve.21, 22
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In the literature, the first case of brain AVM associated with a TN was described by Eisenbrey and Hegarty in 1956.23 Since this first description, we found in Pubmed database 22 cases of TN secondary to bAVM or dAVF. Most of them were isolated cases except for two small series6, 10. After analyzing these articles, we found 6 cases of cryptic AVM of the trigeminal nerve DREZ3, 14-16, 19, 20. The authors described the involvement of the DREZ nerve directly by the nidus and explained the symptomatology by compression. In 6 other cases4, 6, the AVM nidus were located in the cerebellum hemisphere, and were fed by a dilated superior cerebellar artery compressing the trigeminal nerve. In one case, the AVM was fed by the artery of the Rotundum foramen and this dilated feeding artery exerted the compression of the 2nd portion of the nerve. The authors argued that the Onyx embolization of the rotundum foramen artery was effective on the TN. In only 8 cases,5, 8-13 the venous drainage impaired the superior petrosal vein and was recognized to be responsible for the neuralgia. All authors hypothesized that the arterialized superior petrosal vein compressed the trigeminal nerve DREZ or could be irritating it by the pulsatility. No one evoked the hypothesis of a venous reflux into superior petrosal vein tributaries and, in particular, the pontotrigeminal vein. Only one case of trigeminal neuralgia contralateral to the AV shunt was described by Lu et al.8 where authors described the venous reflux into the contralateral superior petrosal vein but did not conclude that the reflux into the ponto-trigeminal vein could explain the neuralgia.
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In all the case reports on this topic, the authors explained the trigeminal neuralgia by direct involvement of the cysternal part of the trigeminal nerve or by its compression. These two hypotheses cannot explain why contralateral involvement could be possible and why the retrograde flow into the latero-mesencephalic vein increases the risk to develop trigeminal neuralgia. We think that the arterialization of the SPV may produce venous hyperpression into the ponto-trigeminal vein, which is a direct tributary of the SPV, and explains the presence of the neuralgia. The treatment by endovascular embolization of such cases was reported in only 6 cases4, 8, 10, 13. In all cases, the trigeminal neuralgia disappeared after significant decreased in flow in the SPS. In our series of 10 cases, the improvement of the symptomatology was the rule after endovascular therapy.
Conclusion
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Acknowledgements
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Authors have no conflict of interest to declare for his paper.
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BAVM and dAVF are rarely revealed by trigeminal neuralgia, only in 0.6-1.5% of cases. The clinical characteristics of the neuralgia are identical to the idiopathic type in case of AV shunt. Whatever the modality of the treatment chosen, the flow decreasing in the SPV determines the cure of the symptoms. The main etiology of the TN seems to be the venous reflux into tributaries of the SPV (and in particular the ponto-trigeminal vein) rather than a direct compression of the nerve.
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References
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Figure Legends
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Figure 1: Illustrative case 1. A 29-year-old female with a right-sided trigeminal neuralgia presented a left cerebellar hemisphere AVM. Axial (a) and coronal (b) MR in FLAIR weighted-imaging showing the diffuse nidus with an enlarged draining vein in the cerebello-pontine angle. Antero-posterior projections DSA with injection of the left vertebral artery before (c) and after (d) the second embolization session demonstrating the decreasing of the venous reflux into the contralateral superior petrosal vein. Since this embolization, the patient is pain-free.
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Figure 2: Illustrative case 2. A 42-year-old male presenting a left-sided trigeminal neuralgia. Pre-operative MR in axial T2 WI (a) showed venous ectasia in the cerebellopontine angle with major compression to the trigeminal nerve (white arrows). Edema of the left middle cerebellar peduncle (white arrowhead) was also visible in axial FLAIR (b). After gadolinium injection (c), the ectasia could be seen without thrombosis. The course of the trigeminal nerve could be followed (white arrows on c). 6 vessels DSA (d,e and f) showed a dural fistula of the cerebello-pontine fissure fed by the petrous branch of the left MMA and the left meningo-hypophyseal trunk. The venous drainage could be appreciated in the figure 2d, and is drained by the SPV and the contralateral superior petrosal sinus through pontine vein. The working projection after micro-catheterism of the petrous branch of the MMA (g) demonstrated a high-flow into the venous ectasia. The injection of Onyx by the MMA (h) went through the venous ectasia and the draining vein. The control DSA in lateral projection after injection of the left common carotid artery (i) confirmed the complete obliteration of the arteriovenous shunt. Since this embolization, the patient is pain-free.
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Figure 3: Schematic representation of venous anatomy within the ambient cistern. Anterior view of the left cerebello-pontine fissure showing the closed relationship between the trigeminal nerve, the ponto-trigeminal vein and the superior petrosal vein. 1: Basal vein of Rosenthal. 2: Latero-mesencephalic vein. 3: Trigeminal nerve. 4: Superior petrosal vein. 5: Vein of the horizontal cerebellar fissure. 6: Lateral recess vein. 7: Ponto-trigeminal vein and trans-pontine vein.
Table 1: Demographic data and trigeminal neuralgia description. Variable Male Mean age (range) Trigeminal territory V1 V2 V3 Trigger Zone Loss of Corneal Reflex Associated Hypoesthesia Side
n=10 8 (80%) 37 (25-56) 3 1 6 6 2 2
(30%) (10%) (60%) (60%) (20%) (20%)
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Homolateral to the shunt Contralateral to the shunt Duration of Symptoms (months) Treatment No Carbamazepine Gabapentine
8 (80%) 2 (20%) 25.9 (1-120)
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3 (30%) 5 (50%) 2 (20%)
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