Dural Arteriovenous Fistula Presenting as Trigeminal Neuralgia: Two Case Reports and Review of the Literature

Journal Pre-proof Dural Arteriovenous Fistula Presenting as Trigeminal Neuralgia: Two Case Reports and Review of the Literature Erik C. Brown, MD, PhD, Pavlos Texakalidis, MD, Brittany Stedelin, BS, Muhibullah S. Tora, BS, Rima S. Rindler, MD, Jonathan A. Grossberg, MD, Ryan Peterson, MD, Melissa Campbell, NP, Justin S. Cetas, MD, PhD, Nicholas Boulis, MD, Ahmed M. Raslan, MD PII:

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https://doi.org/10.1016/j.wneu.2020.02.083

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World Neurosurgery

Received Date: 16 January 2020 Revised Date:

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Accepted Date: 14 February 2020

Please cite this article as: Brown EC, Texakalidis P, Stedelin B, Tora MS, Rindler RS, Grossberg JA, Peterson R, Campbell M, Cetas JS, Boulis N, Raslan AM, Dural Arteriovenous Fistula Presenting as Trigeminal Neuralgia: Two Case Reports and Review of the Literature, World Neurosurgery (2020), doi: https://doi.org/10.1016/j.wneu.2020.02.083. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. 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. © 2020 Elsevier Inc. All rights reserved.

Dural Arteriovenous Fistula Presenting as Trigeminal Neuralgia: Two Case Reports and Review of the Literature Erik C. Brown, MD, PhD1; Pavlos Texakalidis, MD2; Brittany Stedelin, BS1; Muhibullah S Tora, BS2; Rima S Rindler, MD3; Jonathan A Grossberg, MD3; Ryan Peterson, MD3; Melissa Campbell, NP2; Justin S. Cetas, MD, PhD1; Nicholas Boulis, MD2; Ahmed M. Raslan, MD1 1

Departments of Neurological Surgery, Oregon Health & Science University and Veterans Affairs Medical Center, Portland, Oregon, USA Departments of 2Neurosurgery and 3Radiology, School of Medicine, Emory University, Atlanta, Georgia, USA

Corresponding Author: Ahmed M. Raslan Neurological Surgery Oregon Health & Science University 3303 S.W. Bond Ave. Portland, OR, 97239, USA Phone: 503-494-7623 FAX: 503-346-6810 E-mail: [email protected]

Dural Arteriovenous Fistula Presenting as Trigeminal Neuralgia

Abstract

Dural arteriovenous fistulae (dAVF) can sporadically compress the root entry zone (REZ) of the trigeminal nerve or the Gasserian ganglion and can therefore be a rare cause of isolated or complicated trigeminal neuralgia (TN). We describe two cases of TN related to dAVF treated similarly with transarterial embolization but with divergent outcomes. Further, we completed a comprehensive literature review of previously reported cases to date. A sparse but growing literature with regards to this specific and rare but salient cause of TN was noted. The type of dAVF most commonly found to cause TN was that of a tentorial nidus; a lesion generally accepted to be at high risk of hemorrhage and in need of urgent treatment. This warrants imaging for new TN presentations to ensure that a dangerous lesion does not represent the underlying cause, especially when the TN symptoms are comorbid with other symptoms such as a bruit. Treatments pursued span the range of open surgery, endovascular treatment, and radiosurgery with great success in treating both the TN symptoms as well as the rupture risk of the dAVF itself in most case. Indeed, endovascular approaches are becoming more widely employed for these cases over time, often resolving the abnormality on first treatment attempt. Other cases reach resolution after employing a combination of treatment modalities. This work highlights that dAVFs, particularly the tentorial type, are capable of causing TN symptomatically identical to that of other etiologies and that treatment of the dAVF itself is often sufficient. Keywords: Trigeminal neuralgia, arteriovenous fistula, tentorial, embolization, Onyx

Dural Arteriovenous Fistula Presenting as Trigeminal Neuralgia

Introduction Trigeminal neuralgia (TN), or tic douloureux, is a severe form of facial pain that can be associated with significant reduction in quality of life. TN occurs most commonly in the distribution of the maxillary and/or mandibular branch of the trigeminal nerve unilaterally42. The incidence in the general US population is estimated to be 5.9 women and 3.4 men per 100,000. Globally the reported incidence varies owing to differences in diagnostic criteria47. The most prominent method of describing and classifying TN is based on history of clinical characteristics described by the patient themselves.10 A ‘type 1’ pattern is defined as paroxysmal, shooting pains that are often triggered by specific stimuli and interspersed by pain free intervals. Patients can often clearly define the first moment they experienced such pain, with common descriptors including ‘electrical’ or ‘shock-like’. Type 1 TN is more likely to respond to therapy, both medical and surgical. A ‘type 2’ pattern, or continuous TN10, is defined as a constant, often dull, aching, or burning pain. Type 2 TN is less likely to show a complete response to interventions and can be further divided into two types8. “Neurovascular conflict”, in which a surrounding vascular structure physically impedes a neurological structure, is discovered as the underlying etiology in as many as 76-90% of symptomatic individuals with clinically established TN3,10,23. In the case of classical TN10, a blood vessel applies compression to the root entry zone of the trigeminal nerve. Conversely, some institutions have reported a lower proportion, some less than 50%8. Recently direct contact has been argued to be insufficient evidence of neurovascular conflict. Thinning and distortion of the nerve are thought to be more reliable for predicting symptomatology than simple contact alone31. Interestingly, asymptomatic individuals are found to demonstrate neurovascular contact as often as 28.3-71% of the time and occasionally conflict with visible anatomical changes to the nerve at a rate as high as 0.7-1.66%, suggesting that findings on imaging may not equate

Dural Arteriovenous Fistula Presenting as Trigeminal Neuralgia

disease.31,40 The most common causative vascular abnormalities that interfere specifically with the root entry zone of the trigeminal nerve in order of prevalence are: loops from a nearby vessel such as the superior cerebellar artery, vertebrobasilar dolichoectasia, and arteriovenous malformations including dural arteriovenous fistulae (dAVF).7 dAVF represent acquired, abnormal dural-based fistulae between an artery supplying the dura mater and venous structures, bypassing the capillary bed, with the term ‘fistula’ being a misnomer in this case; a single dAVF typically contains multiple fistulae6. They have a detection rate of 0.16-0.51/100,000 per year.2,18 The risk of hemorrhage of any one dAVF may be predicted with either the Cognard9 or Borden6 classification systems, both of which are widely used. Cases are of particular interest when the neurovascular conflict from which TN arises involves a vascular malformation. It presents an intuitive avenue for treatment, ie treating the vascular malformation may lead to resolution of symptoms, but also represents a medical comorbidity with risk of other potentially devastating clinical events making definitive treatment more urgent, eg rupture leading to subarachnoid, intraventricular, and/or intraparenchymal hemorrhage. We present two cases of TN caused by a tentorial dAVF divergent in their response to treatment, one with complete resolution of TN symptoms immediately following successful treatment of the fistula by embolization and the other requiring surgical intervention with persistent symptomatology. We also performed an extensive literature review to update and expand knowledge of this specific and rare clinical entity to enable future systematic reviews as questions on this topic arise.

Dural Arteriovenous Fistula Presenting as Trigeminal Neuralgia

Case Report 1 A 55-year old right handed male veteran with past medical history significant for hypertension, obesity, tobacco use, diabetes mellitus type II with renal manifestations, osteoarthritis, and remote history of right head trauma but no evidence of intracranial surgery, presented on referral from his primary care physician. He described a 3 to 4-month history of left-sided chin, mandibular, tooth, and buccal pain radiating to the left auricle that resembled new-onset TN primarily affecting the V2 branch but also involving V3. Initially the pain appeared as an ‘electrical jolt’ that would come and go, suggesting TN type 1, but then rapidly evolved to a constant ‘deep ache’, suggesting TN type 2. There were no clear inciting events or triggers for his pain and a brief trial of carbamazepine was ineffective at diminishing discomfort. An initial contrast magnetic resonance imaging (MRI) with angiography (MRA) revealed a vascular abnormality suggestive of a dAVF causing local mass effect of the left sided junction between the midbrain and pons with an enlarged draining vessel contacting the root entry zone of the left trigeminal nerve (Figure 1A&B). Diagnostic cerebral angiogram confirmed a Cognard type 4, Borden class 3 left tentorial dAVF with multiple arterial feeders arising off of branches of the left external carotid artery, left meningohypophyseal branches of the left internal carotid artery, as well as posterior meningeal artery. There was also a flow-related aneurysm within the extradural segment of the left meningohypophyseal branch origin deemed to be at high risk of rupture (Figure 1C&D). Venous drainage was complicated by restrictive disease, varices, and reflux ultimately draining to the vein of Galen. The day after transarterial embolization, the patient reported left sided headache but no facial pain at all and was deemed amenable for discharge; interestingly, the patient noted that their headache resolved when they laid on their side as opposed to supine. Five days after

Dural Arteriovenous Fistula Presenting as Trigeminal Neuralgia

discharge the patient described cranial pain originating from the occiput and radiating toward the eyes. This evolved into a constant left-sided headache with neck stiffness that failed to respond to over-the-counter pain medication or a dose of hydrocodone. Methylprednisolone was ordered and the patient reported partial relief at follow-up 8 days later. At 4 months following embolization, the patient continued with gradually improving left sided headache and stable, complete resolution of his facial pain. He underwent repeat diagnostic cerebral angiogram 5 months post embolization that showed continued complete occlusion of the dAVF. At 6 months post embolization, the patient revealed that their headache pain score had decreased to a 2 or 3 out of 10 from a previously described 7 following the embolization procedure. It is unclear if the source of this mild headache was central or systemic, as the patient was experiencing hypertensive symptoms during this period with systolic pressures regularly into the 170s accompanied by symptoms of daytime drowsiness and irritability. The patient did not exhibit a demonstrable neurological deficit at any point in his care related to the fistula, from presentation through ongoing follow-up.

Case Report 2 A 72-year-old female with past medical history significant for ulcerative colitis presented with a 20-year history of right-sided V2 distribution pain consistent with TN type 1 but later developed to involve V3 as well and became constant, consistent with TN type 2. Her pain was resistant to medical therapy, a sinus procedure, orthodontic procedures, radiosurgery, balloon compression rhizotomy, and percutaneous trigeminal nerve stimulation. Physical examination revealed right-sided hearing loss associated with subjective pulsatile tinnitus. MRA was suggestive of a likely arterialized superior petrosal vein (Figure 2A), a finding which raised

Dural Arteriovenous Fistula Presenting as Trigeminal Neuralgia

concern for a vascular aberration beyond simple microvascular compression by an otherwise normal arterial loop. This prompted diagnostic cerebral angiography which demonstrated a Borden class I tentorial dural AVF supplied by the pterygoid branch of the internal maxillary artery (Figure 2B), with small contributions from the facial artery. The fistula drained into the petrosal, facial, and external jugular veins. The patient underwent endovascular transarterial embolization with post-treatment surveillance imaging demonstrating complete obliteration of the dural AVF. At 1-month follow-up, the patient reported complete resolution of pulsatile tinnitus, however her facial pain remained unchanged. Follow-up MRA revealed a persistent vein coursing parallel to the right trigeminal nerve (Figure 2C) that exhibited reduced blood flow relative to pre-operative imaging, with arterial feeders not visualized (Figure 2D). The patient was scheduled for surgical microvascular decompression 3 months later. No arterial compression was noted at the time of surgery, but two large petrosal veins were noted to course medial and lateral to the fifth cranial nerve at its root entry zone. These were coagulated to shrink but maintain their lumen canalization until there was no visible compression, then internal neurolysis was performed and a Teflon felt was placed around the root entry zone. Three months postoperatively, the patient describes dense right sided facial numbness with continued but paroxysmal pain. Trigeminal tractotomy is being considered.

Literature Review A search of PubMed utilizing varying combinations of the search terms ‘trigeminal neuralgia’, ‘dural arteriovenous fistula’, and ‘vascular malformation’, was undertaken. We selected all manuscripts resulting from the search, which described at least one specific case of dAVF associated with TN. Within each of these identified manuscripts, we further reviewed the

Dural Arteriovenous Fistula Presenting as Trigeminal Neuralgia

reference list to yield further manuscripts describing the same. To support our effort to generate an extensive review, we did not limit our search to the English-language literature. We enlisted aid to extract essential information whenever a manuscript was written in a language other than English. Patient characteristics such as sex and age, any medications utilized and time-to-failure, distribution of TN symptoms, any additional symptoms, description of the dAVF, procedures performed throughout the course of the condition, clinical as well as radiographic outcome, duration of follow-up, and any adverse events were collected and tabulated. We distinguished TN type, when able, based upon the provided description of symptoms; ie TN type 1 and type 2, with type 2 further distinguished as type 2a (mixed) or type 2b (atypical) based on the presence or absence of progression from a type 1 state, respectively.35 We chose to classify the dAVFs with the Borden classification system as it is less complex, lending it to be more readily applied to a cohort of cases with varying degrees of descriptive detail. When provided in the manuscript, we noted the Borden class. When a Cognard type was provided, it was translated into a Borden class using the following scheme: Borden class 1 equivalent to Cognard class 1 or IIa, Borden class 2 equivalent to Cognard class IIb or IIa+b, and Borden class 3 equivalent to Cognard class III, IV, or V. When the manuscript did not provide a Borden or Cognard classification, we applied a Borden class, when able, based on the provided imaging and description utilizing the original Borden classification scheme described in 1995.6 Our literature review is summarized in Table 1. Our review yielded a total of 30 manuscripts,1,5,6,13-17,19-22,24-30,32-34,36-39,41,43,44,46 not including the present manuscript, with a total of 48 cases described in varying levels of detail, including the cases describe herein. Two articles were written in Japanese, one in Spanish, and one in Russian and we enlisted the aid of a native Japanese, Spanish, and Russian speaking colleagues to extract information. One article was

Dural Arteriovenous Fistula Presenting as Trigeminal Neuralgia

written in Polish and as we did not have ready access to a native Polish speaking colleague we utilized Google Translate which did prove useful in extracting essential information. Of the 32 patients for whom a sex was specified, 21 (~66%) were male and 11 (~34%) were female. Of the 43 cases in whom both a type of direct dAVF treatment and a clinical outcome measure were described, 40 (~93%) cases experienced immediate or eventual complete relief from symptoms of facial pain. Of these 43 cases, 34 (~79%) underwent some form of endovascular treatment of the dAVF. Of these 34 endovascularly treated cases, 31 (~91%) underwent transarterial embolization and 4 (~12%) transvenous with 1 of these cases representing a combined transarterial and transvenous endovascular approach. A total of 23 (~68%) of them were successful at providing relief from TN with endovascular treatment of the dAVF alone. A total of 14 cases went for open surgical intervention. Regarding radiosurgical intervention for the dAVF, 4 such treatments were employed with 2 cases treated successfully with only gamma-knife therapy. Adverse events following therapy were rare, varied, and usually mild with resolution over time. The one exception was a post transvenous embolization resulting in subarachnoid hemorrhage leading to the development of hydrocephalus requiring surgical placement of a ventriculoperitoneal shunt. This elderly individual did ultimately achieve complete relief from facial pain which had been troubling them for at least 3.5 years. Only one other hemorrhage was reported to have occurred and it was a presenting feature in an elderly individual with his sudden onset facial pain representing a manifestation of hemorrhage from his dAVF.

Discussion The prevalence of TN is quoted to range from 0.03% to 0.3% of population and therefore is quite uncommon. It is considered one of the most painful disorders of the orofacial region. It

Dural Arteriovenous Fistula Presenting as Trigeminal Neuralgia

largely effects an age range from 37 to 67 years with women effected more frequently than men at a ratio of 3 to 1. The pain most commonly occurs in the maxillary (V2) and mandibular (V3) branches, typically unilaterally.12 Based upon our extensive literature review and others previously described, with only 48 cases of TN caused by dAVF in the worldwide literature going back as far as 1966, dAVF as a cause of TN is rare. It has been previously described that <1% of TN cases are due to an underlying vascular malformation.4,45 The TN that is caused by dAVF is the same condition that is more typically described as it shares several critical characteristics. It is typically unilateral and most often involving the V2 and V3 branches, can be described in terms of episodic lancinating pain with triggers (TN type 1) and/or constant dull discomfort (TN type 2), and is associated with a neurovascular conflict. Further, as our two cases highlight, a longstanding TN type 2 status is less likely to be cured by intervention, a well described TN treatment response characteristic.35 However, it carries three critical differences. TN due to dAVF appears to more commonly effect men, the underlying vascular abnormality is dangerous in that there is a risk of intracranial hemorrhage, and successful or even partial treatment of the dAVF often brings immediate, typically complete, and seemingly stable resolution of the TN for which the patient originally presented. The type of dAVF most commonly described as causing TN when this occurs is ‘tentorial’ in that the fistula central to the malformation is occurring along a tentorial leaflet. The neurovascular conflict leading to the TN most often involves an arterialized draining vein extending inferiorly where it contacts the trigeminal nerve, usually but not universally at the root entry zone. The well-known Borden or Cognard systems of classification of dAVFs can aid in prediction of their overall risk of rupture. However, tentorial dAVFs have been thoroughly

Dural Arteriovenous Fistula Presenting as Trigeminal Neuralgia

described to carry a risk of rupture much greater than those of any other location or class. These aggressive lesions are rarely discovered incidentally and have been quoted to rupture at a rate of 58-74%.44 In general, regardless of classification, it is preferred that these lesions be promptly treated. The general trend in treatment has moved toward transarterial or transvenous endovascular therapy with adjunctive open surgery only when necessary.44 Stereotactic radiosurgery has been described as a treatment option and occasionally demonstrated to be successful.36 However, risk of hemorrhage that persists while the lesion gradually involutes following treatment has been widely considered to be unacceptable.44 According to our literature review endovascular embolization, particularly transarterial, in treating TN due to dAVF is on the rise. It is widely recommended that any new case of TN warrants MRI early in the course of illness to rule out intraparenchymal, vascular, or other lesions that may be related to the facial pain experienced by patients. This review of TN due to dAVF further reinforces this recommendation as the TN experienced by patients due to dAVF is clinically identical in almost all respects to that typically seen in any primary care office. Suspicion for an underlying lesion rises if the patient is male and/or there are other neurological changes, such as the presence of a bruit.11 Indeed, although rare, missing the presence of a tentorial dAVF as the underlying cause of a new case of TN could potentially mean death or significant morbidity as these lesions carry a high risk of rupture and devastating intracranial hemorrhage. Treatment of the underlying dAVF often relieves the symptoms of TN without the need of ongoing medical therapy. We recommend that all new cases of TN undergo brain MRI including the posterior fossa with and without contrast enhancement and including posterior fossa selected balanced fast field echo sequencing in the axial plan as well as MRA10, with Computed Tomography (CT) based

Dural Arteriovenous Fistula Presenting as Trigeminal Neuralgia

methods used when MRI is contraindicated or unavailable. Any imaging evidence of a vascular malformation should further undergo a diagnostic cerebral angiogram, if not contraindicated. If a dAVF is discovered to be the underlying cause of TN, we recommend that treatment proceed immediately to the most appropriate definitive intervention for the dAVF. Medical therapy, such as carbamazepine, can be used to temporize the patient’s facial pain. In the interval between discovery and definitive treatment, we would recommend all antiplatelet and anticoagulant medications be halted to mitigate the recently discovered elevated risk of intracranial hemorrhage, unless significant comorbidities exist which require such treatments.

Acknowledgments The authors thank Tetsuro Nagasawa, MD, PhD, of the Raffles Japanese Clinic in Singapore for his aid in extracting critical information from the two manuscripts written in Japanese. We acknowledge Elena Paz Muñoz, BS, of OHSU’s Department of Neurosurgery in Portland, Oregon, USA, who aided in extracting critical information from the manuscript written in Spanish. We also acknowledge Tetiana Korzun, BA, BS, of OHSU School of Medicine’s MSTP Program in Portland, Oregon, USA, who aided in extracting critical information from the manuscript written in Russian. We thank Shirley McCartney, PhD, for her helpfulness in final edits to this manuscript.

Disclosure There is no conflict of interest to report, financial, personal, professional, or otherwise.

Dural Arteriovenous Fistula Presenting as Trigeminal Neuralgia

References 1. 2.

3.

4. 5. 6.

7. 8. 9.

10.

11.

12.

13.

14.

15. 16. 17. 18.

19.

Akhaddar A, Gazzaz M, Elmostarchid B, Boucetta M: Trigeminal neuralgia and dural arteriovenous fistula in an edentulous man. Headache 50:861-862, 2010 Al-Shahi R, Bhattacharya JJ, Currie DG, Papanastassiou V, Ritchie V, Roberts RC, et al: Prospective, population-based detection of intracranial vascular malformations in adults: the Scottish Intracranial Vascular Malformation Study (SIVMS). Stroke 34:1163-1169, 2003 Antonini G, Di Pasquale A, Cruccu G, Truini A, Morino S, Saltelli G, et al: Magnetic resonance imaging contribution for diagnosing symptomatic neurovascular contact in classical trigeminal neuralgia: a blinded case-control study and meta-analysis. Pain 155:1464-1471, 2014 Apfelbaum RI: Surgery for tic douloureux. Clin Neurosurg 31:351-368, 1983 Awad I: Dural arteriovenous malformations, in Spetzler R (ed): Neurovascular Surgery. New York: McGraw-Hill, 1995, pp 905-932 Borden JA, Wu JK, Shucart WA: A proposed classification for spinal and cranial dural arteriovenous fistulous malformations and implications for treatment. J Neurosurg 82:166-179, 1995 Borges A: Trigeminal neuralgia and facial nerve paralysis. Eur Radiol 15:511-533, 2005 Burchiel KJ: Trigeminal Neuralgia: New Evidence for Origins and Surgical Treatment. Neurosurgery 63 Suppl 1:52-55, 2016 Cognard C, Gobin YP, Pierot L, Bailly AL, Houdart E, Casasco A, et al: Cerebral dural arteriovenous fistulas: clinical and angiographic correlation with a revised classification of venous drainage. Radiology 194:671-680, 1995 Cruccu G, Finnerup NB, Jensen TS, Scholz J, Sindou M, Svensson P, et al: Trigeminal Neuralgia: New Classification and Diagnostic Grading for Practice and Research. Neurology 87:220-228, 2016 De Keukeleire K, Vanlangenhove P, Kalala Okito JP, Hallaert G, Van Roost D, Defreyne L: Transarterial embolization with ONYX for treatment of intracranial non-cavernous dural arteriovenous fistula with or without cortical venous reflux. J Neurointerv Surg 3:224-228, 2011 De Toledo IP, Conti Reus J, Fernandes M, Porporatti AL, Peres MA, Takaschima A, et al: Prevalence of trigeminal neuralgia: A systematic review. J Am Dent Assoc 147:570-576 e572, 2016 Du R, Binder DK, Halbach V, Fischbein N, Barbaro NM: Trigeminal neuralgia in a patient with a dural arteriovenous fistula in Meckel's cave: case report. Neurosurgery 53:216-221; discussion 221, 2003 Fukutome K, Nakagawa I, Park HS, Wada T, Motoyama Y, Kichikawa K, et al: Resolution of Trigeminal Neuralgia After Transvenous Embolization of a Cavernous Sinus Dural Arteriovenous Fistula. World Neurosurg 98:880 e885-880 e888, 2017 Ge H, Lv X, Jin H, He H, Li Y: Role of endovascular embolization for trigeminal neuralgia related to cerebral vascular malformation. Interv Neuroradiol 22:600-605, 2016 Grigorian Iu A, Stepanian MA: [Trigeminal neuralgia and tentorial dural arteriovenous malformation]. Zh Vopr Neirokhir Im N N Burdenko:46-51; discussion 52, 2010 Harders A, Gilsbach J, Hassler W: Dural AV malformation of the lateral and sigmoid sinuses as possible cause of trigeminal neuralgia. Case report. Acta Neurochir (Wien) 66:95-102, 1982 Hiramatsu M, Sugiu K, Hishikawa T, Haruma J, Tokunaga K, Date I, et al: Epidemiology of dural arteriovenous fistula in Japan: Analysis of Japanese Registry of Neuroendovascular Therapy (JRNET2). Neurol Med Chir (Tokyo) 54:63-71, 2014 Huang W, Yu J: A case of dural arteriovenous fistula at the foramen magnum presenting with trigeminal neuralgia. Interdisciplinary Neurosurgery 13:151-153, 2018

Dural Arteriovenous Fistula Presenting as Trigeminal Neuralgia 20. 21.

22.

23. 24. 25. 26. 27. 28.

29.

30.

31. 32. 33. 34. 35. 36.

37. 38. 39.

Ito M, Sonokawa T, Mishina H, Iizuka Y, Sato K: Dural arteriovenous malformation manifesting as tic douloureux. Surg Neurol 45:370-375, 1996 Ito M, Sonokawa T, Mishina H, Iizuka Y, Sato K: [Surgical interruption of draining vein or dural sinus: treatment for petrotentorial dural arteriovenous malformation]. No Shinkei Geka 26:123133, 1998 Jiang L, Qi M, Ye M, Li M, Bao Y, Liang J: Recurrent Secondary Trigeminal Neuralgia Caused by Obliterated Tentorial Dural Arteriovenous Fistula Cured with Surgical Resection: Case Report and Literature Review. World Neurosurg 121:243-248, 2019 Kontzialis M, Kocak M: Imaging evaluation of trigeminal neuralgia. J Istanb Univ Fac Dent 51:S62-S68, 2017 Li C, Li Y, Jiang C, Wu Z, Wang Y, Yang X: Remission of neurovascular conflicts in the cerebellopontine angle in interventional neuroradiology. J Neurointerv Surg 8:87-93, 2016 Li J, Ren J, Du S, Ling F, Li G, Zhang H: Dural Arteriovenous Fistulas at the Petrous Apex. World Neurosurg 119:e968-e976, 2018 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 Rep 2013, 2013 Lucas Cde P, Zabramski JM: Dural arteriovenous fistula of the transverse-sigmoid sinus causing trigeminal neuralgia. Acta Neurochir (Wien) 149:1249-1253; discussion 1253, 2007 Macdonald JH, Millar JS, Barker CS: Endovascular treatment of cranial dural arteriovenous fistulae: a single-centre, 14-year experience and the impact of Onyx on local practise. Neuroradiology 52:387-395, 2010 Martinez Rodriguez H, Meza Cano M: Neuralgia del trigemino como manifestacion de una fistula dural tentorial arteriovenosa tratada con terapia endovascular: Reporte de caso. Revista Mexicana de Neurociencia 17:116-123, 2016 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. Surg Neurol 66:519-523; discussion 523, 2006 Maurya V, Sreedhar CM, Khera A, Bhatia M, Sharma V: Trigeminal neuralgia: When does neurovascular contact turn into a conflict? Med J Armed Forces India 75:134-139, 2019 Mazurowski W, Sadowski Z: [Arterio-venous fistula of the posterior cranial fossa as a reason for trigeminal nerve neuralgia]. Czas Stomatol 19:641-643, 1966 Mendelowitsch A, Radue EW, Gratzl O: Aneurysm, arteriovenous malformation and arteriovenous fistula in posterior fossa compression syndrome. Eur Neurol 30:338-342, 1990 Mendes GA, Caire F, Silveira EP, Mounayer C: Dual-Microcatheter Technique for a Dural Arteriovenous Fistula Manifesting as Trigeminal Neuralgia. Clin Neuroradiol 26:117-120, 2016 Miller JP, Magill ST, Acar F, Burchiel KJ: Predictors of long-term success after microvascular decompression for trigeminal neuralgia. J Neurosurg 110:620-626, 2009 Okromelidze L, Vilanilam G, Gupta V, Trifiletti DM, Brown BL, Middlebrooks EH: Trigeminal Neuralgia Caused by Dural Arteriovenous Fistula in Meckel Cave Treated with Gamma Knife Radiosurgery. World Neurosurg 122:607-612, 2019 Ott D, Bien S, Krasznai L: Embolization of a tentorial dural arterio-venous fistula presenting as atypical trigeminal neuralgia. Headache 33:503-508, 1993 Rahme R, Ali Y, Slaba S, Samaha E: Dural arteriovenous malformation: an unusual cause of trigeminal neuralgia. Acta Neurochir (Wien) 149:937-941; discussion 941, 2007 Robert T, Blanc R, Ciccio G, Smajda S, Redjem H, Fahed R, et al: Trigeminal neuralgia due to arterialization of the superior petrosal vein in the context of dural or cerebral arteriovenous shunt. Clin Neurol Neurosurg 138:83-88, 2015

Dural Arteriovenous Fistula Presenting as Trigeminal Neuralgia 40.

41.

42.

43. 44.

45. 46.

47.

Ruiz-Juretschke F, Gonzalez-Quarante LH, Garcia-Leal R, Martinez de Vega V: Neurovascular Relations of the Trigeminal Nerve in Asymptomatic Individuals Studied with High-Resolution Three-Dimensional Magnetic Resonance Imaging. Anat Rec (Hoboken) 302:639-645, 2019 Saglam M, Anagnostakou V, Kocer N, Islak C, Kizilkilic O: Teaching NeuroImages: A rare cause of trigeminal neuralgia: dysplastic venous aneurysm of dural arteriovenous fistula. Neurology 84:e128-129, 2015 Schug SA DH, Stannard KJD: Pathophysiology of Pain, in Fitridge R TM (ed): Mechanisms of Vascular Disease: A Reference Book for Vascular Specialists. Adelaide (AU): University of Adelaide Press, 2011 Seo H, Yamagiwa O, O. N: A case of posterior fossa dural arteriovenous fistulae presening as trigeminal neuralgia. Shinkeinaika (Jpn) 34:429-432, 1991 Tomak PR, Cloft HJ, Kaga A, Cawley CM, Dion J, Barrow DL: Evolution of the management of tentorial dural arteriovenous malformations. Neurosurgery 52:750-760; discussion 760-752, 2003 Tsubaki S, Fukushima T, Tamagawa T, Miyazaki S, Watanabe K, Kuwana N, et al: Parapontine trigeminal cryptic angiomas presenting as trigeminal neuralgia. J Neurosurg 71:368-374, 1989 Wakuta N, Ueba T, Abe H, Nonaka M, Higashi T, Inoue T: Secondary trigeminal neuralgia caused by a tentorial dural arteriovenous fistula: a case report and literature review. Med Bull Fukuoka Univ 40, 2013 Zakrzewska JM, Linskey ME: Trigeminal neuralgia. BMJ Clin Evid 2014, 2014

Figure Legends Figure 1 Depicted is imaging for the patient in case report 1. Initial MRI imaging of the patient’s posterior fossa shows a FIESTA balanced fast field echo sequence with a large vessel running perpendicular to and compressing the left trigeminal nerve’s root entry zone (A). This vessel is understood to be a draining vein of a vascular lesion which becomes apparent at more superior axial cuts of the associated MRA in (B). Pre-intervention diagnostic cerebral angiogram depicts an oblique view of a left external carotid artery injection (C). A tentorial dAVF is plainly visualized with multiple feeding arteries arising off of the middle meningeal artery and branches of the occipital artery. Early venous drainage is observed to involve the vein of Galen with associated venous restrictive disease and a small varix. In dynamic imaging, reflux can be observed within the anterior vein of Galen extending into the straight sinus. On oblique

Dural Arteriovenous Fistula Presenting as Trigeminal Neuralgia

projection of a left internal carotid artery injection (D), there are multiple tentorial branches arising off of the meningohypophyseal trunk (MHT). There is an approximately 3mm aneurysm at the origin of the MHT. Early venous drainage is again observed, although less conspicuously, to lead to the vein of Galen. Not shown is a left vertebral artery injection which demonstrated multiple posterior meningeal artery feeder branches.

Figure 2 Depicted is imaging for the patient in case report 2. Pre-intervention contrast enhanced MRA of the brain in the axial view (A) and diagnostic cerebral angiogram in oblique lateral view of a right injection (B) demonstrates abnormal venous enhancement in the right infratemporal fossa representing vascular shunting to the venous system from branches of the external carotid artery (arrow) demonstrated to represent a large tentorial dAVF. (C) post-treatment axial T2w MRI of the brain demonstrates Onyx embolization material in the previously noted arteriovenous fistula (arrow). (D) post-treatment cerebral angiogram shows angiographic resolution of the fistula.

Table 1 – Literature Review of Dural Arteriorvenous Fistula causing clinical Trigeminal Neuralgia Manuscript Author(s), Year

Patient (n) and sex

Age (years)

Location and Borden Classification

Time to Medication Failure (medication)

TN type (division)

Mazurowski & Sadowski, 1966

1 male

47

Posterior R cranial fossa; Venous drainage N/S

0 months (Carbamazepine & Promazine)

Type 2a (V2 and V3)

Harders, Gilsbach, & Hassler, 1982

1 male

53

L transverse and N/A; new pain sigmoid sinus, Borden associated with the class 1 fistula occurred 5 months after a microvascular decompression

Mendelowitsch, Radue, & Gratzl, 1990

1 female

71

Tentorial, R sigmoid thrombosis, Borden class 3

Seo et al, 1991

1 female

59

Tentorial, Borden class 1

Ott, Bien, & Krasznai, 1993

1 female

56

Awad, 1995

1 patient (gender N/S)

elderly

Tentorial, Borden class 2

N/S (N/S)

N/S

Borden, Wu, & Shucart, 1995

1 patient (gender N/S)

39

superior petrosal sinus, Borden class 3

N/S (N/S)

N/S (N/S; described only as ‘facial pain’)

N/S

1 male

65

Petro-tentorial, Borden class 1

0 months (Carbamazepine)

TN 1 (V2&V3)

None

Ito et al, 1996

Additional Symptoms

Zone of NVC

Procedures

Positive Romberg Abnormal tangle 1) Trigeminal block of venous vessels 2) “Stereotactic analgesic sign, decreased sensation in affected in posterior fossa procedure” branches, intention tremor, pronator drift

Radiographic Outcome

Adverse Events

N/S

N/S

None

Prior type 1 treated surgically, later new type 2b (V3 and possibly V2

Pulsatile tinnitus

N/S (Carbamazepine)

N/A (V1&V2)

None

REZ, large ‘aneurysmal’ draining vein

1)Transarterial embolization x6 2)L temporal craniotomy with embolization

Complete Relief, follow-up N/S

14 years (Carbamazepine)

1 (V2)

None

Presumed REZ, draining veins

1)Multiple nerve blocks 2)Radiation to L S-shaped sinus 3)Transarterial embolization

Complete Relief, 18 months

Tentorial, partial 0 months TN1 for one filling defect of left (Carbamazepine & year, then TN2 sigmoid sinus, Borden Codeine) (V2&V3; notably class 2 familial TN)

Pulsatile tinnitus x10 years

Possible REZ 1)multiple dental extractions although and maxillary procedures uncertain, possible 2)L lateral suboccipital pulsatile craniectomy for microvascular distention of decompression petrosal veins 3)redo L lateral suboccipital craniectomy for ligation 4) repeat L lateral SOC for lateral and sigmoid sinus isolation from dura

Clinical Outcome

Residual fistula Complete Complete Relief, 4 Resolution, end after first months of procedure ligation leading to a third surgery for resolution

Partial Resolution, time of procedure

None

Partial Resolution, at time of procedure

None

N/S

Complete Resolution, at time of procedure

N/S

N/S

N/S

N/S

Complete Resolution, 20 months

Recurrent symptoms after first transarterial embolization, then failed relief

REZ, arterialized 1)Transarterial embolization x2 Complete and tortuous Relief, 16 draining basal months vein of Rosenthal

Transient focal REZ, arterialized 1)L Surgical tentorial leaflet neurologic venous varix excision & coil embolization of draining veins by needle symptoms referable puncture to rostral midbrain N/S, presumed REZ and arterialized draining vein

1)Surgical excision of dural nidus & ligation of draining vein

Partial Transient partial Resolution with trochlear nerve shrinkage of palsy, resolved draining vein, after time N/S time N/S

REZ, arterialized 1)Multiple trigeminal block Complete draining vein procedures Relief, 20 cross-pressing on 2)transarterial embolization x2 months nerve opposite 3)R lateral suboccipital superior cerebellar craniectomy for ligation and

Ito et al, 1998

2 males

artery

microvascular decompression

after second transarterial embolization

70

Petrotentorial, Borden class 2

N/A (seconds after subarachnoid & cerebellar hemorrhage)

N/A (V2 and V3)

ataxia

presumed REZ, arterialized draining vein; subarachnoid & cerebellar hemorrhage

1)Transarterial embolization 2)Lateral suboccipital craniectomy for ligation

Complete Complete Relief, 2 Resolution, 2 months months

None

68

Petrotentorial; Borden class 2

2 years (Carbamazepine)

1 (V2 and V3)

None

REZ, arterialized draining vein

1)Transarterial embolization 2)Lateral suboccipital craniectomy for ligation

Complete Complete Relief, 20 Resolution, 20 months months

None

bruit

Presumed REZ

1) Transvenous embolization Symptoms Complete with Guglielmi detachable coils reduced and resolution, end bruit of procedure resolved at 2 months followup

None

Tomak et al, 2002

1 female

55

L tentorial incisura, Borden class 3

N/S, presented after 15yrs of TN

N/S

Du et al, 2003

1 female

77

R Meckel’s cave to Superior Petrosal Sinus, Borden class 3

3 year 2 months (Gabapentin, acetaminophen & hydrocodone)

1 (V3)

Matsushige et al, 2006

1 male

50

Petrotentorial; Borden N/A; symptoms only class 2 for 1 month

Lucas & Zabramski, 2007

1 male

50

R Transverse-Sigmoid Sinus Junction, with venous aneurysm, Borden class 3

Rahme et al, 2007

1 male

30

Akhaddar et al, 2010

1 male

Grigorian et al, 2010

1 male

None; onset noted Gasserian to be with trauma to Ganglion, face serpiginous vein at Meckel’s cave

1)Multiple tooth extractions Complete Complete Post-Procedure 2)Multiple R Gasserian nerve Relief with Resolution, end Subarachnoid blocks slight R face of procedure Hemorrhage & 3)Transvenous coil reduced Hydrocephalus embolization assisted by sensation, 14 arterial embolization months 4)Ventriculoperitoneal shunt placement

1 (V2 and V3)

None

REZ, venous dilation

1)Gamma Knife Radiation

Complete Complete Relief aided Resolution; 3 by 1 year years with Carbamazepi ne; 3 years

None

5 years 2 months (Carbamazepine)

1 (V3)

Pulsatile tinnitus, “waterfall” sound

REZ, arterialized vein

1)R supra- & infra-tentorial craniotomy ligation & thrombosed sinus resection

Complete Complete Relief, 8 Resolution, 2 months months

None

Tentorial, Borden class 3

N/A

1 (V1)

None

REZ, ectatic 1)retrosigmoid craniectomy for venous ‘pouch’ of ligation draining vein

Complete Relief, 6 months

Complete Resolution, time of procedure

None

42

L Tentorial, Vein in L CPA, Borden class 1

1 year 2 months (N/S)

1 (V2 and/or V3)

None

REZ, arterialized 1)Multiple tooth extractions vein 2) L retrosigmoid craniectomy ligation

Complete Relief, 18 months

Complete Resolution, 18 months

None

72

L Tentorial, Veins in L parapontine region, Borden class 3

N/S (Carbamazepine)

1 (V2 and V3)

Hypoesthesia

REZ, tortuous loop of superior cerebellar artery & arterialized

Complete Relief, follow-up N/S

N/S

None

1)trigeminal nerve branch alcohol ablation 2)multiple trigeminal nerve blocks

cerebellar veins

3)pulsed radiofrequency trigeminal rhizotomy 1)L retrosigmoid craniectomy ligation and microvascular decompression

1 patient (Gender N/S)

N/S

N/S, Borden class 2 or 3

N/S

N/S

Headache, Proptosis

N/S

1)Endovascular treatment; unclear if transarterial or transvenous

Lu et al, 2013

1 male

58

L Tentoral, bilateral draining veins, Borden class 3

2 years 6 months (Carbamazepine)

1 (V2 and V3)

None

REZ, contralateral draining veins

1)Transarterial embolization

Wakuta et al, 2013

1 male

57

L Petrotentorial, Borden class 1

N/S (Carbamazepine)

1 (V3)

Pulsatile tinnitus

N/S

N/S

N/S

REZ, arterialized draining vein in all, one with large ectasia

1)Transarterial embolization

MacDonald et al, 2010

Robert et al, 2015

Saglam et al, 2015

5 patients Mean 37 Cerebellopontine x3, (Gender N/S) foramen magnum x1, tentorial x1; Borden class 3

N/S

N/S

Complete Complete Relief, 9 Resolution, 9 months months

Enlarged L 1)Transarterial embolization Complete Complete petrosal vein in 2)Lateral suboccipital relief Resolution, end cerebellopontine craniotomy for transposition of following of procedure cistern with SCA and arterialized petrosal craniotomy, normal veins vein N/S running to REZ Complete Complete Relief, mean Resolution, 6 11.4 months months

N/S

None x4; one patient experienced transient dysmetria due to iatrogenic venous hemorrhage

56

Tentorial, Borden class 2

N/S

1 (N/S)

N/S

REZ, dysplastic venous aneurysm of draining vein

N/S

Ge et al, 2016

4 male 2 female (6 total)

27-61

5 Tentorial, 1 Meckel’s cave; Borden class 1

N/S (Carbamazepine)

1 all (N/S)

N/S

N/S

1)Transarterial embolization for all, one with detachable coils as well 2) adjuvant gamma-knife radiation for 1 tentorial case

Li et al, 2016

4 patients (Gender N/S)

N/S

Tentorial, Borden class N/S

N/S (N/S)

N/S (N/S)

N/S

N/S; presumed REZ

1)Transarterial embolization, subtotal obliteration

Complete Relief, 48 months

No angiographic follow-up

N/S

N/S

Tentorial, Borden class N/S

N/S (N/S)

N/S (N/S)

N/S

N/S; presumed REZ

1)Transarterial embolization, partial obliteration

Complete Relief, 42 months

No angiographic follow-up

Initial aggravation of TN for 4 days, resolved

N/S

Tentorial, Borden class N/S

N/S (N/S)

N/S (N/S)

N/S

N/S; presumed REZ

1)Transarterial embolization x2

Complete Complete Relief, 27 Resolution, 8 months months

No relief after first embolization

6th decade

Tentorial, Borden class 1

N/S (N/S)

N/S (N/S)

N/S

REZ, variceal vein

1)Transarterial embolization, subtotal obliteration

Complete Subtotal Relief, 28 Obliteration, 6 months months

N/S

70

Tentorial, Borden

0 months

1

None

L cavernous sinus,

1)Gaserian ganglion block

Complete

None

1 male

N/S

None

1 male

Martinez Rodriguez

N/S

Transient worsening of facial pain

N/S

Transient Considerable Complete Relief, mean Resolution in 4, deficits in some, specifics N/S 57.3 months partial in 2, timing N/S

90%

& Meza Cano, 2016

class 3

(Carbamazepine,preg abalin, & levetiracetam)

(V1 and V2)

ectatic draining vein

2)transarterial embolization

Relief obliteration, no achieved angiographic with follow-up adjunctive medication, 6 months

Mendes et al, 2016

1 female

53

Inferior Petrosal Sinus, Borden class 2

1 month (Carbamazepine)

1 (V2)

None

REZ, arterialized draining vein

1)Transvenous coil embolization

Complete Complete Relief, 6 Resolution, 6 months months

None

Fukutome et al, 2017

1 female

75

R Cavernous Sinus near Meckel’s cave to bilateral inferior petrosal sinuses, Borden class 1

0 months (N/S)

2b (V1 and V2)

None

Gasserian Ganglion, pulsatile venous flow in posterior cavernous sinus

1)Transvenous coil and Onyx embolization

Complete Complete Relief, 13 Resolution, 13 months months

Mild transient right abducens nerve palsy, resolved at 1 month

1 male

35

Foramen magnum, Borden class 3

0 months (Carbamazepine)

1 (N/S)

None

REZ, dilated draining veins

1)Microsurgical resection

“great Complete remission”, resolution, end 1 year of procedure

None

4 patients (Gender N/S)

N/S

Tentorial, Borden class 3 in three, class 2 in one

N/S (N/S)

N/S (N/S)

N/S

REZ, dilate draining vein

Three patients underwent transarterial embolization followed by microsurgery, one underwent only transarterial embolization

1 male

57

Tentorial, Borden class 3

2 years, (Carbamazepine)

1 (V2 and V3)

None

REZ, arterialized draining vein

1 female

71

Tentorial, with small venous aneurysm, Borden class 2

8 years, (Carbamazepine)

1 (V1)

None

REZ to Meckel’s cave, multiple tortuous draining veins

1)Gamma Knife radiation therapy

1 male

55

L Tentorial, with small arterial aneurysm, Borden class 3

0 months, (Carbamazepine)

2a (V2>V3)

None

REZ, arterialized draining vein

1)Transarterial embolization

1 female

72

R Tentoral, Borden class 1

0 months, numerous medications attempted

2a (V2 and V3)

Tinnitus

REZ, arterialized draining vein

Huang & Yu, 2018

Li et al, 2018

Jiang et al, 2019

Okromelidze et al, 2019

Present report

Complete Relief, follow-up N/S

1)Transarterial embolization Complete 2)R retrosigmoid craniectomy Relief, 5 for ligation and nidus resection months

N/S

1) Complete Recurrence after embolization; Resolution at post-op transient time of R hypoesthesia procedure x1 week 2) compressive lesion caused by embolized vessels resolved 5 days post-resection

Complete Decrease size Relief, 6 of abnormal months vessels, 6 months Complete Relief, 5 months

1)sinus surgery No Relief 2)orthodontal surgery from TN, tinnitus 3)radiatiosurgery 4)balloon compression resolved, 1 month rhizotomy 5)percutaneous stimulation 6)Transarterial embolization 7)microvascular decompression with internal neurolysis

N/S

None

Complete Resolution, 4 months

Severe left sided headache improving with steroids and time

Partial Resolution, 1 month

Ongoing face pain unchanged, face numbness after open surgery

Abbreviations: R = right; L = left; CPA = cerebellopontine angle; REZ = root entry zone; N/S = not specified; N/A = not applicable; NVC = neurovascular contact

Abbreviations Dural arteriovenous fistulae (dAVF) root entry zone (REZ) trigeminal neuralgia (TN) magnetic resonance imaging (MRI) magnetic resonance angiography (MRA)

Disclosure The authors have no conflict of interest to report, financial, personal, professional, or otherwise.

Acknowledgments The authors thank Tetsuro Nagasawa, MD, PhD, of the Raffles Japanese Clinic in Singapore for his aid in extracting critical information from the two manuscripts written in Japanese. We acknowledge Elena Paz Muñoz, BS, of OHSU’s Department of Neurosurgery in Portland, Oregon, USA, who aided in extracting critical information from the manuscript written in Spanish. We also acknowledge Tetiana Korzun, BA, BS, of OHSU School of Medicine’s MSTP Program in Portland, Oregon, USA, who aided in extracting critical information from the manuscript written in Russian. We thank Shirley McCartney, PhD, for her helpfulness in final edits to this manuscript.