Abstract
Objective
The objective of this article is to describe the trigeminal neuralgia related to cerebral vascular malformation that is rarely reported and the experience referring to endovascular treatment.
Patients and methods
A total of 10 patients who had cerebral vascular malformation (AVM and dAVF) in a single center presented with trigeminal neuralgia. Clinical and angiographic presentations as well as their clinical outcomes after embolization were reviewed.
Results
Of the 10 cases, seven dAVFs and three AVMs were detected. In contrast to the dilated feeding arteries, an ectasia of the draining vein that is adjacent to the root entry zone of the trigeminal nerve such as the petrosal vein and lateral mesencephalic vein has the major role in causing the trigeminal neuralgia. All of these patients had relief of facial pain after endovascular embolization during follow-up (mean 57.3 months, range 5 to 100 months). There were no permanent neurological deficits.
Conclusions
Endovascular embolization is an effective method in treating trigeminal neuralgia related to cerebral vascular malformation.
Keywords: Trigeminal neuralgia, endovascular embolization, arteriovenous malformation, dural arteriovenous fistula
Introduction
Trigeminal neuralgia commonly presents as a serious paroxysmal facial pain and its incidence is 4.7/100,000.1 Compression at the root entry zone of the trigeminal nerve by proximal vessels such as the basilar artery, superior cerebellar artery (SCA) or anterior inferior cerebellar artery (AICA) is identified as the main cause of trigeminal neuralgia.2 Arteriovenous malformations (AVMs) and dural arteriovenous fistulas (dAVFs) are rarely reported as the cause of trigeminal neuralgia in the literature.3,4 Classical treatment of trigeminal neuralgia including microvascular decompression, radiosurgery and percutaneous ablative procedures have resolved the majority of cases.5 However, there is no sufficient experience referring to endovascular treatment on trigeminal neuralgia related to vascular malformation.6,7 In this study, we retrospectively reviewed 10 cases of trigeminal neuralgia secondary to AVM and dAVF treated by transarterial embolization and their long-term clinical outcomes.
Materials and methods
Patient demographics
This study was approved by the ethics committee of Beijing Tiantan Hospital. All patients gave written informed consent to participate and the privacy of patients was strictly protected. We reviewed 577 patients with AVMs and 486 patients with dAVFs who were treated by endovascular embolization in our hospital between 2007 and 2015. Clinical characteristics, including demographic information (age, sex, clinical presentation), radiological findings such as computed tomography angiography (CTA), magnetic resonance angiography (MRA), digital subtraction angiography (DSA) and medical reports were retrospectively reviewed. We retrospectively identified 10 consecutive cases of presenting trigeminal neuralgia. Inclusion criteria were the following: clinical symptoms of trigeminal neuralgia such as facial pain, either occasional pain or constant throbbing sensations, imaging evidence on CTA or MRA and DSA of AVM and dAVF situated along the trigeminal nerve route, treatment with carbamazepine is ineffective or if side effects of the medication are unacceptable, and follow-up with either imaging or clinical interviews. These cases included four males and six females and the mean age was 39.3 years (range 19–61 years).
Endovascular treatment and follow-up
All 10 cases received endovascular embolization under general anesthesia and continuous electrophysiological monitoring. During the procedure, we chose ethylene vinyl alcohol copolymer (Onyx, ev3 Neurovascular, Irvine, CA, USA) for nidus embolization or parent arteries occlusion. Postoperative immediate radiography was used to confirm the decreased size of the nidus and the feeding vessels. As an assistant treatment method, radiosurgery (gamma knife) was performed after endovascular obliteration.
Clinical follow-up was supplemented by telephone or outpatient interview in all cases; angiographic follow-up was obtained for six treated cases. We identified the significant relief of trigeminal neuralgia combining the modified Rankin Scores (mRS) ≤ 2 as good clinical outcome.
Results
Baseline clinical data
All patients who presented with trigeminal neuralgia were treated with carbamazepine initially, but without satisfactory results regarding symptom improvement. The baseline characteristics of each case are presented in Table 1. Of these 10 cases, two presented with sharp pains located at the distribution area of the first trigeminal branch, six cases at the second trigeminal branch and two cases at the third trigeminal branch. One individual had a history of intracranial hemorrhage and was treated conservatively before our hospital admission.
Table 1.
Demographics and clinical outcomes of endovascular embolization for trigeminal neuralgia.
| No. | Age | Sex | Pathology | Location | Symptoms | Feeding arteries | Venous drainage | Venous compression | Treatment summary | Final occlusion | Complication | Clinical outcome | Pain relief |
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| 1 | 37 | M | DAVF | Tentorium | Trigeminal neuralgia | MMA AMA | PV LMV | Varix | Onyx | Complete | Facioplegia, Pain allergy | Good | Complete |
| 2 | 51 | F | DAVF | Tentorium | Trigeminal neuralgia | MMA | PV SOV | Varix | Onyx | Complete | Ptosis, Facial numbness, facioplegia | Good | Complete |
| 3 | 55 | M | DAVF | Tentorium | Trigeminal neuralgia | MMA MHT | PV LMV | SPS | Onyx GKR | Complete | Facial hypesthesia | Good | Complete |
| 4 | 61 | M | DAVF | Meckel’s cave | Trigeminal neuralgia | MMA MHT | PV LMV | SPS | Onyx | Near-complete | N | Good | Complete |
| 5 | 43 | M | DAVF | Tentorium | Trigeminal neuralgia | MMA APA | PV | Varix | Onyx | Partial | N | Good | Alleviative |
| 6 | 32 | F | AVM | Cerebellar hemisphere | Trigeminal neuralgia | SCA AICA | LMV SVV | PV | Onyx | Near-complete | N | Good | Alleviative |
| 7 | 19 | F | AVM | Cerebellar hemisphere | Trigeminal neuralgia | SCA AICA | LMV BVR | N | Onyx | Partial | N | Good | Complete |
| 8 | 24 | F | AVM | Cerebellar hemisphere | Trigeminal neuralgia, hemorrhage | SCA PCA AICA | LMV BVR | LMV | Onyx GKR | Complete | N | Good | Complete |
| 9 | 44 | F | AVF | Temporop-arietal area | Trigeminal neuralgia | MCA PCA | SSS T-SS | N | Coiling Onyx | Complete | Facial pain aggravation | Good | Alleviative |
| 10 | 27 | F | DAVF | Tentorium | Trigeminal neuralgia | MHT APA | PV LMV | PV | Onyx | Complete | N | Good | Complete |
MMA: middle meningeal artery; AMA: accessory meningeal artery; MHT: meningo-hypophyseal trunk; APA: ascending pharyngeal artery; SCA: superior cerebral artery; AICA: antero-inferior cerebellar artery; PCA: posterior cerebral artery; PV: petrosal vein; LMV: lateral mesencephalic vein; SOV: superior ophthalmic artery; SVV: superior vermian vein; BVR: basal vein of Rosenthal; SSS: superior sagittal sinus; T-SS: transverse-sigmoid sinus; SPS: superior petrosal sinus; Y: yes; N: no; GKR: gamma knife radiosurgery; M male; F: female.
Imaging data
There were five dAVFs located at the tentorium and one dAVF at Meckel’s cave. These cases were fed by branches of the middle meningeal artery, clival branches of the meningo-hypophyseal trunk or the branches of the ascending pharyngeal artery. DSA revealed that all of the dAVFs had venous drainage through the petrosal vein and five involved the lateral mesencephalic vein. One fistula at the temporoparietal area was fed by branches of the middle cerebral artery and posterior cerebral artery. The blood was drained into the superior sagittal sinus directly and then the dilated transverse-sigmoid sinus. For three AVMs at the cerebellar hemisphere, all of cases had multiple arterial feeders, and at least the SCA and the AICA were involved. One case was supplied by the postero-inferior cerebellar artery (PICA). The AVM venous drainage was the lateral mesencephalic vein and then basal vein of Rosenthal. Large ectasia of venous drainage or dysplastic venous varix were detected in eight of 10 cases.
Endovascular procedural data
All of these 10 cases were treated by transarterial embolization. Nine cases were embolized by conventional Onyx injection (three AVMs and six dAVFs); one high-flow fistula was embolized by detachable coils combined with Onyx. Six cases (five AVFs and one AVM) achieved complete occlusion with multiple embolization sessions and four cases (two dAVFs and two AVMs) were occluded near-completely or partially. Two cases received gamma-knife radiosurgery therapy after the first incomplete embolization procedure. Figures 1 and 2 show that two cases with trigeminal neuralgia that were caused by dAVF and AVM had complete occlusion of vascular malformation. Table 2 briefly showed literature which reported cases of trigeminal neuralgia associated with AVM or dAVF treated by Onyx.
Figure 1.
(a) Axial T2-weighted MR image shows venous dilation compressing the right entry zone of the trigeminal nerve root. Lateral views of angiography (b) shows a dural fistula of tentorium fed by branches of the right MMA and AMA, with venous drainage through the petrosal vein and lateral mesencephalic vein. Large venous varix was noted. (c) Postoperative angiogram demonstrates complete occlusion of the dural fistula. MMA: middle meningeal artery; AMA: accessory meningeal artery.
Figure 2.
(a) Axial cranial MR imaging (T2 sequence) shows a vessel malformation nidus on the left cerebellar hemispheres with a signal flow void compressing the left trigeminal nerve root. ((b), (c)) Lateral views of angiography demonstrates this AVM was fed by branches of the left PCA, SCA and AICA, with the drainage veins of the dilated lateral mesencephalic vein. (d) Angiography during follow-up reviewed no residual of nidus. MR: magnetic resonance; AVM: arteriovenous malformation; PCA: posterior cerebral artery; SCA: superior cerebellar artery; AICA: anterior inferior cerebellar artery.
Table 2.
Reported cases of trigeminal neuralgia associated with AVM or dAVF treated by Onyx.
| Study | Location | Feeding arteries | Venous drainage | Occlusion rate | Pain relief | Complications |
|---|---|---|---|---|---|---|
| Robert et al.6 reported 10 cases | Cerebellar hemisphere, vermis, cerebellopontine cistern, | SCA, AICA, PICA | PV | Eight complete; two near-complete | All complete | Two hypoesthesia |
| foramen magnum, tentorium | MMA, MHT, AICA | PV | ||||
| Lesley8 | CPA | SCA, PICA | Not mentioned | Near-complete | Complete | No |
| Lu et al.9 | Tentorial | MMA, MHT | PV, SCHV | Near-complete | Complete | No |
| Dou et al.10 | Cauda cerebelli | SCA | Straight sinus | Near-complete | Complete | No |
| Levitt et al.11 | Posterior fossa | IMA, MMA, AICA | Not mentioned | Complete | Complete | No |
AVM: arteriovenous malformation; dAVF: dural arteriovenous fistulas; CPA: cerebellopontine angle; SCA: superior cerebellar artery; PICA: posteroinferior cerebellar artery; AICA: anterior inferior cerebellar artery; IMA: internal maxillary artery; MMA: middle meningeal artery; MHT: meningohypophyseal trunk; PV: petrosal vein; SCHV: superior cerebellar hemispheric vein; VA: vertebral artery; ECA: external carotid artery; ACA: anterior cerebral artery; MCA: middle cerebral artery; PCA: posterior cerebral artery; ICV: internal cerebral vein.
Outcome and adverse effects
All cases had considerable symptom relief after endovascular treatment of trigeminal neuralgia at a mean follow-up period of 57.3 months (range five to 100 months). Among them, seven cases (six complete embolizations and one partial embolization) had complete relief of trigeminal neuralgia and there was no evidence of recurrence; three cases of incomplete embolization achieved significant improvement of facial pain. Angiographic follow-up was obtained for six of 10 (60.0%) endovascular-treated patients and no significant recurrence was detected. There were four cases having transient procedure-related neurological deficits after the first embolization session: one oculomotor nerve palsy, one facioplegia, one facial hypesthesia and one facial prosopospasm. These neurological deficits completely resolved within five to 60 days after the procedure.
Discussion
Most cases of trigeminal neuralgia (80%–90%) are caused by the compression of the fifth cranial nerve in its root entry zone.6,12 The offending vessels are commonly recognized as a branch of the superior cerebellar artery (SCA) or AICA.13 Infrequent intracranial lesions such as AVM or dAVF could result in secondary trigeminal neuralgia by compression.14 Lesley et al. indicated that only 59 cases had been described as trigeminal neuralgia related to AVM from 1936 to 2011.8 McLaughlin et al. reported a large series of trigeminal neuralgia that was treated by surgical operation and indicated that only 0.6% to 1.5% of cases were associated with AVM.15 In our institution, the cases of cerebrovascular malformation accounted for approximately 0.1% of all patients who presented with trigeminal neuralgia.
For the isolated cases of the trigeminal neuralgia related to AVM that have been described in the literature, the majority of AVM nidus were located at the unilateral cerebellar hemispheres. The most common feeding arteries were branches of the SCAs and the AICA.6,16,17 DAVF could be at the location of the tentorium, the cerebellopontine cistern, Meckel’s cave or the foramen magnum and could be supplied by branches of the middle meningeal artery, meningo-hypophyseal trunk or accessory meningeal artery.6,8,18 In the literature, the majority of draining veins of AVMs and dAVFs were identified as the deep venous system such as the basal vein of Rosenthal and the petrosal vein.6,16 For AVMs, direct compression of adjacent vessels or feeding arteries could be the main cause of trigeminal neuralgia.6 On the other hand, dAVFs could cause a flow-related arterial aneurysm or large venous ectasia, which have the potential of stretching the trigeminal nerve root. Robert et al. reported three cases of flow-related aneurysm in the nidus and two cases of large ectasia that created a major compression of the trigeminal nerve.6 Lucas and Zabramski described a single case of a dAVF involving the right transverse-sigmoid sinus junction with a dysplastic venous varix.18 Matsushige et al. showed a dAVF supplied by the middle meningeal artery and tentorial artery, and then draining into the petrosal vein with a large venous varix at the root entry zone of the trigeminal nerve.19 Comparing with the arterial compression of the SCA, trigeminal neuralgia associated with AVM or dAVF commonly had abnormal venous drainage or arterialized veins adjoining to the course of the trigeminal nerve.20
Endovascular embolization not only reduces the nidus size, but also relieves trigeminal neuralgia quickly and relatively safely by decreasing blood flow and thinning the feeding vessels.13 Lu et al. reported a case of trigeminal neuralgia associated with unilateral tentorial dAVF treated by transarterial Onyx embolization and had immediate resolution of the patient’s facial pain.9 Another report described a case presenting with paroxysmal facial pain that was caused by the compression of a huge AVM.10 The nidus was partially embolized with Onyx and the patient was completely pain free during 14 months of follow-up. Wanke et al. reported a case of AVM embolization was effective for pain relief.21 Robert et al. showed 10 similar cases of trigeminal neuralgia related to vascular malformation and nine completely resolved after embolization.6
However, complete obliteration of the nidus is not always easy, and the complications from the embolization procedure should not be neglected in determining treatment strategy.22,23 Lesley reported a patient complaining of initial worsening of facial pain after embosurgery but soon improved.8 Du et al. showed a case of trigeminal neuralgia caused by the compression of dAVF and treated by endovascular embolization. Unfortunately, the patient suffered lethargic, serious headache and diffuse subarachnoid hemorrhage that likely resulted from perforation of a vessel during the embolization procedure.5 The literature described a case of immediate relief of trigeminal pain after embolization and a small area of hypesthesia on the left cheek.11 There was also a report referring to the axonotmetic injuries of the trigeminal nerve caused by microcatheter traction as it was being pulled from the Onyx cast.7 The effectiveness of gamma knife radiosurgery for AVM nidus and trigeminal neuralgia relief was also reported.24,25
Conclusion
Trigeminal neuralgia is a rare manifestation of AVM and dAVF. Ectasia or abnormal tributaries of the drainage vein plays an important role in causing secondary trigeminal neuralgia. Endovascular embolization not only effectively resolves the trigeminal neuralgia related to vascular malformation but also eliminates the nidus of vascular malformation.
Acknowledgments
We are grateful to Dr Xinjian Yang, Dr Chuhan Jiang and Dr Yuhua Jiang for the data collection.
Declaration of conflicting interests
The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This article is supported by the National Natural Science Foundation of China (81471166).
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