Current Insights and Management Strategies for Lower Cervical Arteriovenous Fistulas: A Comprehensive Review

Abstract

Lower cervical arteriovenous fistulas (AVFs) are rare and complex vascular malformations that pose significant clinical challenges due to their location and variable presentation. While upper cervical AVFs have been extensively studied, lower cervical AVFs remain underresearched. This study aims to review the clinical presentations, management strategies, and outcomes of patients with lower cervical AVFs to enhance understanding and improve treatment approaches. We conducted a retrospective analysis of patients with spinal vascular malformations treated at our institute between June 2006 and December 2023, identifying two cases of lower cervical AVFs. Additionally, a systematic literature review was performed following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines, including 44 patients with lower cervical AVFs, using databases such as Ovid MEDLINE, PubMed, and Cochrane. Data collected included patient demographics, clinical presentation, fistula type, arterial and venous involvement, treatment modality, and neurological outcomes. Among the 44 patients with lower cervical AVFs, including our two cases, 50% were female, and the mean age was 48.68 years (range: 4–76 years). Clinical presentations varied, with 27.3% experiencing hemorrhage, 18.2% presenting with myelopathy, and 18.2% remaining asymptomatic. Venous drainage patterns played a significant role in symptom severity, with complex perimedullary and retrograde venous drainage contributing to worse outcomes. Treatment included endovascular embolization (40.9%), surgical resection (25%), and combined approaches (18.2%), with good recovery achieved in 54.5% of cases. Lower cervical AVFs present diverse clinical challenges due to their variable presentations and complex vascular anatomy. Early diagnosis and tailored management, including endovascular embolization and surgical resection, are essential for optimizing patient outcomes. Further research is needed to better understand the natural history of asymptomatic AVFs and improve treatment protocols.

 

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Keywords

lower cervical arteriovenous fistulas - spinal dural arteriovenous fistula - epidural arteriovenous fistulas - perimedullary arteriovenous fistulas - radicular arteriovenous fistulas - spinal cord venous infarction

Introduction

Spinal vascular malformations, including arteriovenous fistulas (AVFs) and arteriovenous malformations, can occur throughout the entire spine, from the craniocervical junction to the sacral region. Their clinical presentation and treatment options vary significantly depending on their location and type.[1] [2] Among these malformations, cervical AVFs represent a unique and complex subset, which can be further categorized into four primary subtypes based on their anatomical location and vascular characteristics: epidural, dural, radicular, and perimedullary.[3] [4] [5]

Epidural AVFs (EAVFs) are located in the epidural space, outside the dura mater, whereas dural AVFs (DAVFs) involve abnormal connections between arteries and veins within the dura. Radicular AVFs (RAVFs) affect the nerve roots, involving abnormal arterial-venous communications, while perimedullary AVFs (PAVFs) are situated near the spinal cord itself but do not directly involve the cord.[2] [6] [7] [8] Each of these subtypes has distinct clinical implications and treatment challenges, underscoring the complexity of managing cervical AVFs.

Cervical AVFs can be classified into two categories: upper cervical AVFs, occurring at the craniocervical junction (C1-C2), and lower cervical AVFs, which are located below C2.[3] [9] While upper cervical AVFs have been extensively studied and analyzed in numerous publications, lower cervical AVFs remain comparatively underresearched and less well understood.[1] [3] [10] [11] [12] Despite advancements in imaging techniques and treatment modalities, the management of lower cervical AVFs continues to present significant clinical challenges. Both endovascular embolization and surgical resection remain viable treatment options, with the choice of intervention determined by the complexity of the fistula, its angioarchitecture, and patient-specific factors. This study aims to review the clinical presentations, management strategies, and outcomes of patients with lower cervical AVFs, contributing to a better understanding of this rare condition and guiding optimal treatment approaches.

 

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Materials and Methods

The authors retrospectively analyzed patients with spinal vascular malformations treated at our institute between June 2006 and December 2023. From a total of 94 cases involving spinal vascular malformations from the upper cervical to sacral regions, two cases of lower cervical AVFs were identified.

Following the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) guidelines, the authors conducted a systematic review of previously reported cases and case series that provided sufficient clinical descriptions and clear imaging demonstrating lower cervical AVFs. A literature search was performed using Ovid MEDLINE, PubMed, Cochrane Database of Systematic Reviews, and Google Scholar (1987–2024), employing the following keywords: “cervical arteriovenous fistulas,” “lower cervical arteriovenous fistulas,” “cervical epidural arteriovenous fistulas,” “cervical radicular arteriovenous fistulas,” and “cervical perimedullary arteriovenous fistulas.” Non-English articles, commentaries, and expert opinion pieces were excluded. Additional relevant articles were identified through the reference lists of included studies. Vertebro-vertebral fistulas were also excluded due to their high-flow nature, distinct pathophysiology, and different clinical management compared to lower cervical AVFs, to ensure the review focused specifically on the latter.

The lower cervical AVFs in this review were categorized into four types based on the anatomical location and involved vascular structures. DAVFs occur within the dura mater and involve abnormal connections between dural arteries and veins. EAVFs are located in the epidural space, outside the dura mater, and involve complex vascular connections. RAVFs involve the nerve roots, with abnormal connections between radicular arteries and veins. PAVFs are located near the spinal cord but do not directly involve the cord itself.

The two patients from our institute, along with those reported in the literature, were reviewed and evaluated by two experienced neuroradiologists (P.L. and C.A.). Collected data included demographic information (patient gender and age), clinical presentation, fistula type, side of the fistula, arterial feeders, venous drainage, treatment, and neurological outcomes following treatment.

Case Illustration 1

A 39-year-old woman was admitted to a local hospital presenting with progressive quadriparesis over 2 months. One week prior to admission, she developed bowel and bladder dysfunction. She had no significant past medical history or history of trauma. Initial magnetic resonance imaging (MRI) of the cervicothoracic spine revealed abnormally high-signal intensity from the lower brainstem to the mid-thoracic cord, suggestive of venous congestion, with intradural flow voids along both the anterior and posterior surfaces of the spinal cord ([Fig. 1A]). A provisional diagnosis of spinal DAVF was made.

Fig. 1 Case illustration 1. Lower cervical epidural arteriovenous fistula. (A) Sagittal T2-weighted magnetic resonance imaging of the cervicothoracic spine showed abnormally high-signal intensity from the lower brainstem to the mid-thoracic cord, indicative of venous congestion, with intradural flow voids evident along both the anterior and posterior surfaces of the spinal cord. Anteroposterior views of (B) contrast-enhanced magnetic resonance angiography of brachiocephalic trunk and vertebrobasilar system, and (C) angiographic image, (D) three-dimensional (3D) reconstruction image, and (E, F) maximum intensity projection reformatted images of angiographic computerized tomography of the right costocervical trunk revealed a spinal epidural arteriovenous fistula along the C8 nerve (C7-T1 vertebral foramen). This fistula is supplied by an enlarged deep cervical artery with prominently engorged draining veins extending rostrally to the pial venous network around the medulla and caudally to the thoracic spinal cord. A venous pouch is indicated by arrowheads.

The patient was subsequently transferred to our institution for further evaluation and management. Neurological examination revealed spastic quadriparesis with muscle strength rated at 3/5, loss of pinprick sensation below the L1 level, hyperreflexia in the upper and lower extremities, clonus, and a positive Babinski sign. Contrast-enhanced magnetic resonance angiography (MRA) indicated a likely spinal EAVF with a small vascular pouch in the right C7-T1 intervertebral foramen, supplied by a feeder from the deep cervical artery. Engorged draining veins were noted extending rostrally to the pial venous network around the medulla and caudally to the thoracic spinal cord ([Fig. 1B]).

Endovascular treatment was planned for the following day. However, the patient developed chest pain, worsened quadriparesis (muscle strength 1/5), and shortness of breath the next morning, necessitating intubation due to hypoxemia. Emergency endovascular treatment was performed, during which spinal angiography and angiographic computed tomography of the right costocervical trunk confirmed the presence of a spinal EAVF along the C8 nerve root ([Fig. 1C–F]). Transarterial embolization using a small amount of N-butyl-2-cyanoacrylate (NBCA) successfully occluded the fistula, the venous pouch, and the proximal draining vein ([Fig. 2A–C]).

Fig. 2 Case illustration 1. Lower cervical epidural arteriovenous fistula. (A) Anteroposterior view of superselective angiographic image of the right deep cervical artery clearly demonstrated a spinal epidural arteriovenous fistula and venous pouch (arrowhead). (B) Image during embolization showed the glue penetrating the fistula and proximal vein. (C) Postembolization image from the right costocervical trunk injection confirmed complete obliteration of the fistula. Sagittal T2-weighted magnetic resonance imaging at (D) 4 months, (E) 2 years, and (F) 5 years after embolization revealed complete and lasting resolution of venous congestion. (G) Contrast-enhanced magnetic resonance angiography of brachiocephalic trunk and vertebrobasilar system obtained 5 years following embolization confirmed no recurrence of the fistula.

The patient was extubated the following day, with rapid recovery of upper extremity strength. Her bowel and bladder functions gradually improved. Follow-up MRI and MRA at 4 months, 2 years, and 5 years postembolization showed complete and sustained resolution of venous congestion with no recurrence of the fistula ([Fig. 2D–G]). At the 5-year follow-up, she was able to walk with a walker and reported no issues with bowel or bladder function after an extensive rehabilitation program.

 

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Case Illustration 2

A 49-year-old woman presented with chronic neck pain and numbness radiating into the left shoulder for 2 years. Neurological examination revealed decreased pinprick sensation in the left C5 dermatome without muscle weakness, and mild hyperreflexia in both upper and lower extremities. Clonus was present, and the Babinski sign was absent. Cervical MRI displayed faintly abnormal high-signal intensity in the cervical cord, with subtle intradural flow voids evident along the posterior surface of the spinal cord. Further imaging with three-dimensional T2-SPACE highlighted more pronounced intradural flow voids ([Fig. 3A–C]). MRA of the brachiocephalic trunk and vertebrobasilar system indicated a potential spinal DAVF along the C5 nerve, supplied by the left ascending cervical artery with engorged draining veins extending rostrally to the pial venous network around the upper cervical cord ([Fig. 3D]).

Fig. 3 Case illustration 2. Lower cervical dural arteriovenous fistula. (A) Sagittal T2-weighted magnetic resonance imaging of the cervical spine showed faint abnormally high-signal intensity of the cervical cord with subtle intradural flow voids evident along the posterior surface of the spinal cord. (B) Sagittal three-dimensional (3D) T2-SPACE image demonstrated more prominent of intradural flow voids (white arrowheads). (C) Coronal T2 turbo inversion recovery magnitude (TIRM) image showed intradural flow voids along the left-sided cervical cord. Anteroposterior (AP) views of (D) contrast-enhanced magnetic resonance angiography and (E) angiography of brachiocephalic trunk and vertebrobasilar system revealed a spinal dural arteriovenous fistula (arrow) along the C5 nerve supplied by the left ascending cervical artery with engorged draining veins extending rostrally to the pial venous network around the upper cervical cord. (F) Lateral view of the left ascending cervical artery injection disclosed dilated perimedullary vein (black arrowheads) along the left-side cervical cord. (G) AP view of the left ascending cervical artery injection in venous phase illustrated venous outlet pathways (asterisks) of the fistula via the right deep cervical and left C8 epidural veins.

Subsequent spinal angiography performed 2 months later confirmed the presence of a left C5 DAVF with venous drainage into engorged veins extending along the posterior aspect of the cervical cord through a left-sided dilated perimedullary vein and venous outlet pathways of the fistula via the right deep cervical and left C8 epidural veins ([Figs. 3E–G] and [4A, B]). In addition, cerebral angiography revealed an unruptured saccular aneurysm located at the left supraclinoid internal carotid artery, measuring 3.2 mm by 2.5 mm in width and height, with a neck of 2.2 mm. Transarterial embolization through the left ascending cervical artery using NBCA successfully occluded the fistula and proximal draining vein ([Fig. 4C–E]). However, the embolic material inadvertently extended beyond the targeted proximal vein into a vein located at the posterolateral aspect of the C4 cord ([Fig. 4F, G]).

Fig. 4 Case illustration 2. Lower cervical dural arteriovenous fistula. (A) Anteroposterior (AP) and (B) lateral views of the superselective left ascending cervical artery injection clearly showed a spinal dural arteriovenous fistula (arrow) along the C5 nerve with venous drainage into engorged draining veins extending rostrally and caudally along the posterior aspect of the cervical cord through a left-sided dilated perimedullary vein (arrowhead). The venous outlet pathways (asterisks) were noted at the right deep cervical and left C8 epidural veins. (C) During embolization, the glue cast penetrated into the fistula and draining vein. (D) AP and (E) lateral views of the left ascending cervical artery following embolization confirmed complete obliteration of the fistula. (F) Sagittal and (G) coronal views of Dyna computerized tomography image after glue embolization demonstrated the glue cast at the posterolateral aspect of the C4 cord.

Immediately postembolization, the patient exhibited no neurological complications. However, the following day, she developed left-sided neck pain radiating to her shoulder, accompanied by weakness in the left deltoid (2/5), biceps (3/5), and triceps (3/5). An urgent MRI revealed a left-sided focal hyperintense T2 lesion at the C3-C4 level of the cervical cord, with restricted diffusion on diffusion-weighted imaging (DWI) and apparent diffusion coefficient (ADC) images, suggesting acute cervical cord ischemia likely due to venous infarction ([Fig. 5]). She was treated with intravenous methylprednisolone and anticoagulation, complemented by a physiotherapy program. The patient gradually recovered full function within 3 months.

Fig. 5 Case illustration 2. Magnetic resonance imaging obtained 1 day after embolization. Sagittal (A) T2-weight, (B) diffusion-weighted imaging (DWI), and (C) apparent diffusion coefficient (ADC) images of the cervical spine and axial (D) T2-wighted and (E) gradient-recalled echo (GRE) images of the C4 level revealed a left-sided focal hyperintense T2 lesion at the C3-C4 level of the cervical cord with restricted diffusion on DWI and ADC images, indicative of acute cervical cord ischemia.

Follow-up MRI obtained 5 months postembolization demonstrated a subtle residual hyperintense lesion on the left side of the cervical cord at the C4 level, without restricted diffusion on DWI and ADC images. There was no recurrence of the fistula ([Fig. 6]).

Fig. 6 Case illustration 2. Magnetic resonance imaging obtained 5 months after embolization. Sagittal (A) T2-weighted, (B) diffusion-weighted imaging (DWI), and (C) apparent diffusion coefficient (ADC) images of the cervical spine and axial (D) T2-wighted and (E) gradient-recalled echo (GRE) images of the C4 level demonstrated a subtle residual hyperintense lesion on the left side of the cervical cord at the C4 level without restricted diffusion on DWI and ADC images.

 

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Results

Following the literature review, a total of 94 articles were initially identified. After screening the titles and abstracts, 49 nonrelevant studies were excluded. The remaining 45 articles were thoroughly assessed for eligibility, resulting in 35 studies that met the inclusion criteria for the final review ([Fig. 7]). From the literature review, a total of 44 patients, including our 2 patients, with 46 lower cervical AVFs were analyzed, including 2 cases with bilateral lesions ([Table 1]).[5] [9] [11] [13] [14] [15] [16] [17] [18] [19] [20] [21] [22] [23] [24] [25] [26] [27] [28] [29] [30] [31] [32] [33] [34] [35] [36] [37] [38] [39] [40] [41] [42] [43] [44] The demographic distribution revealed an equal gender split, with 22 females and 22 males (50% each). The mean age was 48.68 ± 19.15 years, ranging from 4 to 76 years.

Fig. 7 Flow diagram showing a summary of our search strategy using the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) guidelines for relevant studies on lower cervical arteriovenous fistulas.

Table 1 Literature review of lower cervical arteriovenous fistulas

Authors (year)	Gender/Age	Symptoms and signs	Type of fistulas	Side/location	Arterial feeders	Venous drainage	Treatment	Neurological outcome
Cahan et al, 1987[13]	F/51	Radiculopathy bruit	EAVF	L/C5	VA, AsCA, DCA	IVVP	TAE (IBCA)	GR
	M/19	SAH	EAVF	R/C5	VA	IVVP/PMV	TAE (Balloon)	N/A
Willinsky et al, 1990[5]	M/36	SAH, progressive myelopathy, BBD	DAVF	R/C8	VA, CCT	PMV	TAE (NBCA) Surgery (ant, fail) Surgery (post)	IR
Barnwell et al, 1991[14]	F/69	Myelopathy	DAVF	R/C7	CCT	PMV	Surgery (post)	PR
Morimoto et al, 1992[15]	M/61	SAH	DAVF	R/C5	VA	PMV	Surgery (post)	Pain and weakness of deltoid muscle GR
Glasser et al, 1993[16]	M/9	Intradural hemorrhage	DAVF	L/C5	VA	PMV	TAE (PVA)	GR
Willinsky et al, 1993[17]	M/57	Progressive myelopathy, BBD	EAVF	R/C4, R/C5 (multiple)	VA, TCT, CCT	IPPV/SVP/PP	TAE (balloon, NBCA) TVE (coils, balloon)	GR
Kohno et al, 1996[18]	F/51	Radiculopathy	EAVF	L/C3	VA	IVVP	TAE (coil, NBCA) Surgery (post)	GR
Asai et al, 2001[19]	M/24	Progressive radiculopathy and myelopathy	EAVF	L/C7	CCT TCT	IPPV/PP	TAE (NBCA, liquid coil) Surgery (post)	GR
Hida et al, 2002[20]	F/59	Hematomyelia, BBD	PAVF	L/C3	VA-ASA	PMV	Surgery (ant)	PR
	F/62	SAH	PAVF	L/C5	VA-ASA	PMV	Surgery (ant)	GR
Chuang et al, 2003[21]	F/4	EDH	EAVF	L/C8	CCT	IVVP/PP	TAE (NBCA) Surgery (post)	Acute deterioration after embolization IR
Inoue et al, 2006[22]	F/22	Radiculopathy, myelopathy	PAVF	R/C5	VA	PMV/SPS	TAE (NBCA) Surgery (post)	GR
Terao et al, 2006[23]	M/69	Brainstem dysfunction, myelopathy, BBD	DAVF	L/C7	VA	PMV	TAE (coils) Surgery (post)	IR
Akiyama et al, 2006[24]	M/38[a]	Facial sensory disturbance	EAVF	R/C3	VA	IVVP	TAE (N/A)	GR
Geibprasert et al, 2009[9]	M/51	Progressive paraparesis, BBD	DAVF	L/C5	VA	PMV	TAE (NBCA)	GR
Kawabori et al, 2009[25]	F/65	Radiculopathy	EAVF	R/C6	TCT	IVVP/PMV	TAE (NBCA)	GR
Kim et al, 2010[26]	M/73	Progressive myelopathy	DAVF	R/C8	CCT	PMV	TAE (NBCA)	GR
Rangel-Castilla et al, 2011[27]	M/57	Syncope, radiculopathy, myelopathy	EAVF	R/C7	TCT	IVVP	TVE (coils, Onyx)	GR
Kulwin et al, 2012[28]	F/54	Brainstem dysfunction	DAVF	R/C3	VA	PMV	Surgery (post)	IR
Lucas et al, 2012[29]	M/45	SAH	DAVF	R/C5	VA	PMV	Surgery (post)	GR
Teramoto et al, 2012[30]	M/41	Radiculopathy	EAVF	R/C5	TCT	IVVP	TAE (coils)	GR
Sasamori et al, 2013[31]	F/60	Transformation from asymptomatic to progressive myelopathy 5 years later	DAVF	R/C5	AsCA	PMV	TAE (NBCA)	IR
Hetts et al, 2013[32]	M/40	Acute quadriparesis after a febrile illness, pain, BBD	DAVF	Bilateral/C6	CCTs	PMV/intracranial venous drainage	Surgery (post)	GR
Matsumoto et al, 2017[33]	M/64	Transformation from asymptomatic to SAH 4 years later	DAVF	R/C5	VA AsCA TCT	PMV (venous pouch)/TS	TAE (NBCA)	GR
Pülhorn et al, 2018[34]	F/42	Idiopathic intracranial hypertension	DAVF	L/C4	VA	PMV/TS	Surgery (post)	GR
Gao et al, 2019[35]	M/39	SAH	RAVF	R/C5	TCT ASA	PMV	TAE of a spinal pial aneurysm Surgery of AVF (post)	N/A
Kanematsu et al, 2019[36]	M/57	Progressive myelopathy after ant cervical surgery	DAVF	R/C7	VA	PMV	Surgery (post)	GR
Shimizu et al, 2019[37]	M/71	Asymptomatic	DAVF	L/C4	VA	PMV	None	Remained asymptomatic after 6 years F/U
	F/76	Asymptomatic	DAVF	R/C7	DCA	PMV/Extradural drainage at C2	None	Remained asymptomatic after 1 year F/U
	F/68	Asymptomatic	DAVF	R/C4	VA	PMV	None	Remained asymptomatic after 5 years F/U
	M/68	Asymptomatic	RAVF	R/C6	VA/PSA	PMV	None	Remained asymptomatic after 6 months F/U
Almubarak et al, 2019[38]	F/17[a]	Asymptomatic	EAVF	L/C7	VA/DCA/AsCA	IVVP/PP/EJV/IJV	None	N/A
Brinjikji et al, 2020[11]	M/72	Progressive ataxia	DAVF	L/C5	VA	PMV	None	N/A
	F/13	Progressive quadriparesis	EAVF	R/C4	VA	IVVP	TAE (PVA) Surgery (post)	GR
	M/17	Acute quadriparesis/ Hematomyelia	PAVF	R/C4	PSA	PMV	TAE (coils)	IR
Hamid et al, 2020[39]	F/40	SAH	DAVF	R/C3	VA	PMV	TAE (NBCA)	GR
Howard and Barrow, 2020[40]	F/49	Hematomyelia	PAVF	L/ C6	TCT	PMV Cerebellar veins SVP	Surgery (post)	N/A
Han et al, 2022[41]	F/68	Acute paraplegia after lumbar spinal surgery	EAVF	L/C4	VA	IVVP/PMV	TAE (Onyx)	IR
Santangelo et al, 2023[42]	F/55	Radiculopathy	EAVF	R/C6	CCT	IVVP	TAE (coil, Onyx)	GR
Mochizuki et al, 2023[43]	M/64	Asymptomatic fistula developed 5 years after treatment CCJ-AVF	RAVF	L/C5	VA	PMV	None	N/A
Yasuoka et al, 2024[44]	F/57	Repetitive vertigo and vomiting (brainstem symptom)	DAVF	R/C8	TCT	PMV	Surgery (post)	GR
Present study, 2025 Case 1	F/49	Radiculopathy	DAVF	L/C5	TCT	PMV/SVP/EJV/Extradural drainage at C8	TAE (NBCA)	Venous infarction GR
Case 2	F/39	Progressive myelopathy, BBD, brainstem dysfunction	EAVF	R/ C8	CCT	PMV	TAE (NBCA)	IR

Abbreviations: Ant, anterior approach; ASA, anterior spinal artery; AsCA, ascending cervical artery; AVF, arteriovenous fistula; BBD, bowel and bladder dysfunction; CCJ, craniocervical junction; CCT, costocervical trunk; DAVF, dural AVF; DCA, deep cervical artery; EAVF, epidural AVF; EDH, epidural hemorrhage; EJV, external jugular vein; F, female; GR, good functional recovery; F/U, follow-up; IBCA, isobutyl cyanoacrylate; IJV, internal jugular vein; IPPV, intermittent positive pressure ventilation; IR, incomplete functional recovery; IVVP, internal vertebral venous plexus; L, left; M, male; N/A, data not available; NBCA, N-butyl-2-cyanoacrylate; PAVF, perimedullary AVF; PMV, perimedullary vein; post, posterior approach; PP, paravertebral venous plexus; PR, poor recovery; PSA, posterior spinal artery; PVA, polyvinyl alcohol; R, right; RAVF, radicular AVF; SAH, subarachnoid hemorrhage; SPS, superior petrosal sinus; SVP, suboccipital venous plexus; TAE, transarterial embolization; TCT, thyrocervical trunk; TS, transverse sinus; TVE, transvenous embolization; VA, vertebral artery.

^a Association with Lhermitte–Duclos disease.

Patients presented with various symptoms: hemorrhage in 12 cases (27.3%), radiculopathy in 6 (13.6%), myelopathy in 8 (18.2%), radiculomyelopathy in 3 (6.8%), brainstem dysfunction in 4 (9.1%), other findings (e.g., facial sensory disturbances) in 3 (6.8%), and 8 (18.2%) were asymptomatic. Notably, two asymptomatic patients became symptomatic over time, and two cases were associated with Lhermitte–Duclos disease.

Fistulas were located on the right side in 28 patients (60.9%) and on the left in 18 (39.1%). The most common vertebral levels involved were C5 (16 cases, 34.8%), C4 (7 cases, 15.2%), and C7 (7 cases, 15.2%), with additional involvement at C3, C6, and C8. The arterial supply originated from the vertebral artery (VA) alone in 19 cases (41.3%), VA combined with branches from the costocervical (CCT) or thyrocervical trunks (TCT) in 6 cases (13.0%), and CCT/TCT branches alone in 16 cases (34.8%). Less common arterial supplies included combinations of the VA with the anterior or posterior spinal arteries (PSA), or PSA alone.

Of the 46 AVFs, there were 22 (47.8%) DAVFs, 16 (34.8%) EAVFs, 5 (10.9%) PAVFs, and 3 (6.5%) RAVFs. DAVFs were predominantly located at C5, C7, and C8, typically on the right side, with rare bilateral cases. EAVFs were noted at multiple cervical levels, particularly C4 and C5, with a slight right-sided prevalence. PAVFs and RAVFs, though less common, showed no significant lateral or level preference.

In terms of venous drainage, all DAVFs exhibited reflux into perimedullary veins, with four cases extending into the intracranial venous system and two showing extradural drainage, resulting in mild or asymptomatic presentations. Among the 16 EAVFs, most drained into the internal vertebral venous plexus without perimedullary involvement, though 4 cases had retrograde reflux into perimedullary veins. One EAVF had additional drainage into the jugular veins, contributing to an asymptomatic presentation. All PAVFs and RAVFs drained into perimedullary veins, with two PAVFs having additional intracranial drainage.

Treatment modalities included endovascular treatment in 18 patients (40.9%), surgery in 11 patients (25.0%), and combined endovascular and surgical treatment in 8 patients (18.2%). Seven patients (15.9%) remained untreated. Most endovascular treatments were transarterial, with only two cases requiring a transvenous approach. Of the surgical cases, the majority underwent posterior approaches, with only two treated via the anterior approach. One patient required both approaches due to failure of the initial anterior surgery.

Outcomes showed that 24 patients (54.5%) had good recovery, 8 (18.2%) had incomplete recovery, 2 (4.6%) experienced poor recovery, and data were unavailable for 6 patients (13.6%). Four previously asymptomatic patients (9.1%) remained asymptomatic after long-term follow-up.

 

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Discussion

Vascular Anatomy of the Lower Cervical Region

The vascular architecture of the cervical spinal cord is complex and critical for its function and pathology. Notably, the cervical radicular arteries primarily supply the spinal cord from the C4 level downwards, as established by seminal studies including Chakravorty[45] who highlighted that these arteries, while being the main supply routes to the spinal cord below C3, originate variably from the vertebral and subclavian artery branches. Above C3, the spinal cord receives its blood supply predominantly from the intracranial branches of the vertebral arteries.

The cervical radicular arteries typically bifurcate into anterior and posterior branches as they enter the spinal canal through the intervertebral foramina alongside the cervical nerve roots. These arteries have sources including the VA and branches of the subclavian artery, such as the ascending cervical artery from the TCT and the deep cervical artery from the CCT. It is of particular note that the origins of these arteries vary with spinal levels: cervical radicular arteries at the upper six cervical segments often arise from the VA or ascending cervical artery, whereas those at the C7 and C8 levels invariably originate from the deep cervical artery.

Further detailed anatomical insights were provided by Arslan et al,[46] who through cadaveric dissections, found that cervical radicular arteries typically emerge from the posterior aspect of the VA, particularly at the C6 level. The ascending cervical arteries are known to supply the spinal branches to the C4 and C5 nerve roots, whereas the deep cervical arteries consistently penetrate the dural sleeves within the posteroinferior part of the foramina at the C5-6, C6-7, and C7-T1 levels. Additionally, there is a variant where the deep cervical artery may arise directly from the subclavian artery.

The venous drainage of the lower cervical spine is a complex system involving multiple pathways that facilitate the outflow of blood from the spinal cord. Key structures include the internal vertebral venous plexus, perimedullary veins, radicular veins, and in some cases, external jugular veins. These venous pathways are essential for maintaining spinal cord perfusion, particularly in the context of AVFs, where abnormal shunting of blood from arteries to veins can lead to venous hypertension and congestion, resulting in myelopathy and other neurological deficits. Comprehensive knowledge of the complex venous outlets and their interconnections in the cervical spinal cord is paramount for accurately diagnosing and effectively managing cervical AVFs.[47] [48]

 

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Pathogenesis of Lower Cervical AVFs

The pathogenesis of lower cervical AVFs remains unclear and is thought to be either congenital or acquired. AVFs may arise spontaneously or as a result of trauma, surgery, or vascular changes over time.[14] [16] [21] [33] [36] [41] While no definitive cause has been identified, evidence from associated conditions such as Lhermitte–Duclos disease suggests a possible genetic or vascular predisposition for the occurrence of AVFs. Lhermitte–Duclos disease, often linked with Cowden syndrome, is associated with phosphatase and tensin homolog (PTEN) mutations that affect vascular integrity, making it an example of how AVFs could form in patients with underlying vascular anomalies.[24] [38]

In our second case illustration, the patient had an unruptured intracranial aneurysm in addition to the lower cervical AVF, which may support the hypothesis that there could be an underlying genetic or vascular predisposition for developing abnormal vascular structures. The coexistence of these vascular abnormalities, though not fully understood, hints at a potential systemic issue in vascular formation or maintenance, possibly driven by genetic factors that influence vascular health. Understanding these predispositions could provide insight into the mechanisms driving both AVFs and other vascular anomalies.

 

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Clinical Presentation: Symptomatic versus Asymptomatic Patients

The clinical presentation of lower cervical AVFs is highly variable, ranging from asymptomatic cases to severe neurological deficits.[20] [31] [41] [43] [44] In our review of 44 patients, 27.3% presented with hemorrhage, while others exhibited radiculopathy (13.6%), myelopathy (18.2%), and radiculomyelopathy (6.8%). Notably, 9.1% of patients demonstrated brainstem dysfunction, a rare but significant finding in cervical AVFs. Additionally, 18.2% were asymptomatic at presentation, although two of these patients later developed symptoms. This variability highlights the importance of early diagnosis, as clinical progression is often influenced by the venous drainage patterns and location of the fistula. Venous drainage patterns varied significantly across the different types of AVFs. All DAVFs exhibited reflux into the perimedullary veins, with a subset (four cases) also draining into the intracranial venous system, and two cases demonstrating extradural drainage via the cervical roots. The latter was associated with milder symptoms or asymptomatic cases, emphasizing the protective role that alternative venous outlets can play in mitigating venous congestion.

Conversely, most EAVFs drained into the internal vertebral venous plexus without perimedullary involvement, although four patients had retrograde reflux into the perimedullary veins, leading to more pronounced symptoms. One EAVF drained into both the external and internal jugular veins, resulting in an asymptomatic presentation, again illustrating how additional venous drainage pathways can alleviate symptoms.

RAVF and PAVF consistently drained into perimedullary veins, and in two PAVF cases, additional drainage into the intracranial venous system was observed. This complexity in venous outflow across the various types of AVFs plays a crucial role in symptomatology and should be carefully considered in treatment planning to prevent complications associated with venous hypertension and congestion.

 

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Management Strategies: Embolization versus Surgical Intervention

The management of lower cervical AVFs has evolved with the advent of advanced endovascular techniques. Endovascular embolization and microsurgical resection remain the two primary treatment modalities. Each approach has its own merits, and the decision between them is often guided by the type of fistula, its angioarchitecture, and patient-specific factors such as clinical presentation and risk tolerance.[9] [11]

Endovascular embolization has gained prominence as a minimally invasive treatment option, particularly for AVFs with accessible arterial feeders. Embolization using liquid embolic agents, such as Onyx or NBCA, is preferred in cases where the fistula is supplied by the branches of the VA, TCT, or CCT.[5] [11] For EAVFs, endovascular treatment offers a distinct advantage, as it can access both the arterial and venous components of the fistula without the need for open surgery.[18] Furthermore, embolization can be curative or used as a preoperative adjunct to reduce the blood supply prior to surgical resection, thus decreasing the risk of intraoperative hemorrhage.[19] In certain cases, embolization alone has led to significant symptom relief and complete obliteration of the fistula.[42]

Surgical treatment is typically reserved for cases where embolization is not feasible or incomplete. This is often the case with complex DAVFs or fistulas with intricate venous drainage patterns, particularly those involving the perimedullary veins or intracranial venous systems.[11] [27] Microsurgical resection allows for direct visualization and disconnection of the fistula, ensuring complete resolution. In some cases, a combination of embolization followed by surgery is employed to maximize treatment efficacy.[9] [13]

In our literature review, of the 44 cases of lower cervical AVFs, 40.9% of patients were treated with endovascular embolization, while 25% underwent surgical resection. Another 18.2% required a combination of both approaches. The choice between embolization and surgery is heavily influenced by the fistula's location, complexity, and the patient's clinical condition. For DAVF and EAVF, embolization is often the first line of treatment, while surgical intervention is preferred in cases of incomplete embolization or in those presenting with large, complex vascular malformations.[9] [27]

In summary, endovascular embolization and surgical resection are the primary treatment options for lower cervical AVFs, with the choice influenced by lesion characteristics, angioarchitecture, patient factors, and institutional expertise. Endovascular embolization is preferred for lesions with accessible arterial feeders, particularly DAVF and EAVF, as it is minimally invasive and offers reduced procedural risk. It is the first-line treatment for fistulas supplied by the VA, TCT, or CCT, allowing rapid occlusion with minimal recovery time. However, risks include incomplete embolization, venous infarction, and recurrence. Surgical resection is indicated for complex cases, including large or high-flow fistulas, those with challenging vascular access, or when embolization is incomplete. It allows direct visualization and definitive fistula disconnection, particularly for PAVFs or cases with intricate venous drainage. While surgery provides durable outcomes, it carries risks such as cerebrospinal fluid leakage, infection, and spinal cord injury. Institutional experience and the expertise of neurointerventionalists and neurosurgeons play a significant role in treatment selection, as centers with extensive endovascular experience may favor embolization, whereas institutions with strong microsurgical expertise may opt for surgery in complex cases. In select situations, a combined approach involving embolization followed by surgery can be advantageous in reducing vascular supply before definitive resection, minimizing intraoperative bleeding, and improving success rates.

 

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Management of Asymptomatic Lower Cervical AVFs

The management of asymptomatic lower cervical AVFs remains a topic of debate due to the risk of these lesions eventually becoming symptomatic, potentially leading to significant neurological deficits.[31] [33] Asymptomatic AVFs are often discovered incidentally through imaging for unrelated conditions, and their natural history is not well documented, complicating decisions about intervention.

Although many patients with asymptomatic AVFs remain stable for years, there is a risk that these fistulas may eventually cause venous hypertension and progressive myelopathy. As such, some authors advocate for early treatment even in asymptomatic patients, particularly if the fistula demonstrates aggressive angioarchitecture, such as retrograde drainage into perimedullary veins.[31] [41] In contrast, others suggest a more conservative approach, reserving intervention for cases that become symptomatic.[37] [38] [43]

In cases where endovascular embolization or surgery is pursued, treatment outcomes are generally favorable if performed before significant neurological deterioration occurs. However, the decision to treat asymptomatic AVFs must balance the risks of intervention against the potential for spontaneous progression to symptomatic disease, making individualized patient assessment critical.[25]

 

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Outcome and Prognosis of Lower Cervical AVFs

The outcomes of patients with lower cervical AVFs vary widely depending on factors such as the type of fistula, timing of diagnosis, and treatment approach. Early diagnosis and prompt treatment generally result in more favorable outcomes, as delayed intervention can lead to irreversible neurological damage due to venous congestion.[9] [11] [49] In this review of 44 cases, the outcomes ranged from full recovery to partial or poor neurological improvement, particularly in cases where treatment was delayed or incomplete.

In our literature review, 54.5% of patients had good recovery following treatment, while 18.2% experienced incomplete recovery. Only 4.6% had poor recovery outcomes, highlighting the importance of timely intervention. Importantly, four asymptomatic patients (9.1%) remained asymptomatic following long-term follow-up, indicating that treatment can effectively prevent symptom progression in some cases.

Patients treated with embolization, surgery, or a combination of both had varying degrees of recovery. Endovascular embolization alone led to significant neurological improvement in a majority of cases, particularly in those where fistulas were accessible for transarterial approaches. Surgical intervention, often reserved for complex cases or when embolization was incomplete, also yielded favorable outcomes, especially when a posterior approach was used. The presence of additional venous outlets, such as drainage into the jugular veins, was associated with milder symptoms and better outcomes due to reduced venous hypertension.[37] [38]

Overall, the prognosis for lower cervical AVFs is favorable when managed with a multidisciplinary approach combining endovascular and surgical treatments, with outcomes significantly influenced by early diagnosis and the ability to achieve complete obliteration of the fistula.[22] [25] [33]

 

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Complications and Risk Mitigation in Lower Cervical AVFs

Management of lower cervical AVFs involves significant risks, both from the underlying pathology and treatment itself. Common complications include venous hypertension, spinal cord and/or brainstem ischemia, and in severe cases, hemorrhage due to altered hemodynamics. Myelopathy, often resulting from chronic venous congestion, is a key concern, especially in untreated or poorly managed AVFs, leading to progressive neurological deterioration.[14] [15] [21] [44] Endovascular embolization, though minimally invasive, carries risks such as nontarget embolization and incomplete fistula closure, which can result in ischemia or recurrence. Additionally, postembolization venous thrombosis is a critical complication, as thrombosis within draining veins can obstruct venous outflow, leading to further venous congestion and spinal cord ischemia. Surgical intervention, while effective, may also lead to complications such as cerebrospinal fluid leaks or infection.[5] [11]

To mitigate these risks, careful preoperative imaging and angiographic evaluation are essential. Identifying venous drainage patterns, especially retrograde flow into perimedullary veins, is crucial for planning treatment and reducing complications.[9] Prophylactic anticoagulation following embolization has been shown to prevent postprocedural thrombosis. By maintaining venous patency, prophylactic anticoagulation reduces the risk of ischemic complications and promotes better long-term outcomes.[6] A staged approach, involving initial embolization followed by surgery, can further minimize risks by reducing the vascular supply to the fistula before definitive treatment. Posttreatment, close monitoring is critical to manage delayed complications such as venous infarction, thrombosis, or fistula recurrence.[21] [23]

A worst-case scenario in the treatment of lower cervical AVFs involves a combination of incomplete embolization, postprocedural venous thrombosis, and spinal cord ischemia, leading to devastating neurological deficits. In cases where embolization fails to achieve complete occlusion, residual shunting may result in persistent venous hypertension, worsening myelopathy, or even secondary hemorrhage. Additionally, aggressive embolization can inadvertently cause nontarget embolization, occluding critical spinal arteries and leading to acute ischemia or infarction of the spinal cord or brainstem. A particularly severe complication is postembolization venous thrombosis, where abrupt closure of the fistula disrupts venous outflow, causing retrograde congestion and infarction, as seen in cases with perimedullary venous reflux. Patients experiencing this may develop sudden quadriplegia, respiratory failure due to high cervical cord involvement, or irreversible loss of function despite rescue interventions such as anticoagulation or corticosteroids. Surgical resection, while definitive, carries its own worst-case risks, including excessive intraoperative bleeding, inadvertent arterial injury, cerebrospinal fluid leakage, or postoperative infection, potentially resulting in permanent neurological deterioration. In rare cases, a combination of embolization-induced infarction and surgical complications could leave a patient with severe, life-altering disabilities, including loss of ambulation, bowel and bladder dysfunction, or ventilator dependence. Such outcomes highlight the critical importance of meticulous preoperative planning, careful selection of embolic agents, staged treatment approaches, and vigilant postprocedural monitoring to prevent catastrophic complications.

 

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Future Directions and Research Needs

Despite advancements in the diagnosis and treatment of lower cervical AVFs, there remain several gaps in knowledge and areas for further exploration. One critical area of future research is understanding the long-term outcomes of different treatment modalities, particularly the comparison between embolization and surgical interventions. While endovascular techniques have become increasingly favored due to their minimally invasive nature, more data on long-term efficacy, recurrence rates, and patient quality of life are needed to refine treatment protocols.

Additionally, more comprehensive studies are needed to investigate the natural history of asymptomatic AVFs. Identifying reliable predictors of symptom progression in asymptomatic patients could significantly impact clinical decision-making, helping to determine which patients might benefit from early intervention versus conservative management. Research into the role of prophylactic treatments, such as anticoagulation postembolization, in preventing complications like venous infarction or thrombosis could further improve patient outcomes.

Another promising area for future research is the development and refinement of imaging technologies. Advanced imaging techniques, such as high-resolution dynamic MRI and four-dimensional angiography, could allow for better visualization of complex vascular structures and improve preoperative planning. In particular, research focused on noninvasive imaging techniques capable of reliably assessing venous drainage patterns and fistula complexity will be essential for advancing early detection and personalized treatment strategies.[8]

Lastly, the role of genetic and molecular factors in the development of AVFs remains poorly understood. Investigating potential genetic predispositions or molecular pathways involved in AVF formation could open new avenues for targeted therapies and early interventions. These future research directions will not only enhance our understanding of lower cervical AVFs but also improve patient care and outcomes through more personalized and effective treatment approaches.

 

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Limitations

This study has several limitations that need to be acknowledged. First, the retrospective nature of the review introduces potential biases, including selection and recall bias, which may affect the completeness and accuracy of the clinical data collected. Additionally, the sample size, though representative of lower cervical AVFs, remains relatively small, which may limit the generalizability of the findings. Another limitation is the variability in the diagnostic and treatment approaches across different institutions, as the literature reviewed includes case reports and series from various centers with differing clinical practices. This heterogeneity could influence treatment outcomes and complicate comparisons across cases.

Furthermore, there is a lack of long-term follow-up data for many of the cases included in the review, making it difficult to assess the true recurrence rates and long-term efficacy of the treatment modalities. The absence of standardized outcome measures across the studies also limits the ability to perform a robust comparative analysis of treatment outcomes. Lastly, asymptomatic patients were included in the review, but the natural history and potential for progression in these cases remain unclear, which highlights the need for future studies focusing on the prognosis and management of asymptomatic AVFs.

These limitations suggest the need for larger, prospective studies with standardized treatment protocols and longer follow-up periods to better understand the outcomes and optimal management strategies for lower cervical AVFs.

 

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Conclusion

Lower cervical AVFs represent a rare but complex subset of spinal vascular malformations that pose unique diagnostic and therapeutic challenges. This study highlights the variability in clinical presentations, ranging from asymptomatic cases to severe neurological deficits, largely influenced by the fistula's venous drainage patterns and angioarchitecture. Endovascular embolization and surgical resection remain the primary treatment modalities, with outcomes dependent on early diagnosis and appropriate intervention. Despite advancements in imaging and treatment techniques, the management of lower cervical AVFs requires a tailored approach based on the fistula's complexity and the patient's clinical condition. Further research, particularly on the natural history of asymptomatic AVFs and the long-term outcomes of various treatment strategies, is necessary to refine treatment protocols and improve patient care. Understanding the genetic or vascular predispositions that may contribute to AVF development, as seen in cases with coexisting vascular anomalies, could also provide valuable insights into the pathogenesis and management of these conditions.

 

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Conflict of Interest

None declared.

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Publication History

Article published online:
05 May 2025