Arteriovenous malformation with unique drainage through the emissary vein of the foramen ovale: illustrative case

Xiaochun Zhao Division of Pediatric Neurosurgery, Oklahoma Children’s Hospital, Department of Neurosurgery, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma; and

Search for other papers by Xiaochun Zhao in
Current site
jns
Google Scholar
PubMed
Close
 MD
,
Alexander R Evans Division of Pediatric Neurosurgery, Oklahoma Children’s Hospital, Department of Neurosurgery, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma; and

Search for other papers by Alexander R Evans in
Current site
jns
Google Scholar
PubMed
Close
 BS
,
Ali Tayebi Meybodi The Loyal and Edith Davis Neurosurgical Research Laboratory, Department of Neurosurgery, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix, Arizona

Search for other papers by Ali Tayebi Meybodi in
Current site
jns
Google Scholar
PubMed
Close
 MD
,
Nicholas Hopkins Division of Pediatric Neurosurgery, Oklahoma Children’s Hospital, Department of Neurosurgery, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma; and

Search for other papers by Nicholas Hopkins in
Current site
jns
Google Scholar
PubMed
Close
 MD
,
Ira Bowen Division of Pediatric Neurosurgery, Oklahoma Children’s Hospital, Department of Neurosurgery, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma; and

Search for other papers by Ira Bowen in
Current site
jns
Google Scholar
PubMed
Close
 MD
,
Shyian S Jen Division of Pediatric Neurosurgery, Oklahoma Children’s Hospital, Department of Neurosurgery, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma; and

Search for other papers by Shyian S Jen in
Current site
jns
Google Scholar
PubMed
Close
 MD, MS
,
Mark C Preul The Loyal and Edith Davis Neurosurgical Research Laboratory, Department of Neurosurgery, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix, Arizona

Search for other papers by Mark C Preul in
Current site
jns
Google Scholar
PubMed
Close
 MD
, and
Karl Balsara Division of Pediatric Neurosurgery, Oklahoma Children’s Hospital, Department of Neurosurgery, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma; and

Search for other papers by Karl Balsara in
Current site
jns
Google Scholar
PubMed
Close
 MD
Open access

BACKGROUND

As part of the laterotrigeminal venous system (LTVS), the emissary vein of the foramen ovale (EVFO) is an underrecognized venous structure communicating between the cavernous sinus and pterygoid plexus. The sphenobasal sinus is an anatomical variation of the sphenoparietal sinus that drains directly into the EVFO. The authors present the case of a ruptured arteriovenous malformation (AVM) with a unique drainage pattern through the sphenobasal sinus and EVFO.

OBSERVATIONS

A 9-year-old female initially presented with loss of consciousness and was subsequently found to have a ruptured AVM in the left basal frontal area. She underwent an immediate decompressive hemicraniectomy, with a computed tomography angiogram demonstrating a unique anatomical variation in which the sphenobasal sinus communicated with the EVFO and LTVS. The final venous drainage returned to the pterygoid plexus and external jugular vein. Postoperatively, the patient made a substantial recovery, with generalized right-sided weakness remaining as the sole deficit.

LESSONS

The authors present the case of a ruptured AVM with unique venous drainage into the sphenobasal sinus and EVFO, for which the current literature remains limited. As exemplified by this illustrative case, technique modification may be warranted in the setting of this unique anatomical variation to avoid venous sinus injury.

ABBREVIATIONS

AVM = arteriovenous malformation; EVFO = emissary vein of the foramen ovale; GG = Gasserian ganglion; LTVS = laterotrigeminal venous system; MCA = middle cerebral artery; V3 = mandibular nerve root

BACKGROUND

As part of the laterotrigeminal venous system (LTVS), the emissary vein of the foramen ovale (EVFO) is an underrecognized venous structure communicating between the cavernous sinus and pterygoid plexus. The sphenobasal sinus is an anatomical variation of the sphenoparietal sinus that drains directly into the EVFO. The authors present the case of a ruptured arteriovenous malformation (AVM) with a unique drainage pattern through the sphenobasal sinus and EVFO.

OBSERVATIONS

A 9-year-old female initially presented with loss of consciousness and was subsequently found to have a ruptured AVM in the left basal frontal area. She underwent an immediate decompressive hemicraniectomy, with a computed tomography angiogram demonstrating a unique anatomical variation in which the sphenobasal sinus communicated with the EVFO and LTVS. The final venous drainage returned to the pterygoid plexus and external jugular vein. Postoperatively, the patient made a substantial recovery, with generalized right-sided weakness remaining as the sole deficit.

LESSONS

The authors present the case of a ruptured AVM with unique venous drainage into the sphenobasal sinus and EVFO, for which the current literature remains limited. As exemplified by this illustrative case, technique modification may be warranted in the setting of this unique anatomical variation to avoid venous sinus injury.

ABBREVIATIONS

AVM = arteriovenous malformation; EVFO = emissary vein of the foramen ovale; GG = Gasserian ganglion; LTVS = laterotrigeminal venous system; MCA = middle cerebral artery; V3 = mandibular nerve root

The emissary vein of the foramen ovale (EVFO)1 is an underrecognized venous drainage structure that connects the venous sinus of the middle fossa to the pterygoid venous plexus. Subsequently, the pterygoid plexus drains into the external jugular vein, where the blood returns into the circulation.2 The laterotrigeminal venous system (LTVS)3 is located in the middle fossa, contiguous to the Gasserian ganglion (GG) and mandibular nerve root (V3); this venous system contains multiple lacunae that communicate with the cavernous sinus superiorly (via the superior petrosal sinus) and the pterygoid venous plexus inferiorly (via the EVFO). Furthermore, the sphenoparietal sinus is a major venous structure that courses within the anterior temporal dura, which commonly drains into the cavernous sinus; however, in approximately 15% of the cases,3,4 this sinus continues along the basal temporal dura and drains into the pterygoid plexus via the EVFO. The EVFO then goes on to communicate with the LTVS in this subset of patients. Such cases of anatomical variation are termed the “sphenobasal sinus.”4,5

Here, we present the case of a pediatric patient presenting with a ruptured arteriovenous malformation (AVM) who was found to have the aforementioned unique venous drainage pattern via the sphenoparietal sinus, sphenobasal sinus, and EVFO, eventually draining into the pterygoid plexus.

Illustrative Case

A 9-year-old female presented with sudden-onset severe headaches and rapidly became unresponsive and required intubation upon the arrival of emergency personnel. After transport to our institution, a computed tomography (CT) scan demonstrated a sizeable intracranial hematoma involving the frontal and temporal lobe (Fig. 1A). On neurological examination, she demonstrated decorticate posturing in the bilateral upper extremities, with a fixed left pupil dilated to 6 mm. An emergent hemicraniectomy was then completed without evacuation of the hematoma, as knowledge of the underlying cause was lacking. Her elevated intracranial pressure was monitored and managed during the acute phase.

FIG. 1
FIG. 1

Axial CT scan (A) demonstrated a large intracerebral hemorrhage in the left frontal and temporal lobes, measuring up to 76 mm anteroposteriorly. Lateral view of the left internal carotid artery (ICA) injection on an angiogram (B), during the arterial phase, demonstrated a nidus (red circle) in the basal frontal area and draining to the abnormally early filling vein. An intranidal aneurysm was also visible (asterisk). The capillary phase of the lateral left ICA injection (C) demonstrating abnormally early filling to the draining vein. The nidus drained into the sphenoparietal sinus, sphenobasal sinus, EVFO, and pterygoid plexus. The anteroposterior view of the angiogram (D) again demonstrated the nidus (red circle) with the aneurysm (asterisk). The nidus received arterial feeders from the MCA superiorly. A sagittal view of a CT angiogram (E) demonstrated filling of the sphenoparietal and sphenobasal sinuses (arrowheads), which drained into the EVFO through the foramen ovale; the EVFO was shown to be significantly dilated. An axial view of the CT angiogram (F) demonstrated the dilated pterygoid plexus (blue circle) within the infratemporal fossa. Postoperative lateral (G) and anteroposterior (H) angiograms showed no residual of the previously demonstrated nidus, no abnormally early filling vessels, and no significant filling defect.

A CT angiogram was subsequently obtained after the patient was stabilized, demonstrating an AVM with multiple arterial feeders from the second segment (M2) of the middle cerebral artery (MCA). The AVM nidus was filling during the early arterial phase (Fig. 1B), in which the venous drainage pattern was identified sequentially through the sphenoparietal sinus, sphenobasal sinus, and EVFO (Fig. 1C). Moreover, the draining vein was fully perfused during the capillary phase of the angiogram, indicating high-speed shunting from the nidus. A coronal view of the angiogram demonstrated that the nidus was superior to the M2 branches within the basal frontal lobe (Fig. 1D). Notably, an intranidal aneurysm was also observed.

The CT angiogram elucidated the course of venous drainage into the sphenoparietal and sphenobasal sinuses (Fig. 1E) and through the foramen ovale into the pterygoid plexus in the infratemporal fossa (Fig. 1F), which was also found to be dilated. A transsylvian approach for AVM resection was then performed uneventfully. Postoperative angiograms demonstrated no residual nidus or early filling of abnormal vasculature (Fig. 1G–H).

After surgical management, the patient was successfully extubated and experienced a substantial recovery. After extensive physical therapy, she was discharged to a rehabilitation facility with decreased right-sided motor function (not antigravity) her only deficit.

Patient Informed Consent

The necessary patient informed consent was obtained in this study.

Discussion

We present a case of ruptured AVM with a rare venous drainage pattern to the EVFO, along with an uncommon anatomical variation in the middle fossa, termed the “sphenobasal sinus.”

The prevalence of AVM in the pediatric population is lower than that in the adult population, comprising approximately 3% of all AVM cases.6 In addition, pediatric AVMs carry a slightly higher risk of rupture than adult AVMs (3.2% vs 2.2%, respectively),7 with a significant risk of recurrence (2.7%).8

Observations

The floor of the middle fossa (Fig. 2A) carries substantial venous channels, allowing for communication of the cavernous sinus anteromedially, superior petrosal sinus posteromedially, and pterygoid plexus inferiorly. Moreover, the venous system contiguous to the GG was named the “laterotrigeminal venous system” by Simoes3 in 1993 and was found to vary in terms of the venous drainage pattern; however, the majority of venous channels in the LTVS are found at the following locations (Fig. 2B): GG, the V3, the communicating vein to the superior petrosal sinus, the middle meningeal vein coursing through the foramen spinosum, and the EVFO. The EVFO is the major emissary vein connecting the LTVS and middle fossa venous structures to the pterygoid plexus, which eventually drains into the external jugular vein, where blood is returned to the circulation.

FIG. 2
FIG. 2

A: A cadaveric dissection of the middle fossa floor on the right side. After extradural subtemporal dissection, the LTVS is demonstrated in proximity to the GG and V3. B: Illustration of the normal anatomy of the LTVS, which contains the following components: GG, the V3, the communicating vein to the superior petrosal sinus, the middle meningeal vein coursing through the foramen spinosum, and the EVFO. The LTVS provides venous communication to the cavernous sinus, superior petrosal sinus, and pterygoid plexus. C: Illustration of the sphenobasal variation, where the sphenoparietal sinus drains into the LTVS and EVFO. Cav. = cavernous; em. = eminence; FO = foramen ovale; For. = foramen; FR = foramen rotundum; GSPN = greater superficial petrosal nerve; IPS = inferior petrosal sinus; Intercav. = intercavernous; LPN = lesser petrosal nerve; sin. = sinus; SPS = superior petrosal sinus; SS = sigmoid sinus; TT = tagmen tympani; V2 = maxillary nerve.

The sphenoparietal sinus is another major draining venous structure located within the anterior temporal dura that courses along the anterior branch of the middle meningeal artery.5 This sinus receives flow from the superficial middle cerebral vein (also known as the “Sylvian vein”) and often drains into the cavernous sinus. However, it has been reported that the superficial middle cerebral vein drains directly into the LTVS via the sphenoparietal sinus in up to 18% of patients.3 In addition, a surgical cohort described by Shibao et al.4 further exemplified this finding, demonstrating that this variation was present in up to 12.5% of cases. The “sphenobasal sinus” was then coined to name this drainage variation based on the Hacker classification (Fig. 2C).9

Within the context of the above discussion, our patient’s AVM drained into the superficial middle cerebral vein, sphenoparietal sinus, sphenobasal sinus, EVFO, and pterygoid plexus. This unique drainage pattern is evident in Fig. 1E, in which the dilated EVFO is visible within the foramen ovale. After all arterial feeders were disconnected from the AVM and circumferential dissection of the nidus was achieved, the draining vein was disconnected only at the nidus as the final step of resection.

Notably, if a subtemporal or pretemporal extradural dissection is warranted (e.g., anterior petrosectomy) in the setting of anatomical variation (as in the presence of a sphenobasal sinus draining through the EVFO), the dural opening should be modified posteriorly in an attempt to preserve venous drainage.4

Lessons

The LTVS (including the EVFO) is underrecognized in clinical scenarios and the current literature. We present the case of a pediatric ruptured AVM with drainage into the pterygoid plexus via the EVFO, with an uncommon anatomical variation termed the “sphenobasal sinus.” The middle fossa venous system may be involved in such pathological conditions; thus, it is essential to glean a deep comprehension of these structures to safely navigate through this unusual anatomy.

Author Contributions

Conception and design: Zhao, Hopkins. Acquisition of data: Balsara, Tayebi Meybodi, Hopkins, Jen, Preul. Analysis and interpretation of data: Jen. Drafting the article: Zhao. Critically revising the article: Evans, Tayebi Meybodi, Hopkins, Bowen, Jen, Preul. Reviewed submitted version of manuscript: Balsara, Tayebi Meybodi, Hopkins, Bowen, Jen, Preul. Approved the final version of the manuscript on behalf of all authors: Balsara. Administrative/technical/material support: Tayebi Meybodi. Study supervision: Balsara.

References

  • 1

    Tsutsumi S, Ono H, Ishii H The emissary veins of the foramen ovale: an anatomical study using magnetic resonance imaging. Surg Radiol Anat. 2020;42(7):771777.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Golub B, Bordoni B Neuroanatomy, Pterygoid Plexus. In: StatPearls. StatPearls Publishing; 2023. Accessed October 28, 2023. http://www.ncbi.nlm.nih.gov/books/NBK555896/

    • PubMed
    • Export Citation
  • 3

    Simões S An anatomical study of the laterotrigeminal venous system. Ann Anat. 1993;175(2):115118.

  • 4

    Shibao S, Toda M, Orii M, Fujiwara H, Yoshida K Various patterns of the middle cerebral vein and preservation of venous drainage during the anterior transpetrosal approach. J Neurosurg. 2016;124(2):432439.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Tayebi Meybodi A, Mignucci-Jiménez G, Lawton MT, Liu JK, Preul MC, Sun H Comprehensive microsurgical anatomy of the middle cranial fossa: part II-neurovascular anatomy. Front Surg. 2023;10:1132784.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    El-Ghanem M, Kass-Hout T, Kass-Hout O, et al. Arteriovenous malformations in the pediatric population: review of the existing literature. Intervent Neurol. 2016;5(3–4):218225.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Di Rocco C, Tamburrini G, Rollo M Cerebral arteriovenous malformations in children. Acta Neurochir (Wien). 2000;142(2):145156, discussion 156–158.

  • 8

    Sorenson TJ, Brinjikji W, Bortolotti C, Kaufmann G, Lanzino G Recurrent brain arteriovenous malformations (AVMs): a systematic review. World Neurosurg. 2018;116:e856e866.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Hacker H Normal supratentorial veins and dural sinuses. Radiology of the Skull and Brain. 1974;2:18511877.

  • Collapse
  • Expand
  • FIG. 1

    Axial CT scan (A) demonstrated a large intracerebral hemorrhage in the left frontal and temporal lobes, measuring up to 76 mm anteroposteriorly. Lateral view of the left internal carotid artery (ICA) injection on an angiogram (B), during the arterial phase, demonstrated a nidus (red circle) in the basal frontal area and draining to the abnormally early filling vein. An intranidal aneurysm was also visible (asterisk). The capillary phase of the lateral left ICA injection (C) demonstrating abnormally early filling to the draining vein. The nidus drained into the sphenoparietal sinus, sphenobasal sinus, EVFO, and pterygoid plexus. The anteroposterior view of the angiogram (D) again demonstrated the nidus (red circle) with the aneurysm (asterisk). The nidus received arterial feeders from the MCA superiorly. A sagittal view of a CT angiogram (E) demonstrated filling of the sphenoparietal and sphenobasal sinuses (arrowheads), which drained into the EVFO through the foramen ovale; the EVFO was shown to be significantly dilated. An axial view of the CT angiogram (F) demonstrated the dilated pterygoid plexus (blue circle) within the infratemporal fossa. Postoperative lateral (G) and anteroposterior (H) angiograms showed no residual of the previously demonstrated nidus, no abnormally early filling vessels, and no significant filling defect.

  • FIG. 2

    A: A cadaveric dissection of the middle fossa floor on the right side. After extradural subtemporal dissection, the LTVS is demonstrated in proximity to the GG and V3. B: Illustration of the normal anatomy of the LTVS, which contains the following components: GG, the V3, the communicating vein to the superior petrosal sinus, the middle meningeal vein coursing through the foramen spinosum, and the EVFO. The LTVS provides venous communication to the cavernous sinus, superior petrosal sinus, and pterygoid plexus. C: Illustration of the sphenobasal variation, where the sphenoparietal sinus drains into the LTVS and EVFO. Cav. = cavernous; em. = eminence; FO = foramen ovale; For. = foramen; FR = foramen rotundum; GSPN = greater superficial petrosal nerve; IPS = inferior petrosal sinus; Intercav. = intercavernous; LPN = lesser petrosal nerve; sin. = sinus; SPS = superior petrosal sinus; SS = sigmoid sinus; TT = tagmen tympani; V2 = maxillary nerve.

  • 1

    Tsutsumi S, Ono H, Ishii H The emissary veins of the foramen ovale: an anatomical study using magnetic resonance imaging. Surg Radiol Anat. 2020;42(7):771777.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Golub B, Bordoni B Neuroanatomy, Pterygoid Plexus. In: StatPearls. StatPearls Publishing; 2023. Accessed October 28, 2023. http://www.ncbi.nlm.nih.gov/books/NBK555896/

    • PubMed
    • Export Citation
  • 3

    Simões S An anatomical study of the laterotrigeminal venous system. Ann Anat. 1993;175(2):115118.

  • 4

    Shibao S, Toda M, Orii M, Fujiwara H, Yoshida K Various patterns of the middle cerebral vein and preservation of venous drainage during the anterior transpetrosal approach. J Neurosurg. 2016;124(2):432439.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Tayebi Meybodi A, Mignucci-Jiménez G, Lawton MT, Liu JK, Preul MC, Sun H Comprehensive microsurgical anatomy of the middle cranial fossa: part II-neurovascular anatomy. Front Surg. 2023;10:1132784.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    El-Ghanem M, Kass-Hout T, Kass-Hout O, et al. Arteriovenous malformations in the pediatric population: review of the existing literature. Intervent Neurol. 2016;5(3–4):218225.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Di Rocco C, Tamburrini G, Rollo M Cerebral arteriovenous malformations in children. Acta Neurochir (Wien). 2000;142(2):145156, discussion 156–158.

  • 8

    Sorenson TJ, Brinjikji W, Bortolotti C, Kaufmann G, Lanzino G Recurrent brain arteriovenous malformations (AVMs): a systematic review. World Neurosurg. 2018;116:e856e866.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Hacker H Normal supratentorial veins and dural sinuses. Radiology of the Skull and Brain. 1974;2:18511877.

Metrics

All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 306 306 58
PDF Downloads 196 196 18
EPUB Downloads 0 0 0