Detection of inferolateral trunk syndrome by neuromonitoring during catheter angiography with provocative testing
- 1Department of Neurology and Intraoperative Neuromonitoring, Stanford University Medical Center, Stanford, California, USA
- 2Department of Neurosurgery and Radiology, Stanford University School of Medicine, Stanford, California, USA
- Correspondence to Dr S Le, Department of Neurology, Stanford University Medical Center, 300 Pasteur Drive, A343, Stanford, CA 94305, USA;
Contributors SL: fellow in intraoperative neuromonitoring physician during the case, primary author of case, discussion, and literature review. RD: attending neurointerventionalist during the case, provided angiographic figures and help with literature review. JL: director intraoperative neuromonitoring, reviewed and edited paper. VN: intraoperative neuromonitoring physician, reviewed and edited paper. SCC: intraoperative neuromonitoring physician, reviewed and edited paper. LL: attending intraoperative neuromonitoring physician during the case, reviewed and edited paper.
- Received 16 December 2011
- Accepted 12 January 2012
- Published Online First 19 February 2012
Background and importance It is not uncommon that endovascular balloon test occlusion (BTO) is performed to assess collateral blood flow and risk of injury of permanent occlusion of the internal carotid artery (ICA). This case is the first reported of detection and reversal of the inferolateral trunk (ILT) syndrome in an awake patient during provocative BTO; prompt recognition of the syndrome effectively prevented permanent neurologic deficits.
Clinical presentation The case of a 42-year-old woman is reported who had a left sphenoid wing meningioma with extension into the cavernous sinus and who underwent awake catheter angiography with provocative BTO of the ICA. Serial examinations by intraoperative monitoring neurologists and neurointerventionalists detected acute progressive left retro-orbital pressure followed by sudden inability to adduct the left eye, or a left medial rectus palsy, indicative of the ILT syndrome which led to immediate balloon deflation and resolution of the deficits. The hypothesis was that hypoperfusion of the ILT, an arterial branch of the ICA which provides blood supply to several cranial nerves (CN) III, CN V1 and CN V2, caused her acute symptoms.
Conclusion Although cerebral ischemia is a well known complication of endovascular procedures, CN ischemia is a rare potential risk. Knowledge of cerebrovascular anatomy and serial examinations prevented neurologic deficits; this case underscores the added utility of examinations by intraoperative monitoring neurologists and interdisciplinary collaboration.
Diagnostic catheterization and therapeutic embolization procedures for intracranial lesions arising from the internal carotid artery (ICA) are routinely and successfully performed but carry potential risks of dissection, transient ischemic attack, stroke and retinal ischemia. At our institution, diagnostic and interventional angiograms are often performed on awake patients accompanied by continuous neurophysiologic monitoring. The goal of this comprehensive approach is to maintain the integrity of the CNS and to allow for provocative testing with detailed serial neurologic examinations prior to permanent embolization of vascular lesions, such as meningiomas, aneurysms, arteriovenous malformations (AVMs) or hemangioblastomas. It is not uncommon that endovascular balloon test occlusion (BTO) is performed during evaluation of a sphenoid wing meningioma of the dominant hemisphere to assess collateral blood flow and the risk of injury after permanent occlusion of the ICA.1 We report a unique case of detection and reversal of the inferolateral trunk (ILT) syndrome by intraoperative neuromonitoring (IONM) neurologists and neurointerventionalists during BTO.
We report the case of a 42-year-old woman who underwent diagnostic catheter angiography and provocative BTO of the ICA for a left sphenoid wing meningioma with extension into the cavernous sinus. During BTO, she developed acute progressive left retro-orbital pressure and sudden inability to adduct the left eye, the latter finding consistent with a left eye medial rectus palsy, confirmed by serial neurologic examinations.
The patient initially presented with 2 years of worsening retro-orbital headaches and progressive visual loss in the left eye, subsequently found on brain MRI to have a left cavernous sinus meningioma encasing the left ICA with direct compression of the left optic nerve (figure 1A, B). A baseline pre-procedure neurologic examination revealed a deficit only in the left eye nasal visual field of poor visual acuity limited to detection of motion. An awake diagnostic catheter angiogram was performed with continuous neuromonitoring that included upper extremity somatosensory evoked potentials (SSEPs) and eight channel EEG. Mean arterial pressure during the procedure was maintained at 20 mm Hg lower than the patient's baseline with a nitroprusside drip. After the region of interest in the left ICA was identified, the neurointerventionalists proceeded with BTO of the cervical ICA with serial detailed neurologic examination performed by neurologists of the IONM team (figure 2A, B). Dedicated neurologic examinations included mental status, language testing with reading, naming, memory testing, cranial nerves, including extraocular movements, strength in four limbs, finger and foot taps and light touch. Although visual fields were also serially assessed, confrontation testing was not relied upon because of the patient's baseline poor visual acuity in the left eye.
Almost instantaneously on full inflation of the balloon, the patient reported a mild sensation of pressure behind the left orbit. Her neurologic examination, SSEPs and EEG remained stable. By 10 min, she reported progressively worsening left retro-orbital pressure and altered sensation in the left forehead and nasal areas, although her neurologic examination otherwise remained at baseline. At approximately 17 min, her head pressure escalated to 7/10 on the pain scale, she looked visibly distressed and her examination revealed an acutely dysconjugate gaze with inability to adduct the left eye. The balloon was immediately deflated and the patient reported nearly immediate relief of retro-orbital pain. A repeat examination at approximately 3 min after balloon deflation showed return to her baseline neurologic status with full resolution of the left medial rectus palsy. Because of the acute neurologic deficit observed during provocative balloon testing, the decision was made not to perform therapeutic embolization of the ICA.
The ILT is an arterial branch typically arising from the horizontal cavernous portion of the ICA (figure 3), approximately at the C4 level.2 ,3 Although anatomic variation exists, the ILT has been identified to arise from the ICA in about 90% of cases.4 ,5 Cranial nerves (CN) III, IV, V1 and VI which course through the cavernous sinus receive vascular supply from the ILT and therefore are at risk during endovascular procedures.2 ,5 ,6 Although the cavernous portion of the carotid artery is often involved in dissection or thrombosis,3 CN deficits are rare because of collateral circulation from the external carotid artery or meningohypophyseal trunk.7 ,8
We hypothesize that BTO caused interruption of arterial blood flow to the ILT and more specifically caused vascular insufficiency involving several branches of the ILT resulting in a transient ischemia attack equivalent to CN III, V1 and V2 (figure 4). The balloon was inflated at the cervical portion of the ICA, proximal to the cavernous ICA where the ILT arises. The patient reported increasing retro-orbital pressure after inflation, likely secondary to ischemia to CN V1 via the anteromedial branch of the ILT. The abnormal subjective sensation reported by the patient to the left forehead and nasal areas could also implicate ischemia to CN V1 and V2; the anterolateral branch of the ILT feeds the arterial supply of CN V2. In addition, at 17 min after inflation, the patient developed an acute dysconjugate gaze with a left medial rectus or partial CN III palsy, also likely secondary to arterial ischemia to either or both the superior and anteromedial branches of the ILT. Although hypoperfusion of the ILT is our leading hypothesis, it is plausible that another arterial branch of the cavernous ICA, including the meningohypophyseal trunk, could have been occluded, leading to vascular insufficiency of the CN.7
This case underscores the importance of serial detailed neurologic examinations by a neurologist during BTO in the catheter angiography suite. BTO was first described by Serbinenko in 1974 and is currently a well established endovascular method of risk stratifying patients for cerebral ischemia during subsequent therapeutic embolization.6 ,9 ,10 In our case, focused clinical examinations at frequent intervals during the critical period were more sensitive than neurophysiologic testing with SSEPs or EEG which remained unchanged. Examinations must also be modified given the constraints of the sterile field and limited mobility of the catheterized patient on the angiography table. Testing time for BTO in the medical literature has been variable, ranging from 15 to 120 min.9 Given our experience, BTO should be performed for at least 20–30 min as a shorter testing interval—for example, 15 min would not have been a sufficient amount of time to detect clinically neurological deficits.10 ,11 Additionally, the patient reported escalating pain and altered sensation before 17 min of BTO, which was not objectively testable on the bedside neurologic examination but in retrospect these symptoms were most likely secondary to true ischemia to CN V1 and V2. Therefore, we advocate that if the patient reports symptoms such as pain or paresthesias that are not easily measurable, the time interval of the BTO should be extended to at least 30 min or longer to improve the diagnostic yield of the test.
In addition, this case highlights the anatomy of the arterial supply of individual CN which may be pertinent during endovascular procedures. The fast onset and offset of symptoms during BTO argued for an arterial ischemic process to CN III, V1 and V2. Prompt recognition of the ILT syndrome during serial neurologic examinations allowed for feedback to the neurointerventionalists, deflation of the balloon and reversal and prevention of permanent neurologic deficits. In addition, at our institution, hypotensive challenge is commonly used to further test the patient's collateral circulation and to reduce the false negative value of the test.11 Although Abud et al have advocated the technique of venous phase symmetry testing wherein risk stratification for predicting the safety of permanent occlusion of the ICA is based solely on angiographic criteria, this technique is not routinely performed at our institution. Venous symmetry testing evaluates for greater than a 2 s delay in filling between the venous phases of the balloon occluded and unoccluded hemispheres.9 However, this technique requires bilateral femoral artery punctures and bilateral cervical artery catheterization and would fail to detect an ILT syndrome or vascular insufficiency to small arterial branches to the ICA.9 ,11 In our case, no angiographic studies were performed during the period of BTO; the ILT was visualized both before and after BTO.
During endovascular procedures of the cavernous carotid artery, retinal ischemia via the ophthalmic branch of the ICA is a well known complication and patients may report phosphenes, scotomata or loss of vision.12 Although rare, cases of the ILT syndrome have been described in the medical literature and treating physicians must be aware of the potential risk of arterial ischemia to CN, especially with evolving endovascular techniques and smaller vessels being catheterized and embolized.2 Capo et al described a case of a complete CN III palsy following endovascular embolization of a left temporal AVM fed by both the middle meningeal artery and ILT,8 however, it was not mentioned if provocative testing, IONM or serial neurologic examinations were employed during the case. CN deficits have also been described following chemotherapy infusion into the ICA and resultant toxicity to the ILT.6 Robinson and associates reported successful selective catheterization and embolization of the ILT in three patients with either meningiomas or AVMs without any neurologic deficits post-procedure2; the lack of postoperative CN deficits was likely secondary to collateral arterial supply.
This case further illustrates the potential for false negative results during BTO with serial neurologic examinations which may be secondary to collateral circulation present distal to the BTO site that is sacrificed during permanent embolization.6 Despite the added benefit of clinical neurologic examinations during BTO, intraoperative serial examinations have a reported false negative rate of 4–10%.7 In a retrospective case series of 481 cerebral angiograms for Wada testing with sodium amobarbital, 54.3% of patients had at least one angiographically identifiable skull base ICA branch; of those cases, the ILT was identified in 50/481 cases or 10.4%.6 Although in Allen's retrospective series no provocative BTO was performed, based on the finding that over 50% of patients had identifiable ICA branches, Allen recommended screening angiography for collateral ICA supply and for procedures employing BTO and inflation of the balloon distal to the site of collateral branches to improve the diagnostic yield of concurrent neurologic examinations.6
Catheterization and embolization of branches of the ICA, although challenging, have been successfully performed through endovascular techniques.2 However, CN deficits secondary to arterial ischemia are potential risks in addition to well known complications of ischemia or dissection.2 This case is the first reported in the medical literature of detection and reversal of the ILT syndrome in an awake patient during provocative BTO during catheter angiography; an interdisciplinary approach with recognition of the syndrome led to balloon deflation, restoration of arterial flow and effectively prevented permanent neurologic deficits. Although ILT syndrome is rare, the team of neurosurgeons, neurointerventional radiologists, neurologists and IONM staff should be mindful of cerebrovascular anatomy during angiography procedures. This case also underscores the added utility of IONM during endovascular procedures, including detailed neurologic examinations by a neurologist in conjunction with neurophysiology studies.
Competing interests None.
Patient consent Obtained.
Provenance and peer review Not commissioned; externally peer reviewed.