A taxonomy for deep cerebral cavernous malformations: subtypes of basal ganglia lesions.

OBJECTIVE: Anatomical taxonomy is a practical tool that has successfully guided clinical decision-making for patients with brain arteriovenous malformations and brainstem cavernous malformations (CMs). Deep CMs are similarly complex lesions that are difficult to access and highly variable in size, shape, and position. The authors propose a novel taxonomy for deep CMs in the basal ganglia based on clinical presentation (syndromes) and anatomical location. METHODS: The taxonomy system was developed and applied to an extensive 2-surgeon experience over 19 years (2001-2019). Lesions involving the basal ganglia were identified and subtyped on the basis of the predominant superficial presentation identified on preoperative MRI. Three subtypes of basal ganglia CMs were defined: caudate (31, 57%), putaminal (16, 30%), and pallidal (7, 13%). Neurological outcomes were assessed using the modified Rankin Scale (mRS). Postoperative mRS scores ≤ 2 were defined as a favorable outcome, and scores > 2 were defined as a poor outcome. Clinical and surgical characteristics and neurological outcomes were compared among subtypes. RESULTS: Fifty-four basal ganglia lesions were identified in 54 patients. Each basal ganglia CM subtype was associated with a recognizable constellation of neurological symptoms. The most common symptoms at presentation were severe or worsening headaches (25, 43%), mild hemiparesis (13, 24%), seizures (7, 13%), and dysmetria or ataxia (6, 11%). Patients with caudate CMs were the most likely to present with headaches and constitutional symptoms. Patients with putaminal CMs were the most likely to present with hemibody sensory deficits and dysmetria or ataxia. Patients with pallidal CMs were the most likely to present with mild hemiparesis and visual field deficits. A single surgical approach was preferred (> 80% of cases) for each basal ganglia subtype: caudate (contralateral transcallosal-transventricular, 28/31, 90%), putaminal (transsylvian-anterior transinsular, 13/16, 81%), and pallidal (transsylvian supracarotid-infrafrontal, 7/7, 100%). Most patients with follow-up had stable or improved mRS scores postoperatively (94%, 44/47); mRS scores of > 2 at final follow-up did not differ among the 3 basal ganglia subtypes. CONCLUSIONS: The study confirms the authors' hypothesis that this taxonomy for basal ganglia CMs meaningfully guides the selection of surgical approach and resection strategy. Furthermore, the proposed taxonomy can increase the diagnostic acumen at the patient bedside, help identify optimal surgical approaches, enhance the consistency of clinical communications and publications, and improve patient outcomes.

A taxonomy for deep cerebral cavernous malformations: subtypes of thalamic lesions.

OBJECTIVE: Anatomical taxonomy is a practical tool to successfully guide clinical decision-making for patients with brain arteriovenous malformations and brainstem cavernous malformations (CMs). Deep cerebral CMs are complex, difficult to access, and highly variable in size, shape, and position. The authors propose a novel taxonomic system for deep CMs in the thalamus based on clinical presentation (syndromes) and anatomical location (identified on MRI). METHODS: The taxonomic system was developed and applied to an extensive 2-surgeon experience from 2001 through 2019. Deep CMs involving the thalamus were identified. These CMs were subtyped on the basis of the predominant surface presentation identified on preoperative MRI. Six subtypes among 75 thalamic CMs were defined: anterior (7/75, 9%), medial (22/75, 29%), lateral (10/75, 13%), choroidal (9/75, 12%), pulvinar (19/75, 25%), and geniculate (8/75, 11%). Neurological outcomes were assessed using modified Rankin Scale (mRS) scores. A postoperative score ≤ 2 was defined as a favorable outcome and > 2 as a poor outcome. Clinical and surgical characteristics and neurological outcomes were compared among subtypes. RESULTS: Seventy-five patients underwent resection of thalamic CMs and had clinical and radiological data available. Their mean age was 40.9 (SD 15.2) years. Each thalamic CM subtype was associated with a recognizable constellation of neurological symptoms. The common symptoms were severe or worsening headaches (30/75, 40%), hemiparesis (27/75, 36%), hemianesthesia (21/75, 28%), blurred vision (14/75, 19%), and hydrocephalus (9/75, 12%). The thalamic CM subtype determined the selection of surgical approach. A single approach was associated with each subtype for most patients. The main exception to this paradigm was that in the surgeons' early experience, pulvinar CMs were resected through a superior parietal lobule-transatrial approach (4/19, 21%), which later evolved to the paramedian supracerebellar-infratentorial approach (12/19, 63%). Relative outcomes implied by mRS scores were unchanged or improved in most patients (61/66, 92%) postoperatively. CONCLUSIONS: This study confirms the authors' hypothesis that this taxonomy for thalamic CMs can meaningfully guide the selection of surgical approach and resection strategy. The proposed taxonomy can increase diagnostic acumen at the patient bedside, help identify optimal surgical approaches, enhance the clarity of clinical communications and publications, and improve patient outcomes.

A taxonomy for brainstem cavernous malformations: subtypes of medullary lesions.

OBJECTIVE: Medullary cavernous malformations are the least common of the brainstem cavernous malformations (BSCMs), accounting for only 14% of lesions in the authors' surgical experience. In this article, a novel taxonomy for these lesions is proposed based on clinical presentation and anatomical location. METHODS: The taxonomy system was applied to a large 2-surgeon experience over a 30-year period (1990-2019). Of 601 patients who underwent microsurgical resection of BSCMs, 551 were identified who had the clinical and radiological information needed for inclusion. These 551 patients were classified by lesion location: midbrain (151 [27%]), pons (323 [59%]), and medulla (77 [14%]). Medullary lesions were subtyped on the basis of their predominant surface presentation. Neurological outcomes were assessed according to the modified Rankin Scale (mRS), with an mRS score ≤ 2 defined as favorable. RESULTS: Five distinct subtypes were defined for the 77 medullary BSCMs: pyramidal (3 [3.9%]), olivary (35 [46%]), cuneate (24 [31%]), gracile (5 [6.5%]), and trigonal (10 [13%]). Pyramidal lesions are located in the anterior medulla and were associated with hemiparesis and hypoglossal nerve palsy. Olivary lesions are found in the anterolateral medulla and were associated with ataxia. Cuneate lesions are located in the posterolateral medulla and were associated with ipsilateral upper-extremity sensory deficits. Gracile lesions are located outside the fourth ventricle in the posteroinferior medulla and were associated with ipsilateral lower-extremity sensory deficits. Trigonal lesions in the ventricular floor were associated with nausea, vomiting, and diplopia. A single surgical approach was preferred (> 90% of cases) for each medullary subtype: the far lateral approach for pyramidal and olivary lesions, the suboccipital-telovelar approach for cuneate lesions, the suboccipital-transcisterna magna approach for gracile lesions, and the suboccipital-transventricular approach for trigonal lesions. Of these 77 patients for whom follow-up data were available (n = 73), 63 (86%) had favorable outcomes and 67 (92%) had unchanged or improved functional status. CONCLUSIONS: This study confirms that the constellation of neurological signs and symptoms associated with a hemorrhagic medullary BSCM subtype is useful for defining the BSCM clinically according to a neurologically recognizable syndrome at the bedside. The proposed taxonomical classifications may be used to guide the selection of surgical approaches, which may enhance the consistency of clinical communications and help improve patient outcomes.

A system of anatomical triangles defining dissection routes to brainstem cavernous malformations: definitions and application to a cohort of 183 patients.

OBJECTIVE: Anatomical triangles defined by intersecting neurovascular structures delineate surgical routes to pathological targets and guide neurosurgeons during dissection steps. Collections or systems of anatomical triangles have been integrated into skull base surgery to help surgeons navigate complex regions such as the cavernous sinus. The authors present a system of triangles specifically intended for resection of brainstem cavernous malformations (BSCMs). This system of triangles is complementary to the authors' BSCM taxonomy that defines dissection routes to these lesions. METHODS: The anatomical triangle through which a BSCM was resected microsurgically was determined for the patients treated during a 23-year period who had both brain MRI and intraoperative photographs or videos available for review. RESULTS: Of 183 patients who met the inclusion criteria, 50 had midbrain lesions (27%), 102 had pontine lesions (56%), and 31 had medullary lesions (17%). The craniotomies used to resect these BSCMs included the extended retrosigmoid (66 [36.1%]), midline suboccipital (46 [25.1%]), far lateral (30 [16.4%]), pterional/orbitozygomatic (17 [9.3%]), torcular (8 [4.4%]), and lateral suboccipital (8 [4.4%]) approaches. The anatomical triangles through which the BSCMs were most frequently resected were the interlobular (37 [20.2%]), vallecular (32 [17.5%]), vagoaccessory (30 [16.4%]), supracerebellar-infratrochlear (16 [8.7%]), subtonsillar (14 [7.7%]), oculomotor-tentorial (11 [6.0%]), infragalenic (8 [4.4%]), and supracerebellar-supratrochlear (8 [4.4%]) triangles. New but infrequently used triangles included the vertebrobasilar junctional (1 [0.5%]), supratrigeminal (3 [1.6%]), and infratrigeminal (5 [2.7%]) triangles. Overall, 15 BSCM subtypes were exposed through 6 craniotomies, and the approach was redirected to the BSCM by one of the 14 triangles paired with the BSCM subtype. CONCLUSIONS: A system of BSCM triangles, including 9 newly defined triangles, was introduced to guide dissection to these lesions. The use of an anatomical triangle better defines the pathway taken through the craniotomy to the lesion and refines the conceptualization of surgical approaches. The triangle concept and the BSCM triangle system increase the precision of dissection through subarachnoid corridors, enhance microsurgical execution, and potentially improve patient outcomes.

Anatomical Triangles for Use in Skull Base Surgery: A Comprehensive Review.

Procedures performed along the skull base require technical prowess and a thorough knowledge of cranial anatomy to navigate the operative field. Anatomical triangles created by unique anatomical structures serve as landmarks to guide the surgeon during meticulous skull base procedures. The corridors rapidly orient the surgeon to the operative field and permit greater confidence regarding skull base position during dissection. A literature review was performed with use of the PubMed database and reference list searches from full-text reviewed articles, which resulted in the identification of 31 distinct anatomical triangles of the skull base. The 31 anatomical triangles are categorized into a corresponding cranial fossa or the extracranial subsection. The triangles described in the manuscript include junctional, interoptic, precommunicating, opticocarotid, supracarotid, parasellar, clinoidal, oculomotor, carotid-oculomotor, supratrochlear, infratrochlear, anteromedial, quadrangular, anterolateral, posteromedial, posterolateral, lateral, superior petrosal, oculomotor-tentorial, inferomedial, inferolateral, glossopharyngo-cochlear, vagoaccessory, suprahypoglossal, hypoglossal-hypoglossal, infrahypoglossal, parapetrosal, suprameatal, retromeatal, suboccipital, and the inferior suboccipital. The goal of this review is to create a comprehensive resource for existing skull base triangles that includes borders, contents, surgical applications, and illustrations to enhance awareness and inform microsurgical dissection.

A taxonomy for brainstem cavernous malformations: subtypes of pontine lesions. Part 1: basilar, peritrigeminal, and middle peduncular.

OBJECTIVE: Brainstem cavernous malformations (BSCMs) are complex, difficult to access, and highly variable in size, shape, and position. The authors have proposed a novel taxonomy for pontine cavernous malformations (CMs) based upon clinical presentation (syndromes) and anatomical location (findings on MRI). METHODS: The proposed taxonomy was applied to a 30-year (1990-2019), 2-surgeon experience. Of 601 patients who underwent microsurgical resection of BSCMs, 551 with appropriate data were classified on the basis of BSCM location: midbrain (151 [27%]), pons (323 [59%]), and medulla (77 [14%]). Pontine lesions were then subtyped on the basis of their predominant surface presentation identified on preoperative MRI. Neurological outcomes were assessed according to the modified Rankin Scale, with a score ≤ 2 defined as favorable. RESULTS: The 323 pontine BSCMs were classified into 6 distinct subtypes: basilar (6 [1.9%]), peritrigeminal (53 [16.4%]), middle peduncular (MP) (100 [31.0%]), inferior peduncular (47 [14.6%]), rhomboid (80 [24.8%]), and supraolivary (37 [11.5%]). Part 1 of this 2-part series describes the taxonomic basis for the first 3 of these 6 subtypes of pontine CM. Basilar lesions are located in the anteromedial pons and associated with contralateral hemiparesis. Peritrigeminal lesions are located in the anterolateral pons and are associated with hemiparesis and sensory changes. Patients with MP lesions presented with mild anterior inferior cerebellar artery syndrome with contralateral hemisensory loss, ipsilateral ataxia, and ipsilateral facial numbness without cranial neuropathies. A single surgical approach and strategy were preferred for each subtype: for basilar lesions, the pterional craniotomy and anterior transpetrous approach was preferred; for peritrigeminal lesions, extended retrosigmoid craniotomy and transcerebellopontine angle approach; and for MP lesions, extended retrosigmoid craniotomy and trans-middle cerebellar peduncle approach. Favorable outcomes were observed in 123 of 143 (86%) patients with follow-up data. There were no significant differences in outcomes between the 3 subtypes or any other subtypes. CONCLUSIONS: The neurological symptoms and key localizing signs associated with a hemorrhagic pontine subtype can help to define that subtype clinically. The proposed taxonomy for pontine CMs meaningfully guides surgical strategy and may improve patient outcomes.

A taxonomy for brainstem cavernous malformations: subtypes of pontine lesions. Part 2: inferior peduncular, rhomboid, and supraolivary.

OBJECTIVE: Part 2 of this 2-part series on pontine cavernomas presents the taxonomy for subtypes 4-6: inferior peduncular (IP) (subtype 4), rhomboid (5), and supraolivary (6). (Subtypes 1-3 are presented in Part 1.) The authors have proposed a novel taxonomy for pontine cavernous malformations based on clinical presentation (syndromes) and anatomical location (MRI findings). METHODS: The details of taxonomy development are described fully in Part 1 of this series. In brief, pontine lesions (323 of 601 [53.7%] total lesions) were subtyped on the basis of predominant surface presentation identified on preoperative MRI. Neurological outcomes were assessed according to the modified Rankin Scale, with score ≤ 2 defined as favorable. RESULTS: The 323 pontine brainstem cavernous malformations were classified into 6 distinct subtypes: basilar (6 [1.9%]), peritrigeminal (53 [16.4%]), middle peduncular (100 [31.0%]), IP (47 [14.6%]), rhomboid (80 [24.8%]), and supraolivary (37 [11.5%]). Subtypes 4-6 are the subject of the current report. IP lesions are located in the inferolateral pons and are associated with acute vestibular syndrome. Rhomboid lesions present to the fourth ventricle floor and are associated with disconjugate eye movements. Larger lesions may cause ipsilateral facial weakness. Supraolivary lesions present to the surface at the ventral pontine underbelly. Ipsilateral abducens palsy is a strong localizing sign for this subtype. A single surgical approach and strategy were preferred for subtypes 4-6: for IP cavernomas, the suboccipital craniotomy and telovelar approach predominated; for rhomboid lesions, the suboccipital craniotomy and transventricular approach were preferred; and for supraolivary malformations, the far lateral craniotomy and transpontomedullary sulcus approach were preferred. Favorable outcomes were observed in 132 of 150 (88%) patients with follow-up. There were no significant differences in outcomes between subtypes. CONCLUSIONS: The neurological symptoms and signs associated with a hemorrhagic pontine subtype can help define that subtype clinically with key localizing signs. The proposed taxonomy for pontine cavernous malformation subtypes 4-6 meaningfully guides surgical strategy and may improve patient outcomes.

A taxonomy for brainstem cavernous malformations: subtypes of midbrain lesions.

OBJECTIVE: Anatomical taxonomy is a practical tool that has successfully guided clinical decision-making for patients with brain arteriovenous malformations. Brainstem cavernous malformations (BSCMs) are similarly complex lesions that are difficult to access and highly variable in size, shape, and position. The authors propose a novel taxonomy for midbrain cavernous malformations based on clinical presentation (syndromes) and anatomical location (identified with MRI). METHODS: The taxonomy system was developed and applied to an extensive 2-surgeon experience over a 30-year period (1990-2019). Of 551 patients with appropriate data who underwent microsurgical resection of BSCMs, 151 (27.4%) had midbrain lesions. These lesions were further subtyped on the basis of predominant surface presentation identified on preoperative MRI. Five distinct subtypes of midbrain BSCMs were defined: interpeduncular (7 lesions [4.6%]), peduncular (37 [24.5%]), tegmental (73 [48.3%]), quadrigeminal (27 [17.9%]), and periaqueductal (7 [4.6%]). Neurological outcomes were assessed using modified Rankin Scale (mRS) scores. A postoperative score ≤ 2 was defined as a favorable outcome; a score > 2 was defined as a poor outcome. Clinical and surgical characteristics and neurological outcomes were compared among subtypes. RESULTS: Each midbrain BSCM subtype was associated with a recognizable constellation of neurological symptoms. Patients with interpeduncular lesions commonly presented with ipsilateral oculomotor nerve palsy and contralateral cerebellar ataxia or dyscoordination. Peduncular lesions were associated with contralateral hemiparesis and ipsilateral oculomotor nerve palsy. Patients with tegmental lesions were the most likely to present with contralateral sensory deficits, whereas those with quadrigeminal lesions commonly presented with the features of Parinaud syndrome. Periaqueductal lesions were the most likely to cause obstructive hydrocephalus. A single surgical approach was preferred (> 90% of cases) for each midbrain subtype: interpeduncular (transsylvian-interpeduncular approach [7/7 lesions]), peduncular (transsylvian-transpeduncular [24/37]), tegmental (lateral supracerebellar-infratentorial [73/73]), quadrigeminal (midline or paramedian supracerebellar-infratentorial [27/27]), and periaqueductal (transcallosal-transchoroidal fissure [6/7]). Favorable outcomes (mRS score ≤ 2) were observed in most patients (110/136 [80.9%]) with follow-up data. No significant differences in outcomes were observed between subtypes (p = 0.92). CONCLUSIONS: The study confirmed the authors' hypothesis that taxonomy for midbrain BSCMs can meaningfully guide the selection of surgical approach and resection strategy. The proposed taxonomy can increase diagnostic acumen at the patient bedside, help identify optimal surgical approaches, enhance the consistency of clinical communications and publications, and improve patient outcomes.

The Superficial Anastomosing Veins of the Human Brain Cortex: A Microneurosurgical Anatomical Study.

Introduction: In this microneurosurgical and anatomical study, we characterized the superficial anastomosing veins of the human brain cortex in human specimens. Material and Methods: We used 21 brain preparations fixed in formalin (5%) that showed no pathological changes and came from the autopsy sections. The superficial veins were dissected out of the arachnoid with the aid of a surgical microscope. Results: We dissected nine female and 12 male brain specimens, with an average age of 71 ± 11 years (range 51-88 years). We classified the superficial veins in five types: (I) the vein of Trolard as the dominat vein; (II) the vein of Labbé as the dominant vein; (III) a dominant sylvian vein group, and the veins of Trolard and Labbé nonexistent or only rudimentary present without contact to the Sylvian vein group; (IV) very weak sylvian veins with the veins of Trolard and Labbé codominant; and V) direct connection of Trolard and Labbé bypassing the Sylvian vein group. The vein of Trolard was dominant (Type I) in 21.4% and the vein of Labbé (Type II) in 16.7%. A dominant sylvian vein group (Type III) was found in 42.9%. Type IV and Type V were found in 14.3 and 4.7% respectively. Conclusion: No systematic description or numerical distribution of the superior anastomotic vein (V. Trolard) and inferior anastomotic vein (V. Labbé) has been found in the existing literature. This study aimed to fill this gap in current literature and provide data to neurosurgeons for the practical planning of surgical approaches.