Endoscopic Endonasal Transclival Approach to the Ventral Brainstem: Anatomic Study of the Safe Entry Zones Combining Fiber Dissection Technique with 7 Tesla Magnetic Resonance Guided Neuronavigation

Endoscopic Endonasal Transclival Approach to the Ventral Brainstem: Anatomic Study of the Safe... Abstract BACKGROUND Treatment of intrinsic lesions of the ventral brainstem is a surgical challenge that requires complex skull base antero- and posterolateral approaches. More recently, endoscopic endonasal transclival approach (EETA) has been reported in the treatment of selected ventral brainstem lesions. OBJECTIVE In this study we explored the endoscopic ventral brainstem anatomy with the aim to describe the degree of exposure of the ventral safe entry zones. In addition, we used a newly developed method combining traditional white matter dissection with high-resolution 7T magnetic resonance imaging (MRI) of the same specimen coregistered using a neuronavigation system. METHODS Eight fresh-frozen latex-injected cadaver heads underwent EETA. Additional 8 formalin-fixed brainstems were dissected using Klingler technique guided by ultra-high resolution MRI. RESULTS The EETA allows a wide exposure of different safe entry zones located on the ventral brainstem: the exposure of perioculomotor zone requires pituitary transposition and can be hindered by superior cerebellar artery. The peritrigeminal zone was barely visible and its exposure required an extradural anterior petrosectomy. The anterolateral sulcus of the medulla was visible in most of specimens, although its close relationship with the corticospinal tract makes it suboptimal as an entry point for intrinsic lesions. In all cases, the use of 7T-MRI allowed the identification of tiny fiber bundles, improving the quality of the dissection. CONCLUSIONS Exposure of the ventral brainstem with EETA requires mastering surgical maneuvers, including pituitary transposition and extradural petrosectomy. The correlation of fiber dissection with 7T-MRI neuronavigation significantly improves the understanding of the brainstem anatomy. Brainstem, Endoscopy, Skull base, Endoscopic endonasal, Cavernoma, 7 Tesla magnetic resonance, Klingler, Fiber dissection ABBREVIATIONS ABBREVIATIONS AICA anteroinferior cerebellar artery BA basilar artery CST corticospinal tract EETA endoscopic endonasal transclival approach FOV field-of-view ICA internal carotid artery ML medial lemniscus MRI magnetic resonance imaging PCA posterior cerebral artery RN red nucleus SCA superior cerebellar artery VA vertebral artery The majority of brainstem cavernomas are operated on through the regions of the brainstem where they reach the surface. However, when lesions do not emerge from the pia, surgical strategies require small neurotomies in safe entry zones on the brainstem surface where critical neural structures are sparse and few perforating arteries are present.1–7 Several transcranial approaches have been described to access intrinsic lesions of the ventral brainstem; nevertheless, these approaches require extensive drilling of bone, manipulation of neurovascular structures, and do not provide a direct working angle to the ventral brainstem.8–14 During the past decade, skull-base surgery has been enriched by the introduction of endoscopic endonasal approaches to access lesions located in the ventral skull-base.15–20 More recently, anatomic and clinical studies concerning the endoscopic endonasal transclival approach (EETA) documented the possibility of obtaining a wide exposure of the brainstem ventral surface.21–24 In the present study, we explored the anterolateral surface of brainstem via EETA to evaluate the degree of exposure of the safe entry zones. In addition, the identified safe entry zones were further investigated combining white matter dissection with ultra-high-field magnetic resonance imaging (MRI) in formalin-fixed brainstems coregistered using a neuronavigation system. METHODS The study was approved by the ethical committee of the Faculty of Medicine of our University. The specimens were obtained in the first 12-h postmortem from donors without clinical history of neurological disease. Endoscopic Endonasal Transclival Approach Endoscopic dissections were performed on 8 fresh-frozen latex-injected cadaver heads using a rigid endoscope 4 mm in diameter, 18 cm in length, with 0° optics (Karl-Storz, Tuttlingen, Germany) connected to a light source through and a camera. EETA was performed following the steps as described in the literature.15,16,18,19,21 The nasal steps of dissections included monolateral right middle turbinectomy, lateralization of the contralateral middle turbinate, posterior septectomy, anterior sphenoidotomy, and antrostomy of the maxillary sinus. After opening of the sella, the tuberculum sellae, the dorsum sellae, and the posterior clinoids were removed exposing the retrosellar area. The vomer and the sphenoidal floor were removed. The pterygoid canals were identified about 4 mm lateral to the vomer–sphenoid junction.17 The bone of the clivus was progressively removed down to the anterior arch of C1. The caudal lateral boundaries of the bone removal were represented by the anterior third of the occipital condyles. In all specimens an extradural anterior petrosectomy was performed to evaluate the effect of lateral extending of bone removal on exposure of peritrigeminal zone.22 At this point, the dura was opened along the midline. The resulting intradural working area is a rectangular space delimited superiorly by the indentation of tuberculum sellae, caudally by the anterior arch of C1, and laterally by the parasellar and paraclival segments of the internal carotid artery (ICA). As previously described, the operative field obtained with EETA can be divided into 3 surgical working areas, namely upper, middle, and lower levels (Figure 1).17 The grade of exposure of selected safe entry zones for each working area was evaluated. The safe entry zones explored were as follows: the lateral mesencephalic sulcus and the perioculomotor zone at the upper level, the peritrigeminal zone at the middle level, and the anterolateral sulcus at the lower level. The extent of exposure for each working area was evaluated by using a numerical grading system as described by Kawashima et al.25 A value of 0 refers to a structure that is not exposed at all, a value of 1 indicates that the structure is exposed in less than 50% of specimens, a value of 2 indicates an exposure comprised between 50% and 99% of specimens, and a value of 3 indicates full exposure in 100% of specimens. FIGURE 1. View largeDownload slide Identification of the surgical working areas via the EETA. The upper level is limited by the posterior clinoid processes superiorly and by the abducens nerves entering the dural porus inferiorly (red-dotted line). The middle level is limited upwardly by a line joining the abducens nerves and downwardly by a line joining the intracranial openings of the hypoglossal canal (pale blue-dotted line). The lower level is bounded superiorly by the middle level and inferiorly by the superior margin of C1 (green-dotted line). AICA, anteroinferior cerebellar artery; BA, basilar artery; ICAc, clival segment of the internal carotid artery; ICAs, sellar segment of the internal carotid artery; ON, optic nerve; pg, pituitary gland; VA, vertebral artery; VI, abducens nerve; XII, hypoglossal nerve. FIGURE 1. View largeDownload slide Identification of the surgical working areas via the EETA. The upper level is limited by the posterior clinoid processes superiorly and by the abducens nerves entering the dural porus inferiorly (red-dotted line). The middle level is limited upwardly by a line joining the abducens nerves and downwardly by a line joining the intracranial openings of the hypoglossal canal (pale blue-dotted line). The lower level is bounded superiorly by the middle level and inferiorly by the superior margin of C1 (green-dotted line). AICA, anteroinferior cerebellar artery; BA, basilar artery; ICAc, clival segment of the internal carotid artery; ICAs, sellar segment of the internal carotid artery; ON, optic nerve; pg, pituitary gland; VA, vertebral artery; VI, abducens nerve; XII, hypoglossal nerve. Fiber Dissection and Neuronavigation Eight formalin-fixed brainstems were prepared using the method originally described by Klinger26,27 in order to dissect the safe entry zones identified through EETA. Vitamin-E fiducials were placed on the lateral aspects of the brainstem avoiding the regions previously selected for fiber dissection.28 MRI sections were performed on a 7.0-T BioSpec70/30 horizontal scanner (Bruker-BioSpin, Ettlingen, Germany), equipped with a circular polarized transmit/receive coil for rabbit-body-imaging with a 15.4 cm inner diameter actively shielded gradient system (400 mT/m). Specimens were placed horizontally inside a hermetically sealed plastic tube with the following dimensions: diameter: 35 mm, length: 125 mm. Tripilot scans were performed for positioning the specimens inside the magnet. T1-weighetd anatomic images were acquired using the Fast-Low-Angle-Shot sequence (parameters: repetition time = 4390.09 ms, echo time = 8.46 ms, field-of-view (FOV) = 130 mm × 80 mm, matrix size = 394 pixels × 242 pixels, with a resulting in-plane resolution of 0.33 mm × 0.33 mm in 1-mm slice thickness). The acquisition of this set of images was repeated three times acquiring the highest in-plane resolution for each orientation (axial, coronal, and sagittal) maintaining the same FOV. The MRI was subsequently loaded in a Medtronic-AxiEM electromagnetic-neuronavigation system (Medtronic, Minneapolis, Minnesota), and the brainstems were registered using the fiducials previously located on the lateral aspects. The dissections were performed in a stepwise manner under microscopic magnification with wooden spatulas and microsurgical instruments. After exposure of fiber tracts and their nuclei, several measurements were taken with an electronic digital caliper (±0.01 mm; Table 1). TABLE 1. Measurements From 8 Brainstems Bilaterally (n = 16) Midbrain Mean (range), SD, mm mm Width of interpeduncular fossa 5.1 (3.2-7.5) 1.4 Substantia nigra to frontopontine tract 3.2 (1-7.3) 1.83 ML to frontopontine tract 13.1 (10.8-16.5) 1.79 RN to frontopontine tract 7.8 (5.2-12.1) 1.55 Substantia nigra to oculomotor nerve exit point 1.4 (1.1-1.8) 0.36 Pons  Trigeminal nerve exit point to facial nerve exit point 8.9 (6.8-9.6) 1.30  Trigeminal nerve exit point to trigeminal motor nucleus 13.7 (10.9-16.3) 1.89  Trigeminal motor nucleus to facial nerve exit point 10 (6.6-13.7) 3.53  Facial nerve exit point to CST 6.9 (4.4-7.8) 1.12  Acoustic nerve exit point to CST 9.5 (7.5-12) 1.37  Trigeminal nerve intrapontine segment to CST 6.1 (4-8.2) 1.134  Trigeminal motor nucleus to CST 7 (4.7-9.8) 1.68 Medulla  Anterior median fissure width 0.7 (0.2-1.3) 0.33  Pyramidal width 11 (9.3-11.9) 0.76  Olivary nucleus rostrocaudal length 13.5 (9.9-16.2) 1.6  Olivary nucleus anteroposterior length 4.2 (2.9-5.6) 0.7  Olivary nucleus to trigeminal spinal tract 1.4 (0.7-2.6) 0.6  Pontomedullary sulcus to pyramidal decussation 27.1 (24.9-29.2) 1.9 Midbrain Mean (range), SD, mm mm Width of interpeduncular fossa 5.1 (3.2-7.5) 1.4 Substantia nigra to frontopontine tract 3.2 (1-7.3) 1.83 ML to frontopontine tract 13.1 (10.8-16.5) 1.79 RN to frontopontine tract 7.8 (5.2-12.1) 1.55 Substantia nigra to oculomotor nerve exit point 1.4 (1.1-1.8) 0.36 Pons  Trigeminal nerve exit point to facial nerve exit point 8.9 (6.8-9.6) 1.30  Trigeminal nerve exit point to trigeminal motor nucleus 13.7 (10.9-16.3) 1.89  Trigeminal motor nucleus to facial nerve exit point 10 (6.6-13.7) 3.53  Facial nerve exit point to CST 6.9 (4.4-7.8) 1.12  Acoustic nerve exit point to CST 9.5 (7.5-12) 1.37  Trigeminal nerve intrapontine segment to CST 6.1 (4-8.2) 1.134  Trigeminal motor nucleus to CST 7 (4.7-9.8) 1.68 Medulla  Anterior median fissure width 0.7 (0.2-1.3) 0.33  Pyramidal width 11 (9.3-11.9) 0.76  Olivary nucleus rostrocaudal length 13.5 (9.9-16.2) 1.6  Olivary nucleus anteroposterior length 4.2 (2.9-5.6) 0.7  Olivary nucleus to trigeminal spinal tract 1.4 (0.7-2.6) 0.6  Pontomedullary sulcus to pyramidal decussation 27.1 (24.9-29.2) 1.9 View Large TABLE 1. Measurements From 8 Brainstems Bilaterally (n = 16) Midbrain Mean (range), SD, mm mm Width of interpeduncular fossa 5.1 (3.2-7.5) 1.4 Substantia nigra to frontopontine tract 3.2 (1-7.3) 1.83 ML to frontopontine tract 13.1 (10.8-16.5) 1.79 RN to frontopontine tract 7.8 (5.2-12.1) 1.55 Substantia nigra to oculomotor nerve exit point 1.4 (1.1-1.8) 0.36 Pons  Trigeminal nerve exit point to facial nerve exit point 8.9 (6.8-9.6) 1.30  Trigeminal nerve exit point to trigeminal motor nucleus 13.7 (10.9-16.3) 1.89  Trigeminal motor nucleus to facial nerve exit point 10 (6.6-13.7) 3.53  Facial nerve exit point to CST 6.9 (4.4-7.8) 1.12  Acoustic nerve exit point to CST 9.5 (7.5-12) 1.37  Trigeminal nerve intrapontine segment to CST 6.1 (4-8.2) 1.134  Trigeminal motor nucleus to CST 7 (4.7-9.8) 1.68 Medulla  Anterior median fissure width 0.7 (0.2-1.3) 0.33  Pyramidal width 11 (9.3-11.9) 0.76  Olivary nucleus rostrocaudal length 13.5 (9.9-16.2) 1.6  Olivary nucleus anteroposterior length 4.2 (2.9-5.6) 0.7  Olivary nucleus to trigeminal spinal tract 1.4 (0.7-2.6) 0.6  Pontomedullary sulcus to pyramidal decussation 27.1 (24.9-29.2) 1.9 Midbrain Mean (range), SD, mm mm Width of interpeduncular fossa 5.1 (3.2-7.5) 1.4 Substantia nigra to frontopontine tract 3.2 (1-7.3) 1.83 ML to frontopontine tract 13.1 (10.8-16.5) 1.79 RN to frontopontine tract 7.8 (5.2-12.1) 1.55 Substantia nigra to oculomotor nerve exit point 1.4 (1.1-1.8) 0.36 Pons  Trigeminal nerve exit point to facial nerve exit point 8.9 (6.8-9.6) 1.30  Trigeminal nerve exit point to trigeminal motor nucleus 13.7 (10.9-16.3) 1.89  Trigeminal motor nucleus to facial nerve exit point 10 (6.6-13.7) 3.53  Facial nerve exit point to CST 6.9 (4.4-7.8) 1.12  Acoustic nerve exit point to CST 9.5 (7.5-12) 1.37  Trigeminal nerve intrapontine segment to CST 6.1 (4-8.2) 1.134  Trigeminal motor nucleus to CST 7 (4.7-9.8) 1.68 Medulla  Anterior median fissure width 0.7 (0.2-1.3) 0.33  Pyramidal width 11 (9.3-11.9) 0.76  Olivary nucleus rostrocaudal length 13.5 (9.9-16.2) 1.6  Olivary nucleus anteroposterior length 4.2 (2.9-5.6) 0.7  Olivary nucleus to trigeminal spinal tract 1.4 (0.7-2.6) 0.6  Pontomedullary sulcus to pyramidal decussation 27.1 (24.9-29.2) 1.9 View Large RESULTS Endoscopic Dissection The upper level is limited upward by a line joining the 2 posterior clinoid processes and inferiorly by a line joining the abducens nerves (VI) entering the dural porus (Figure 1). Because of the pituitary gland, the exposure of the ventral midbrain is limited (Figure 2A). The transection of the inferior hypophyseal artery and the dissection of ligaments between the pituitary gland and the lateral aspect of the dura allowed the gland to be mobilized cranially (Figure 2B).29 After this maneuver, the basilar-apex, the superior cerebellar artery (SCA), the P1 segment of the posterior cerebral artery (PCA), and the oculomotor nerves (III) were visible (Figure 2C and 2D). The lateral mesencephalic sulcus, which extends from the pontomesencephalic sulcus to the medial geniculate body, was not visible. The perioculomotor zone (Figure 2E), which is located laterally to the emergence of the III on the medial one-third of the cerebral peduncle, was visible in 60% of the specimens. In the remaining cases, the anterior pontomesencephalic segment of SCA with its short perforators obstructed the exposure of the area (Table 2). FIGURE 2. View largeDownload slide Endoscopic view of the upper working area. A, At this level the pituitary gland limits the exposure of the ventral surface of the midbrain. B, After dissection of the soft attachments of the pituitary gland with the lateral sellar dura, the pituitary gland can be mobilized with exposure of the C, basilar apex, superior cerebellar artery, P1 and P2 segments of PCA, and the oculomotor nerves. D, The operative access to the perioculomotor zone passes inferiorly to the superior cerebellar artery and is limited by a perforating branch. E, The perioculomotor zone is exposed (orange area). BA, basilar artery; ICAc, clival segment of the internal carotid artery; ICAs, sellar segment of the internal carotid artery; OCR, opticocarotid recess; ON, optic nerve; pg, pituitary gland; PCA, posterior cerebral artery; SCA, superior cerebellar artery; III, oculomotor nerve; VI, abducens nerve. FIGURE 2. View largeDownload slide Endoscopic view of the upper working area. A, At this level the pituitary gland limits the exposure of the ventral surface of the midbrain. B, After dissection of the soft attachments of the pituitary gland with the lateral sellar dura, the pituitary gland can be mobilized with exposure of the C, basilar apex, superior cerebellar artery, P1 and P2 segments of PCA, and the oculomotor nerves. D, The operative access to the perioculomotor zone passes inferiorly to the superior cerebellar artery and is limited by a perforating branch. E, The perioculomotor zone is exposed (orange area). BA, basilar artery; ICAc, clival segment of the internal carotid artery; ICAs, sellar segment of the internal carotid artery; OCR, opticocarotid recess; ON, optic nerve; pg, pituitary gland; PCA, posterior cerebral artery; SCA, superior cerebellar artery; III, oculomotor nerve; VI, abducens nerve. TABLE 2. Exposure of Anatomic Structures at the Midbrain Upper Level With Transclival Approacha Exposure after transclival approach Neural structures  Anterior mesencephalic zone 2  Lateral mesencephalic sulcus 0  Oculomotor nerve 3  Mammillary body 2 Arteries  BA 3  SCA (anterior pontomesencephalic segment) 3  PCA (P1 segment) 2  Posterior communicating artery 1 Exposure after transclival approach Neural structures  Anterior mesencephalic zone 2  Lateral mesencephalic sulcus 0  Oculomotor nerve 3  Mammillary body 2 Arteries  BA 3  SCA (anterior pontomesencephalic segment) 3  PCA (P1 segment) 2  Posterior communicating artery 1 a The scoring system is as follows: 0, no exposure in any specimen; 1, structure exposed in less than 50% of specimens; 2, structure exposed in more than 50% of specimens; and 3, complete exposure in 100% of specimens. View Large TABLE 2. Exposure of Anatomic Structures at the Midbrain Upper Level With Transclival Approacha Exposure after transclival approach Neural structures  Anterior mesencephalic zone 2  Lateral mesencephalic sulcus 0  Oculomotor nerve 3  Mammillary body 2 Arteries  BA 3  SCA (anterior pontomesencephalic segment) 3  PCA (P1 segment) 2  Posterior communicating artery 1 Exposure after transclival approach Neural structures  Anterior mesencephalic zone 2  Lateral mesencephalic sulcus 0  Oculomotor nerve 3  Mammillary body 2 Arteries  BA 3  SCA (anterior pontomesencephalic segment) 3  PCA (P1 segment) 2  Posterior communicating artery 1 a The scoring system is as follows: 0, no exposure in any specimen; 1, structure exposed in less than 50% of specimens; 2, structure exposed in more than 50% of specimens; and 3, complete exposure in 100% of specimens. View Large The middle level is bounded superiorly by a line joining the abducens nerves and inferiorly by a line joining the intracranial openings of the hypoglossal canal (Figure 3A). At this level the pons and medulla ventral surfaces, the bulbopontine sulcus with the emergence of the VI, the basilar artery (BA), and the anterior segment of anteroinferior cerebellar artery (AICA) were visualized. The petrous apex limits the dissection of the peritrigeminal zone, located between the emergences of trigeminal (V) and facial nerves (VII). This area is located medial to the V and laterally to the corticospinal tract (CST). The exposure of the peritrigeminal zone was obtained in all specimens by an extradural anterior petrosectomy behind the paraclival carotids and then moving the endoscope laterally under the course of the VI (Figure 3B). After the anterior petrosectomy, the lateral pontine segment of the AICA was observed in its course toward the cerebellopontine angle. In 8 sides (50%) the AICA passed through the peritrigeminal zone halfway between the V superiorly and the VII and vestibulocochlear nerves inferiorly. In this scenario, the surgical access requires a careful dissection in order to avoid vascular injury of perforating arteries (Table 3). FIGURE 3. View largeDownload slide Endoscopic view of the middle working area. A, The abducens nerve leaves the brainstem from the bulbopontine sulcus and presents a caudocranial and mediolateral direction toward the Dorello's canal. B, Drilling of the petrous bone is required to fully expose the apparent origin of trigeminal nerve in the pons and the peritrigeminal zone (orange area). AICA, anteroinferior cerebellar artery; BA, basilar artery; VA, vertebral artery; pb, petrous bone; V, trigeminal nerve; VI, abducens nerve; VII, facial nerve; VIII, vestibulocochlear nerve; IX, glossopharyngeal nerve; X, vagal nerve; XII, hypoglossal nerve. FIGURE 3. View largeDownload slide Endoscopic view of the middle working area. A, The abducens nerve leaves the brainstem from the bulbopontine sulcus and presents a caudocranial and mediolateral direction toward the Dorello's canal. B, Drilling of the petrous bone is required to fully expose the apparent origin of trigeminal nerve in the pons and the peritrigeminal zone (orange area). AICA, anteroinferior cerebellar artery; BA, basilar artery; VA, vertebral artery; pb, petrous bone; V, trigeminal nerve; VI, abducens nerve; VII, facial nerve; VIII, vestibulocochlear nerve; IX, glossopharyngeal nerve; X, vagal nerve; XII, hypoglossal nerve. TABLE 3. Exposure of Anatomic Structures at the Pons Middle Level With Transclival Approacha Exposure after transclival approach Exposure after transclival approach with extradural anterior petrosectomy Neural structures  Peritrigeminal zone 0 3  Facial nerve 1 3  Trigeminal nerve 0 3  Abducens nerve 3 3 Arteries  BA 3 3  Anterior inferior cerebellar artery (anterior pontine segment) 3 3  Anterior inferior cerebellar artery (lateral pontine segment) 1 3 Exposure after transclival approach Exposure after transclival approach with extradural anterior petrosectomy Neural structures  Peritrigeminal zone 0 3  Facial nerve 1 3  Trigeminal nerve 0 3  Abducens nerve 3 3 Arteries  BA 3 3  Anterior inferior cerebellar artery (anterior pontine segment) 3 3  Anterior inferior cerebellar artery (lateral pontine segment) 1 3 a Scoring system is as in Table 2. View Large TABLE 3. Exposure of Anatomic Structures at the Pons Middle Level With Transclival Approacha Exposure after transclival approach Exposure after transclival approach with extradural anterior petrosectomy Neural structures  Peritrigeminal zone 0 3  Facial nerve 1 3  Trigeminal nerve 0 3  Abducens nerve 3 3 Arteries  BA 3 3  Anterior inferior cerebellar artery (anterior pontine segment) 3 3  Anterior inferior cerebellar artery (lateral pontine segment) 1 3 Exposure after transclival approach Exposure after transclival approach with extradural anterior petrosectomy Neural structures  Peritrigeminal zone 0 3  Facial nerve 1 3  Trigeminal nerve 0 3  Abducens nerve 3 3 Arteries  BA 3 3  Anterior inferior cerebellar artery (anterior pontine segment) 3 3  Anterior inferior cerebellar artery (lateral pontine segment) 1 3 a Scoring system is as in Table 2. View Large The lower level is limited by the hypoglossal nerve (XII) entering its canal cranially and the superior margin of C1 caudally (Figure 4). The anterolateral sulcus was exposed in 60% of specimens moving the endoscope laterally and inferiorly to the vertebral artery (VA) and the rootlets of the glossopharyngeal nerve. The variability of the course of the VA lying on the anterolateral sulcus hindered the surgical exposure of this entry zone in 40% of specimens (Table 4). FIGURE 4. View largeDownload slide Endoscopic view of the lower working area. The exposure of the anterolateral sulcus is limited by the vertebral artery. BA, basilar artery; VA, vertebral artery; IX, glossopharyngeal nerve; XII, hypoglossal nerve. FIGURE 4. View largeDownload slide Endoscopic view of the lower working area. The exposure of the anterolateral sulcus is limited by the vertebral artery. BA, basilar artery; VA, vertebral artery; IX, glossopharyngeal nerve; XII, hypoglossal nerve. TABLE 4. Exposure of Anatomic Structures at the Medulla Lower Level With Transclival Approacha Exposure Neural structures  Anterolateral sulcus 2  Glossopharyngeal nerve 2  Vagus nerve 2  Accessory rootlets 2  Hypoglossal nerve 3  C1 rootlets 3 Vascular structures  VA 3  Anterior spinal artery 3  Posterior inferior cerebellar artery 2 Exposure Neural structures  Anterolateral sulcus 2  Glossopharyngeal nerve 2  Vagus nerve 2  Accessory rootlets 2  Hypoglossal nerve 3  C1 rootlets 3 Vascular structures  VA 3  Anterior spinal artery 3  Posterior inferior cerebellar artery 2 a Scoring system is as in Table 2. View Large TABLE 4. Exposure of Anatomic Structures at the Medulla Lower Level With Transclival Approacha Exposure Neural structures  Anterolateral sulcus 2  Glossopharyngeal nerve 2  Vagus nerve 2  Accessory rootlets 2  Hypoglossal nerve 3  C1 rootlets 3 Vascular structures  VA 3  Anterior spinal artery 3  Posterior inferior cerebellar artery 2 Exposure Neural structures  Anterolateral sulcus 2  Glossopharyngeal nerve 2  Vagus nerve 2  Accessory rootlets 2  Hypoglossal nerve 3  C1 rootlets 3 Vascular structures  VA 3  Anterior spinal artery 3  Posterior inferior cerebellar artery 2 a Scoring system is as in Table 2. View Large Fiber Dissection Guided with 7T-MRI Neuronavigation The perioculomotor zone is located between the emergence of III and the medial one-third of the cerebral peduncle (Figure 5A). Removing the basis of the cerebral peduncle laterally to the emergence of the oculomotor nerve uncovers the substantia nigra. At this point, the red nucleus (RN) was identified and correlated with the 7T-MRI (Figures 5B-5E). The distance between the RN and the surface of cerebral peduncle at the level of frontopontine tract averaged 7.8 mm. The dissection should not fully expose the RN because of the risk of damaging the fibers of III curving around its medial aspect. The medial lemniscus (ML) courses posteriorly and laterally to the RN (Figure 5D). FIGURE 5. View largeDownload slide Perioculomotor zone. A, This entry zone (orange area) is located between the exit point of the oculomotor nerve medially and the corticospinal tract laterally. B to E, Neuronavigation in axial B, sagittal C, and coronal plane D, and fiber dissection of perioculomotor zone E. E, The pointer is located on the anterior wall of the RN just above the course of the intramesencephalic segment of the oculomotor nerve. CST, corticospinal tract; FPT, frontopontine tract; MB, mammillary body; ML, medial lemniscus; OPTPT, occipito-parieto-temporo-pontine tract; RN, red nucleus; III, oculomotor nerve; V, trigeminal nerve. FIGURE 5. View largeDownload slide Perioculomotor zone. A, This entry zone (orange area) is located between the exit point of the oculomotor nerve medially and the corticospinal tract laterally. B to E, Neuronavigation in axial B, sagittal C, and coronal plane D, and fiber dissection of perioculomotor zone E. E, The pointer is located on the anterior wall of the RN just above the course of the intramesencephalic segment of the oculomotor nerve. CST, corticospinal tract; FPT, frontopontine tract; MB, mammillary body; ML, medial lemniscus; OPTPT, occipito-parieto-temporo-pontine tract; RN, red nucleus; III, oculomotor nerve; V, trigeminal nerve. The peritrigeminal zone is located between the emergences of V and VII nerves (Figure 6A) and averaged 8.9 mm. Progressive removal of superficial transverse pontine fibers discloses the pontine nuclei and the deep transverse fibers. The CST is broken up into discrete bundles separated by the transverse fibers and is located medially to the peritrigeminal zone (Figures 6B-6E). The peritrigeminal zone is limited laterally by the intrapontine fibers of V, dorsally by the trigeminal motor nucleus and the trigeminal spinal tract, and inferiorly by the intrapontine fibers of VII (Figure 6E). The average distance between the emergence of V and its motor nucleus was 13.7 mm. Extending the dissection medially, there is the risk of damaging the CST that is located 6 mm medial to the intrapontine segment of the V. Enlarging the dissection behind the deep transverse fibers there is the risk to injury the ML, the spinothalamic tract, and the lateral lemniscus, which on MRI form paired “crescents” that arc dorsally (Figure 6C and 6E). FIGURE 6. View largeDownload slide Peritrigeminal zone. A, This entry zone (orange area) is located between the origin of trigeminal and facial nerves. B to D, Fiber-dissection of the peritrigeminal zone and neurovavigation in axial B, sagittal C, and coronal planes D. The peritrigeminal zone is bounded medially by the corticospinal tract, laterally by the intrapontine fibers of the trigeminal nerve, dorsally by the trigeminal motor nucleus and the trigeminal spinal tract, and inferiorly by the intrapontine fibers of the facial nerve. E, The pointer is located on the trigeminal motor nucleus. CST, corticospinal tract; CTT, central tegmental tract; LL, lateral lemniscus; MCP, middle cerebellar peduncle; ML, medial lemniscus; O, olive; SCP, superior cerebellar peduncle; TST, trigeminal spinal tract; III, oculomotor nerve; V, trigeminal nerve, VI, abducens nerve; VII, facial nerve; VIII, vestibulocochlear nerve; IX, glossopharyngeal nerve; X, vagal nerve; XII, hypoglossal nerve. FIGURE 6. View largeDownload slide Peritrigeminal zone. A, This entry zone (orange area) is located between the origin of trigeminal and facial nerves. B to D, Fiber-dissection of the peritrigeminal zone and neurovavigation in axial B, sagittal C, and coronal planes D. The peritrigeminal zone is bounded medially by the corticospinal tract, laterally by the intrapontine fibers of the trigeminal nerve, dorsally by the trigeminal motor nucleus and the trigeminal spinal tract, and inferiorly by the intrapontine fibers of the facial nerve. E, The pointer is located on the trigeminal motor nucleus. CST, corticospinal tract; CTT, central tegmental tract; LL, lateral lemniscus; MCP, middle cerebellar peduncle; ML, medial lemniscus; O, olive; SCP, superior cerebellar peduncle; TST, trigeminal spinal tract; III, oculomotor nerve; V, trigeminal nerve, VI, abducens nerve; VII, facial nerve; VIII, vestibulocochlear nerve; IX, glossopharyngeal nerve; X, vagal nerve; XII, hypoglossal nerve. The anterolateral sulcus is located in the ventral surface of the medulla along the anterolateral preolivary sulcus inferior to the roots of XII (Figure 7A). The caudal limit is represented by the rostral C1 rootlets. The MRI clearly depicted the gray-folded lamina of the inferior olivary nucleus indicating the upper limit of the dissection (Figures 7B-7D). The CST in the medulla is located anteromedially to the inferior olivary nucleus and defines the medial border of the entry zone (Figure 7E). FIGURE 7. View largeDownload slide Anterolateral sulcus. A, This entry zone (orange area) is located between the inferior roots of the hypoglossal nerve and the superior C1 rootlets. B to D, Fiber-dissection of the anterolateral sulcus and neuronavigation in axial (B), sagittal (C), and coronal plane (D). E, The pointer is located in the anterolateral sulcus just below the apparent origin of the hypoglossal nerve. CST, costicospinal tract; ML, medial lemniscus; V, trigeminal nerve; VI, abducens nerve; VII, facial nerve; VIII, vestibulocochlear nerve nerve; IX glossopharyngeal nerve; X, vagal nerve; XII, hypoglossal nerve. FIGURE 7. View largeDownload slide Anterolateral sulcus. A, This entry zone (orange area) is located between the inferior roots of the hypoglossal nerve and the superior C1 rootlets. B to D, Fiber-dissection of the anterolateral sulcus and neuronavigation in axial (B), sagittal (C), and coronal plane (D). E, The pointer is located in the anterolateral sulcus just below the apparent origin of the hypoglossal nerve. CST, costicospinal tract; ML, medial lemniscus; V, trigeminal nerve; VI, abducens nerve; VII, facial nerve; VIII, vestibulocochlear nerve nerve; IX glossopharyngeal nerve; X, vagal nerve; XII, hypoglossal nerve. DISCUSSION EETA for Brainstem Lesions In brainstem cavernomas, EETA provides some advantages over standard microsurgical approaches, including a direct midline surgical corridor to the lesion avoiding cerebral retraction.30–36 The entry zones described in the literature for microsurgical resection of ventral intrinsic lesions of the brainstem include the perioculomotor zone and the lateral mesencephalic sulcus in the midbrain, the peritrigeminal zone in the pons, and the anterolateral and postolivary sulci in the medulla.1–7 In this study, we investigated the extent of endoscopic transclival exposure of safe entry zones for the 3 surgical working areas described. The EETA allowed exposure of the perioculomotor zone at the midbrain level, the peritrigeminal zone at the pons level, and the anterolateral sulcus at the medulla level. The endoscopic transclival exposure of the ventral surface of midbrain at the upper level requires mobilization of the pituitary gland and offers a wide view of the interpeduncular cistern. The perioculomotor zone was visible in 60% of specimens, whereas the parasellar segment of the ICA limited the exposure of the lateral mesencephalic sulcus. Pituitary transposition is the key step when the exposure of interpeduncular cistern is planned through an EETA. Kassam et al29 described the intradural transposition of the pituitary gland to access tumors extending to the interpeduncular fossa.29 However, this surgical maneuver is associated with a nonnegligible risk of producing pituitary dysfunction.29 Extradural pituitary transposition,37 which consists of mobilization of the gland covered by both layers of dura (meningeal and periosteal), and interdural transposition,38 which involves mobilization of the gland covered by the medial wall of the cavernous sinus, minimize the risk of pituitary dysfunction and provide access to selected extradural lesions and tumors with parasellar–retrosellar–suprasellar extensions, respectively. Recently, He et al32 treated a symptomatic ventral midbrain cavernoma via EETA using pituitary transposition. Our study showed that the endoscopic transclival exposure of the ventral pons allows unobstructed view of BA, of anterior pontine segment of AICA, and of the cisternal portion of VI. Moreover, the emergences of V and VII were barely visible. The exposure of the peritrigeminal zone was obtained with an extradural anterior petrosectomy that required removal of the additional bone surrounding the inferomedial surface of the horizontal segment of the petrous ICA.19,22,39 EETA to ventral pontine cavernomas has been described in 5 case reports from different groups30,31,33,34,36: gross-total resection was achieved in 4 cases and subtotal resection in 1 case. Clinical improvement was described in 4 cases and no postoperative deficits occurred in the remaining case. In our study, EETA of the lower level allowed exposure of the ventral surface of the medulla cranially to the anterior arch of C1 and medially to the inferior olives. The anterolateral sulcus was generally visible, although its exposure can be obstructed by the variable course of the VA. A lower extension of the approach with removal of anterior arch of C1 can be performed when the exposure of ventral cervicomedullary junction is required.40 Recently, Nayak et al35 reported 1 case of anterior medullary cavernoma resected through an EETA and C1 removal. Although the clinical results of brainstem cavernomas resected via EETA seem to be promising; the risk of postoperative CSF-leak remains a concern. In fact, of the 5 pontine cavernomas reported, 2 presented postoperative CSF-leak and required surgical revision.33,36 Furthermore, the bleeding generally observed when the prepontine dura is incised can increase the complexity of the approach. Brainstem Fiber Dissection Combined With Ultra-High-Field MRI The anatomy of the ventral safe entry zones exposed using EETA was investigated using fiber-dissection technique and correlated with 7T-MRI of the same specimen. Ultra-high-resolution MRI allows improved visualization of tiny anatomic structures of brainstem and offers unique opportunity for a detailed study of safe entry zones.28,41 The perioculomotor zone was originally described as a surgical corridor located lateral to the emergence of the III and medial to the CST.2,7 Neurotomy in this area should be performed in a rostrocaudal direction parallel to the frontopontine fibers running through the medial one-fifth of the cerebral peduncle. This surgical corridor is minute and care must be taken to avoid injury of the intramesencepahalic segment of III medially, of the CST laterally, and of the RN that is located approximately 8 mm from the pial surface. The peritrigeminal zone is actually considered the safest entry zone for the pontine lesions.1,42 Some authors favor a transverse neurotomy respecting the course of the pontocerebellar fibers to minimize the damage.6,27 When a transverse incision is performed, care should be taken to avoid damage to the CST located approximately 6 mm medially to the intrapontine segment of the V. The neurotomy should remain medially to the emergences of V and VII to preserve their intrapontine segments and their nuclei. The approach through the anterolateral sulcus, proposed for lesions of the anterolateral medulla, requires a vertical incision between the inferior roots of the XII and the superior C1 rootlets.3 The resultant surgical corridor is extremely narrow and carries high risk of damaging the CST. Accordingly, lesions at this level should be resected only when come to the surface and provide a direct corridor of attack. Although the combination of fiber-dissection with MRI information using a neuronavigation system has been previously reported for the analysis of the central-core of the cerebrum28; to the best of our knowledge, this is the first work describing this multimethodological validation in the study of brainstem anatomy. The ultra-high-field MRI resulted extremely effective in localization of fiber tracts and nuclei adjacent to the safe entry zones studied. Limitations Because our investigation is based on findings from normal cadaveric specimens, the conclusions are not strictly applicable to clinical cases in which the anatomic structures can be displaced by the pathology. In addition, although we investigated the extent of exposure of different working areas, we did not analyze the degree to which the different anatomic areas are suitable for surgical maneuvers. Finally, Klinger's technique produces some degree of tissue dehydration reducing the accuracy of our morphometric data. CONCLUSION EETA allows the exposure of selected safe entry zones of the ventral brainstem. The perioculomotor zone, exposed at midbrain level, requires mobilization of the pituitary gland and can be hindered by the SCA. The peritrigeminal zone is exposed at pontine level after extradural removal of anterior petrous bone. The anterolateral sulcus is exposed at medullary level although the course of VA can complicate its access. The combination of high-definition anatomic information provided by ultra-high-field MRI and fiber-dissection of the same specimen resulted useful in understanding the internal architecture of the brainstem. Disclosures This work has been partly supported by the grant “Marató TV3 Project” [411/U/2011—title: Quantitative analysis and computer aided simulation of minimally invasive approaches for intracranial vascular lesions]. The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article. 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Extended endoscopic endonasal transphenoidal approach to the suprasellar reagion, planum sphenoidale and clivus. In: Cappabianca P , de Divitis E , eds. Endoscopic Endonasal Transsphenoidal Surgery . New York : Springer-Verlag ; 2003 ; 176 – 187 . 16. Cavallo LM , Messina A , Cappabianca P et al. Endoscopic endonasal surgery of the midline skull base: anatomical study and clinical consideration . Neurosurg Focus . 2005 ; 19 ( 1 ): 1 – 14 . 17. de Notaris M , Cavallo LM , Prats-Galino A et al. Endoscopic endonasal transclival approach and retrosigmoid approach to the clival and petroclival regions . Neurosurgery . 2009 ; 65 ( 6 suppl ): 42 – 52 ; discussion 50-52 . 18. Jho HD , Ha HG . Endoscopic endonasal skull base surgery: part 3 - the clivus and posterior fossa . Minim Invasive Neurosurg . 2004 ; 47 ( 1 ): 16 – 23 . 19. Kassam AB , Gardner P , Snyderman C , Mintz A , Carrau R . 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Three-dimensional microsurgical anatomy of cerebellar peduncles . Neurosurg Rev . 2013 ; 36 ( 2 ): 215 – 225 ; discussion 224-225 . 28. Alarcon C , de Notaris M , Palma K et al. Anatomic study of the central core of the cerebrum correlating 7-T magnetic resonance imaging and fiber dissection with the aid of a neuronavigation system . Neurosurgery . 2014 ; 10 ( suppl 2) : 294 – 304 ; discussion 304 . 29. Kassam AB , Prevedello DM , Thomas A et al. Endoscopic endonasal pituitary transposition for a transdorsum sellae approach to the interpeduncular cistern . Neurosurgery . 2008 ; 62 ( 3 suppl 1 ): 57 – 72 ; discussion 72-74 . 30. Dallan I , Battaglia P , De Notaris M , Caniglia M , Turri-Zanoni M . Endoscopic endonasal transclival approach to a pontine cavernous malformation: case report . Int J Pediatr Otorhinolaryngol . 2015 ; 79 ( 9 ): 1584 – 1588 . 31. Gomez Amador JL , Ortega Porcayo LA , Palacios Ortiz IJ , Perdomo Pantoja A , Nares Lopez FE , Vega Alarcon A . Endoscopic endonasal transclival resection of a ventral pontine cavernous malformation: technical case report . J Neurosurg . 2017 ; 127 ( 3 ): 553 – 558 . 32. He SM , Wang Y , Zhao TZ et al. Endoscopic endonasal approach to mesencephalic cavernous malformation . World Neurosurg . 2016 ; 90 : 701.e7 – 701.e10 . 33. Kimbal MM , Lewis SB , Werning JW , Mocco JD . Resection of a pontine cavernous malformation via an endoscopic endonasal approach: a case report . Neurosurgery . 2012 ; 71 ( 1 Suppl Operative ): 186 – 193 ; discussion 193-194 . 34. Linsler S , Oertel J . Endoscopic endonasal transclival resection of a brainstem cavernoma: a detailed account of our technique and comparison with the literature . World Neurosurg . 2015 ; 84 ( 6 ): 2064 – 2071 . 35. Nayak NR , Thawani JP , Sanborn MR , Storm PB , Lee JY . Endoscopic approaches to brainstem cavernous malformations: case series and review of the literature . Surg Neurol Int . 2015 ; 24 : 6 – 68 . 36. Sanborn MR , Kramarz MJ , Storm PB , Adappa ND , Palmer JN , Lee JY . Endoscopic, endonasal, transclival resection of a pontine cavernoma: case report . Neurosurgery . 2012 ; 71 ( 1 Suppl Operative ): 198 – 203 . 37. Silva D , Attia M , Kandasamy J , Alimi M , Anand VK , Schwartz TH . Endoscopic endonasal posterior clinoidectomy . Surg Neurol Int . 2012 ; 3 ( 1) : 1 – 35 (Epub) . 38. Fernandez-Miranda JC , Gardner PA , Rastelli MM Jr et al. Endoscopic endonasal transcavernous posterior clinoidectomy with interdural pituitary transposition . J Neurosurg . 2014 ; 121 ( 1 ): 91 – 99 . 39. Zanation AM , Snyderman CH , Carrau RL , Gardner PA , Prevedello DM , Kassam AB . Endoscopic endonasal surgery for petrous apex lesions . Laryngoscope . 2009 ; 119 ( 1 ): 19 – 25 . 40. Kassam AB , Snyderman C , Gardner P , Carrau R , Spiro R . The expanded endonasal approach: a fully endoscopic transnasal approach and resection of the odontoid process: technical case report . Neurosurgery . 2005 ; 57 ( ONS Suppl 1 ): ONS213 – ONS214 . 41. Duyn JH . The future of ultra-high field MRI and fMRI for study of the human brain . Neuroimage . 2012 ; 15 ; 62 ( 2 ): 1241 – 1248 42. Baghai P , Vries JK , Bechtel PC . Retromastoid approach for biopsy of brain stem tumors . Neurosurgery . 1982 ; 10 ( 5 ): 574 – 579 . COMMENTS The authors performed a detailed and richly illustrated anatomical study of the safe entry zones to the ventral brainstem provided via the endoscopic endonasal transclival approach. The anterior aspect of the brainstem is notoriously difficult to reach and expose adequately using complex transcranial skull base approaches due to the significant brain retraction required. The endonasal transclival trajectory provides a direct working angle to the ventral brainstem and represents a valid option for most of ventral brainstem locations except, in our opinion, for lesions of the peritrigeminal area which can be accessed using a less invasive presigmoid retrolabyrinthine approach. However, some lesions do not reach the surface of the brainstem and thus small neurotomies are required. Regardless of the approach, a comprehensive understanding of the brainstem's internal architecture is essential for any neurosurgeon working within this critical region. Surface points and surgical corridors that are less dense in eloquent neurovascular structures can be considered as safe entry zones and knowledge of these optimal entry zones along with knowledge of the anatomy of the most critical structures is key for minimizing surgery related morbidity and mortality. In this comprehensive anatomical study, the authors not only investigated endoscopic endonasal transclival access to the ventral brainstem but provided a good explanation of the anatomy in a methodologically novel and thorough manner that sets a high bar for anatomosurgical studies. Antonio Bernardo Alexander I. Evins New York, New York This paper presents the careful white fiber dissection and 7T MRI anatomic correlation of ventral corridors into the brainstem via and endoscopic endonasal approach (EEA). The study is meticulously done and demonstrates remarkable anatomic knowledge as well as feasibility of endonasal entry points into the brainstem. However, it is critical to recognize this as a purely anatomic study; access is based and graded on ‘exposure’ of structures such as sulci or cranial nerves. The EEA was developed as a midline corridor for access to medial, ventral skull base pathologies. Merely exposing or visualizing these structures does not equate with ability to surgically access or safely dissect them via EEA. Indeed, the white matter dissections performed in this paper were done via traditional approaches (eg, anterior petrosectomy) using ‘open’ microsurgical technique; this is demonstrated in several figures, as pointers are introduced via a non-EEA trajectory which can be confusing (Figure 6). Future studies would be useful to include endonasal dissection of the proposed entry points as well as MRI based hi definition fiber tracking to demonstrate access points. Paul A. Gardner Pittsburgh, Pennsylvania The authors present a series of 8 cadaveric endoscopic endonasal transclival dissections of whole heads, and describe 8 white matter dissections of explanted cadaveric brainstems guided by surgical navigation using 7T MRIs of these brain stem specimens. The endoscopic dissections are excellent and provide good detail of the anatomy identified through such approaches. The technique of white matter dissection of the brain stem using surgical navigation with 7T MRIs is performed beautifully, and appears to be a powerful technique for study of white matter anatomy. One challenge with regard to this work is that the true clinical relevance of this work is uncertain as it is based solely on cadaveric dissections and 7T MRIs without definite applicability to “real life surgery”. Nonetheless, it is an excellent investigation of this anatomy and these surgical approaches as we moved to advance these techniques. Michael Chicoine St. Louis, Missouri Copyright © 2018 by the Congress of Neurological Surgeons This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Operative Neurosurgery Oxford University Press

Endoscopic Endonasal Transclival Approach to the Ventral Brainstem: Anatomic Study of the Safe Entry Zones Combining Fiber Dissection Technique with 7 Tesla Magnetic Resonance Guided Neuronavigation

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Congress of Neurological Surgeons
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Copyright © 2018 by the Congress of Neurological Surgeons
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2332-4252
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10.1093/ons/opy080
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Abstract

Abstract BACKGROUND Treatment of intrinsic lesions of the ventral brainstem is a surgical challenge that requires complex skull base antero- and posterolateral approaches. More recently, endoscopic endonasal transclival approach (EETA) has been reported in the treatment of selected ventral brainstem lesions. OBJECTIVE In this study we explored the endoscopic ventral brainstem anatomy with the aim to describe the degree of exposure of the ventral safe entry zones. In addition, we used a newly developed method combining traditional white matter dissection with high-resolution 7T magnetic resonance imaging (MRI) of the same specimen coregistered using a neuronavigation system. METHODS Eight fresh-frozen latex-injected cadaver heads underwent EETA. Additional 8 formalin-fixed brainstems were dissected using Klingler technique guided by ultra-high resolution MRI. RESULTS The EETA allows a wide exposure of different safe entry zones located on the ventral brainstem: the exposure of perioculomotor zone requires pituitary transposition and can be hindered by superior cerebellar artery. The peritrigeminal zone was barely visible and its exposure required an extradural anterior petrosectomy. The anterolateral sulcus of the medulla was visible in most of specimens, although its close relationship with the corticospinal tract makes it suboptimal as an entry point for intrinsic lesions. In all cases, the use of 7T-MRI allowed the identification of tiny fiber bundles, improving the quality of the dissection. CONCLUSIONS Exposure of the ventral brainstem with EETA requires mastering surgical maneuvers, including pituitary transposition and extradural petrosectomy. The correlation of fiber dissection with 7T-MRI neuronavigation significantly improves the understanding of the brainstem anatomy. Brainstem, Endoscopy, Skull base, Endoscopic endonasal, Cavernoma, 7 Tesla magnetic resonance, Klingler, Fiber dissection ABBREVIATIONS ABBREVIATIONS AICA anteroinferior cerebellar artery BA basilar artery CST corticospinal tract EETA endoscopic endonasal transclival approach FOV field-of-view ICA internal carotid artery ML medial lemniscus MRI magnetic resonance imaging PCA posterior cerebral artery RN red nucleus SCA superior cerebellar artery VA vertebral artery The majority of brainstem cavernomas are operated on through the regions of the brainstem where they reach the surface. However, when lesions do not emerge from the pia, surgical strategies require small neurotomies in safe entry zones on the brainstem surface where critical neural structures are sparse and few perforating arteries are present.1–7 Several transcranial approaches have been described to access intrinsic lesions of the ventral brainstem; nevertheless, these approaches require extensive drilling of bone, manipulation of neurovascular structures, and do not provide a direct working angle to the ventral brainstem.8–14 During the past decade, skull-base surgery has been enriched by the introduction of endoscopic endonasal approaches to access lesions located in the ventral skull-base.15–20 More recently, anatomic and clinical studies concerning the endoscopic endonasal transclival approach (EETA) documented the possibility of obtaining a wide exposure of the brainstem ventral surface.21–24 In the present study, we explored the anterolateral surface of brainstem via EETA to evaluate the degree of exposure of the safe entry zones. In addition, the identified safe entry zones were further investigated combining white matter dissection with ultra-high-field magnetic resonance imaging (MRI) in formalin-fixed brainstems coregistered using a neuronavigation system. METHODS The study was approved by the ethical committee of the Faculty of Medicine of our University. The specimens were obtained in the first 12-h postmortem from donors without clinical history of neurological disease. Endoscopic Endonasal Transclival Approach Endoscopic dissections were performed on 8 fresh-frozen latex-injected cadaver heads using a rigid endoscope 4 mm in diameter, 18 cm in length, with 0° optics (Karl-Storz, Tuttlingen, Germany) connected to a light source through and a camera. EETA was performed following the steps as described in the literature.15,16,18,19,21 The nasal steps of dissections included monolateral right middle turbinectomy, lateralization of the contralateral middle turbinate, posterior septectomy, anterior sphenoidotomy, and antrostomy of the maxillary sinus. After opening of the sella, the tuberculum sellae, the dorsum sellae, and the posterior clinoids were removed exposing the retrosellar area. The vomer and the sphenoidal floor were removed. The pterygoid canals were identified about 4 mm lateral to the vomer–sphenoid junction.17 The bone of the clivus was progressively removed down to the anterior arch of C1. The caudal lateral boundaries of the bone removal were represented by the anterior third of the occipital condyles. In all specimens an extradural anterior petrosectomy was performed to evaluate the effect of lateral extending of bone removal on exposure of peritrigeminal zone.22 At this point, the dura was opened along the midline. The resulting intradural working area is a rectangular space delimited superiorly by the indentation of tuberculum sellae, caudally by the anterior arch of C1, and laterally by the parasellar and paraclival segments of the internal carotid artery (ICA). As previously described, the operative field obtained with EETA can be divided into 3 surgical working areas, namely upper, middle, and lower levels (Figure 1).17 The grade of exposure of selected safe entry zones for each working area was evaluated. The safe entry zones explored were as follows: the lateral mesencephalic sulcus and the perioculomotor zone at the upper level, the peritrigeminal zone at the middle level, and the anterolateral sulcus at the lower level. The extent of exposure for each working area was evaluated by using a numerical grading system as described by Kawashima et al.25 A value of 0 refers to a structure that is not exposed at all, a value of 1 indicates that the structure is exposed in less than 50% of specimens, a value of 2 indicates an exposure comprised between 50% and 99% of specimens, and a value of 3 indicates full exposure in 100% of specimens. FIGURE 1. View largeDownload slide Identification of the surgical working areas via the EETA. The upper level is limited by the posterior clinoid processes superiorly and by the abducens nerves entering the dural porus inferiorly (red-dotted line). The middle level is limited upwardly by a line joining the abducens nerves and downwardly by a line joining the intracranial openings of the hypoglossal canal (pale blue-dotted line). The lower level is bounded superiorly by the middle level and inferiorly by the superior margin of C1 (green-dotted line). AICA, anteroinferior cerebellar artery; BA, basilar artery; ICAc, clival segment of the internal carotid artery; ICAs, sellar segment of the internal carotid artery; ON, optic nerve; pg, pituitary gland; VA, vertebral artery; VI, abducens nerve; XII, hypoglossal nerve. FIGURE 1. View largeDownload slide Identification of the surgical working areas via the EETA. The upper level is limited by the posterior clinoid processes superiorly and by the abducens nerves entering the dural porus inferiorly (red-dotted line). The middle level is limited upwardly by a line joining the abducens nerves and downwardly by a line joining the intracranial openings of the hypoglossal canal (pale blue-dotted line). The lower level is bounded superiorly by the middle level and inferiorly by the superior margin of C1 (green-dotted line). AICA, anteroinferior cerebellar artery; BA, basilar artery; ICAc, clival segment of the internal carotid artery; ICAs, sellar segment of the internal carotid artery; ON, optic nerve; pg, pituitary gland; VA, vertebral artery; VI, abducens nerve; XII, hypoglossal nerve. Fiber Dissection and Neuronavigation Eight formalin-fixed brainstems were prepared using the method originally described by Klinger26,27 in order to dissect the safe entry zones identified through EETA. Vitamin-E fiducials were placed on the lateral aspects of the brainstem avoiding the regions previously selected for fiber dissection.28 MRI sections were performed on a 7.0-T BioSpec70/30 horizontal scanner (Bruker-BioSpin, Ettlingen, Germany), equipped with a circular polarized transmit/receive coil for rabbit-body-imaging with a 15.4 cm inner diameter actively shielded gradient system (400 mT/m). Specimens were placed horizontally inside a hermetically sealed plastic tube with the following dimensions: diameter: 35 mm, length: 125 mm. Tripilot scans were performed for positioning the specimens inside the magnet. T1-weighetd anatomic images were acquired using the Fast-Low-Angle-Shot sequence (parameters: repetition time = 4390.09 ms, echo time = 8.46 ms, field-of-view (FOV) = 130 mm × 80 mm, matrix size = 394 pixels × 242 pixels, with a resulting in-plane resolution of 0.33 mm × 0.33 mm in 1-mm slice thickness). The acquisition of this set of images was repeated three times acquiring the highest in-plane resolution for each orientation (axial, coronal, and sagittal) maintaining the same FOV. The MRI was subsequently loaded in a Medtronic-AxiEM electromagnetic-neuronavigation system (Medtronic, Minneapolis, Minnesota), and the brainstems were registered using the fiducials previously located on the lateral aspects. The dissections were performed in a stepwise manner under microscopic magnification with wooden spatulas and microsurgical instruments. After exposure of fiber tracts and their nuclei, several measurements were taken with an electronic digital caliper (±0.01 mm; Table 1). TABLE 1. Measurements From 8 Brainstems Bilaterally (n = 16) Midbrain Mean (range), SD, mm mm Width of interpeduncular fossa 5.1 (3.2-7.5) 1.4 Substantia nigra to frontopontine tract 3.2 (1-7.3) 1.83 ML to frontopontine tract 13.1 (10.8-16.5) 1.79 RN to frontopontine tract 7.8 (5.2-12.1) 1.55 Substantia nigra to oculomotor nerve exit point 1.4 (1.1-1.8) 0.36 Pons  Trigeminal nerve exit point to facial nerve exit point 8.9 (6.8-9.6) 1.30  Trigeminal nerve exit point to trigeminal motor nucleus 13.7 (10.9-16.3) 1.89  Trigeminal motor nucleus to facial nerve exit point 10 (6.6-13.7) 3.53  Facial nerve exit point to CST 6.9 (4.4-7.8) 1.12  Acoustic nerve exit point to CST 9.5 (7.5-12) 1.37  Trigeminal nerve intrapontine segment to CST 6.1 (4-8.2) 1.134  Trigeminal motor nucleus to CST 7 (4.7-9.8) 1.68 Medulla  Anterior median fissure width 0.7 (0.2-1.3) 0.33  Pyramidal width 11 (9.3-11.9) 0.76  Olivary nucleus rostrocaudal length 13.5 (9.9-16.2) 1.6  Olivary nucleus anteroposterior length 4.2 (2.9-5.6) 0.7  Olivary nucleus to trigeminal spinal tract 1.4 (0.7-2.6) 0.6  Pontomedullary sulcus to pyramidal decussation 27.1 (24.9-29.2) 1.9 Midbrain Mean (range), SD, mm mm Width of interpeduncular fossa 5.1 (3.2-7.5) 1.4 Substantia nigra to frontopontine tract 3.2 (1-7.3) 1.83 ML to frontopontine tract 13.1 (10.8-16.5) 1.79 RN to frontopontine tract 7.8 (5.2-12.1) 1.55 Substantia nigra to oculomotor nerve exit point 1.4 (1.1-1.8) 0.36 Pons  Trigeminal nerve exit point to facial nerve exit point 8.9 (6.8-9.6) 1.30  Trigeminal nerve exit point to trigeminal motor nucleus 13.7 (10.9-16.3) 1.89  Trigeminal motor nucleus to facial nerve exit point 10 (6.6-13.7) 3.53  Facial nerve exit point to CST 6.9 (4.4-7.8) 1.12  Acoustic nerve exit point to CST 9.5 (7.5-12) 1.37  Trigeminal nerve intrapontine segment to CST 6.1 (4-8.2) 1.134  Trigeminal motor nucleus to CST 7 (4.7-9.8) 1.68 Medulla  Anterior median fissure width 0.7 (0.2-1.3) 0.33  Pyramidal width 11 (9.3-11.9) 0.76  Olivary nucleus rostrocaudal length 13.5 (9.9-16.2) 1.6  Olivary nucleus anteroposterior length 4.2 (2.9-5.6) 0.7  Olivary nucleus to trigeminal spinal tract 1.4 (0.7-2.6) 0.6  Pontomedullary sulcus to pyramidal decussation 27.1 (24.9-29.2) 1.9 View Large TABLE 1. Measurements From 8 Brainstems Bilaterally (n = 16) Midbrain Mean (range), SD, mm mm Width of interpeduncular fossa 5.1 (3.2-7.5) 1.4 Substantia nigra to frontopontine tract 3.2 (1-7.3) 1.83 ML to frontopontine tract 13.1 (10.8-16.5) 1.79 RN to frontopontine tract 7.8 (5.2-12.1) 1.55 Substantia nigra to oculomotor nerve exit point 1.4 (1.1-1.8) 0.36 Pons  Trigeminal nerve exit point to facial nerve exit point 8.9 (6.8-9.6) 1.30  Trigeminal nerve exit point to trigeminal motor nucleus 13.7 (10.9-16.3) 1.89  Trigeminal motor nucleus to facial nerve exit point 10 (6.6-13.7) 3.53  Facial nerve exit point to CST 6.9 (4.4-7.8) 1.12  Acoustic nerve exit point to CST 9.5 (7.5-12) 1.37  Trigeminal nerve intrapontine segment to CST 6.1 (4-8.2) 1.134  Trigeminal motor nucleus to CST 7 (4.7-9.8) 1.68 Medulla  Anterior median fissure width 0.7 (0.2-1.3) 0.33  Pyramidal width 11 (9.3-11.9) 0.76  Olivary nucleus rostrocaudal length 13.5 (9.9-16.2) 1.6  Olivary nucleus anteroposterior length 4.2 (2.9-5.6) 0.7  Olivary nucleus to trigeminal spinal tract 1.4 (0.7-2.6) 0.6  Pontomedullary sulcus to pyramidal decussation 27.1 (24.9-29.2) 1.9 Midbrain Mean (range), SD, mm mm Width of interpeduncular fossa 5.1 (3.2-7.5) 1.4 Substantia nigra to frontopontine tract 3.2 (1-7.3) 1.83 ML to frontopontine tract 13.1 (10.8-16.5) 1.79 RN to frontopontine tract 7.8 (5.2-12.1) 1.55 Substantia nigra to oculomotor nerve exit point 1.4 (1.1-1.8) 0.36 Pons  Trigeminal nerve exit point to facial nerve exit point 8.9 (6.8-9.6) 1.30  Trigeminal nerve exit point to trigeminal motor nucleus 13.7 (10.9-16.3) 1.89  Trigeminal motor nucleus to facial nerve exit point 10 (6.6-13.7) 3.53  Facial nerve exit point to CST 6.9 (4.4-7.8) 1.12  Acoustic nerve exit point to CST 9.5 (7.5-12) 1.37  Trigeminal nerve intrapontine segment to CST 6.1 (4-8.2) 1.134  Trigeminal motor nucleus to CST 7 (4.7-9.8) 1.68 Medulla  Anterior median fissure width 0.7 (0.2-1.3) 0.33  Pyramidal width 11 (9.3-11.9) 0.76  Olivary nucleus rostrocaudal length 13.5 (9.9-16.2) 1.6  Olivary nucleus anteroposterior length 4.2 (2.9-5.6) 0.7  Olivary nucleus to trigeminal spinal tract 1.4 (0.7-2.6) 0.6  Pontomedullary sulcus to pyramidal decussation 27.1 (24.9-29.2) 1.9 View Large RESULTS Endoscopic Dissection The upper level is limited upward by a line joining the 2 posterior clinoid processes and inferiorly by a line joining the abducens nerves (VI) entering the dural porus (Figure 1). Because of the pituitary gland, the exposure of the ventral midbrain is limited (Figure 2A). The transection of the inferior hypophyseal artery and the dissection of ligaments between the pituitary gland and the lateral aspect of the dura allowed the gland to be mobilized cranially (Figure 2B).29 After this maneuver, the basilar-apex, the superior cerebellar artery (SCA), the P1 segment of the posterior cerebral artery (PCA), and the oculomotor nerves (III) were visible (Figure 2C and 2D). The lateral mesencephalic sulcus, which extends from the pontomesencephalic sulcus to the medial geniculate body, was not visible. The perioculomotor zone (Figure 2E), which is located laterally to the emergence of the III on the medial one-third of the cerebral peduncle, was visible in 60% of the specimens. In the remaining cases, the anterior pontomesencephalic segment of SCA with its short perforators obstructed the exposure of the area (Table 2). FIGURE 2. View largeDownload slide Endoscopic view of the upper working area. A, At this level the pituitary gland limits the exposure of the ventral surface of the midbrain. B, After dissection of the soft attachments of the pituitary gland with the lateral sellar dura, the pituitary gland can be mobilized with exposure of the C, basilar apex, superior cerebellar artery, P1 and P2 segments of PCA, and the oculomotor nerves. D, The operative access to the perioculomotor zone passes inferiorly to the superior cerebellar artery and is limited by a perforating branch. E, The perioculomotor zone is exposed (orange area). BA, basilar artery; ICAc, clival segment of the internal carotid artery; ICAs, sellar segment of the internal carotid artery; OCR, opticocarotid recess; ON, optic nerve; pg, pituitary gland; PCA, posterior cerebral artery; SCA, superior cerebellar artery; III, oculomotor nerve; VI, abducens nerve. FIGURE 2. View largeDownload slide Endoscopic view of the upper working area. A, At this level the pituitary gland limits the exposure of the ventral surface of the midbrain. B, After dissection of the soft attachments of the pituitary gland with the lateral sellar dura, the pituitary gland can be mobilized with exposure of the C, basilar apex, superior cerebellar artery, P1 and P2 segments of PCA, and the oculomotor nerves. D, The operative access to the perioculomotor zone passes inferiorly to the superior cerebellar artery and is limited by a perforating branch. E, The perioculomotor zone is exposed (orange area). BA, basilar artery; ICAc, clival segment of the internal carotid artery; ICAs, sellar segment of the internal carotid artery; OCR, opticocarotid recess; ON, optic nerve; pg, pituitary gland; PCA, posterior cerebral artery; SCA, superior cerebellar artery; III, oculomotor nerve; VI, abducens nerve. TABLE 2. Exposure of Anatomic Structures at the Midbrain Upper Level With Transclival Approacha Exposure after transclival approach Neural structures  Anterior mesencephalic zone 2  Lateral mesencephalic sulcus 0  Oculomotor nerve 3  Mammillary body 2 Arteries  BA 3  SCA (anterior pontomesencephalic segment) 3  PCA (P1 segment) 2  Posterior communicating artery 1 Exposure after transclival approach Neural structures  Anterior mesencephalic zone 2  Lateral mesencephalic sulcus 0  Oculomotor nerve 3  Mammillary body 2 Arteries  BA 3  SCA (anterior pontomesencephalic segment) 3  PCA (P1 segment) 2  Posterior communicating artery 1 a The scoring system is as follows: 0, no exposure in any specimen; 1, structure exposed in less than 50% of specimens; 2, structure exposed in more than 50% of specimens; and 3, complete exposure in 100% of specimens. View Large TABLE 2. Exposure of Anatomic Structures at the Midbrain Upper Level With Transclival Approacha Exposure after transclival approach Neural structures  Anterior mesencephalic zone 2  Lateral mesencephalic sulcus 0  Oculomotor nerve 3  Mammillary body 2 Arteries  BA 3  SCA (anterior pontomesencephalic segment) 3  PCA (P1 segment) 2  Posterior communicating artery 1 Exposure after transclival approach Neural structures  Anterior mesencephalic zone 2  Lateral mesencephalic sulcus 0  Oculomotor nerve 3  Mammillary body 2 Arteries  BA 3  SCA (anterior pontomesencephalic segment) 3  PCA (P1 segment) 2  Posterior communicating artery 1 a The scoring system is as follows: 0, no exposure in any specimen; 1, structure exposed in less than 50% of specimens; 2, structure exposed in more than 50% of specimens; and 3, complete exposure in 100% of specimens. View Large The middle level is bounded superiorly by a line joining the abducens nerves and inferiorly by a line joining the intracranial openings of the hypoglossal canal (Figure 3A). At this level the pons and medulla ventral surfaces, the bulbopontine sulcus with the emergence of the VI, the basilar artery (BA), and the anterior segment of anteroinferior cerebellar artery (AICA) were visualized. The petrous apex limits the dissection of the peritrigeminal zone, located between the emergences of trigeminal (V) and facial nerves (VII). This area is located medial to the V and laterally to the corticospinal tract (CST). The exposure of the peritrigeminal zone was obtained in all specimens by an extradural anterior petrosectomy behind the paraclival carotids and then moving the endoscope laterally under the course of the VI (Figure 3B). After the anterior petrosectomy, the lateral pontine segment of the AICA was observed in its course toward the cerebellopontine angle. In 8 sides (50%) the AICA passed through the peritrigeminal zone halfway between the V superiorly and the VII and vestibulocochlear nerves inferiorly. In this scenario, the surgical access requires a careful dissection in order to avoid vascular injury of perforating arteries (Table 3). FIGURE 3. View largeDownload slide Endoscopic view of the middle working area. A, The abducens nerve leaves the brainstem from the bulbopontine sulcus and presents a caudocranial and mediolateral direction toward the Dorello's canal. B, Drilling of the petrous bone is required to fully expose the apparent origin of trigeminal nerve in the pons and the peritrigeminal zone (orange area). AICA, anteroinferior cerebellar artery; BA, basilar artery; VA, vertebral artery; pb, petrous bone; V, trigeminal nerve; VI, abducens nerve; VII, facial nerve; VIII, vestibulocochlear nerve; IX, glossopharyngeal nerve; X, vagal nerve; XII, hypoglossal nerve. FIGURE 3. View largeDownload slide Endoscopic view of the middle working area. A, The abducens nerve leaves the brainstem from the bulbopontine sulcus and presents a caudocranial and mediolateral direction toward the Dorello's canal. B, Drilling of the petrous bone is required to fully expose the apparent origin of trigeminal nerve in the pons and the peritrigeminal zone (orange area). AICA, anteroinferior cerebellar artery; BA, basilar artery; VA, vertebral artery; pb, petrous bone; V, trigeminal nerve; VI, abducens nerve; VII, facial nerve; VIII, vestibulocochlear nerve; IX, glossopharyngeal nerve; X, vagal nerve; XII, hypoglossal nerve. TABLE 3. Exposure of Anatomic Structures at the Pons Middle Level With Transclival Approacha Exposure after transclival approach Exposure after transclival approach with extradural anterior petrosectomy Neural structures  Peritrigeminal zone 0 3  Facial nerve 1 3  Trigeminal nerve 0 3  Abducens nerve 3 3 Arteries  BA 3 3  Anterior inferior cerebellar artery (anterior pontine segment) 3 3  Anterior inferior cerebellar artery (lateral pontine segment) 1 3 Exposure after transclival approach Exposure after transclival approach with extradural anterior petrosectomy Neural structures  Peritrigeminal zone 0 3  Facial nerve 1 3  Trigeminal nerve 0 3  Abducens nerve 3 3 Arteries  BA 3 3  Anterior inferior cerebellar artery (anterior pontine segment) 3 3  Anterior inferior cerebellar artery (lateral pontine segment) 1 3 a Scoring system is as in Table 2. View Large TABLE 3. Exposure of Anatomic Structures at the Pons Middle Level With Transclival Approacha Exposure after transclival approach Exposure after transclival approach with extradural anterior petrosectomy Neural structures  Peritrigeminal zone 0 3  Facial nerve 1 3  Trigeminal nerve 0 3  Abducens nerve 3 3 Arteries  BA 3 3  Anterior inferior cerebellar artery (anterior pontine segment) 3 3  Anterior inferior cerebellar artery (lateral pontine segment) 1 3 Exposure after transclival approach Exposure after transclival approach with extradural anterior petrosectomy Neural structures  Peritrigeminal zone 0 3  Facial nerve 1 3  Trigeminal nerve 0 3  Abducens nerve 3 3 Arteries  BA 3 3  Anterior inferior cerebellar artery (anterior pontine segment) 3 3  Anterior inferior cerebellar artery (lateral pontine segment) 1 3 a Scoring system is as in Table 2. View Large The lower level is limited by the hypoglossal nerve (XII) entering its canal cranially and the superior margin of C1 caudally (Figure 4). The anterolateral sulcus was exposed in 60% of specimens moving the endoscope laterally and inferiorly to the vertebral artery (VA) and the rootlets of the glossopharyngeal nerve. The variability of the course of the VA lying on the anterolateral sulcus hindered the surgical exposure of this entry zone in 40% of specimens (Table 4). FIGURE 4. View largeDownload slide Endoscopic view of the lower working area. The exposure of the anterolateral sulcus is limited by the vertebral artery. BA, basilar artery; VA, vertebral artery; IX, glossopharyngeal nerve; XII, hypoglossal nerve. FIGURE 4. View largeDownload slide Endoscopic view of the lower working area. The exposure of the anterolateral sulcus is limited by the vertebral artery. BA, basilar artery; VA, vertebral artery; IX, glossopharyngeal nerve; XII, hypoglossal nerve. TABLE 4. Exposure of Anatomic Structures at the Medulla Lower Level With Transclival Approacha Exposure Neural structures  Anterolateral sulcus 2  Glossopharyngeal nerve 2  Vagus nerve 2  Accessory rootlets 2  Hypoglossal nerve 3  C1 rootlets 3 Vascular structures  VA 3  Anterior spinal artery 3  Posterior inferior cerebellar artery 2 Exposure Neural structures  Anterolateral sulcus 2  Glossopharyngeal nerve 2  Vagus nerve 2  Accessory rootlets 2  Hypoglossal nerve 3  C1 rootlets 3 Vascular structures  VA 3  Anterior spinal artery 3  Posterior inferior cerebellar artery 2 a Scoring system is as in Table 2. View Large TABLE 4. Exposure of Anatomic Structures at the Medulla Lower Level With Transclival Approacha Exposure Neural structures  Anterolateral sulcus 2  Glossopharyngeal nerve 2  Vagus nerve 2  Accessory rootlets 2  Hypoglossal nerve 3  C1 rootlets 3 Vascular structures  VA 3  Anterior spinal artery 3  Posterior inferior cerebellar artery 2 Exposure Neural structures  Anterolateral sulcus 2  Glossopharyngeal nerve 2  Vagus nerve 2  Accessory rootlets 2  Hypoglossal nerve 3  C1 rootlets 3 Vascular structures  VA 3  Anterior spinal artery 3  Posterior inferior cerebellar artery 2 a Scoring system is as in Table 2. View Large Fiber Dissection Guided with 7T-MRI Neuronavigation The perioculomotor zone is located between the emergence of III and the medial one-third of the cerebral peduncle (Figure 5A). Removing the basis of the cerebral peduncle laterally to the emergence of the oculomotor nerve uncovers the substantia nigra. At this point, the red nucleus (RN) was identified and correlated with the 7T-MRI (Figures 5B-5E). The distance between the RN and the surface of cerebral peduncle at the level of frontopontine tract averaged 7.8 mm. The dissection should not fully expose the RN because of the risk of damaging the fibers of III curving around its medial aspect. The medial lemniscus (ML) courses posteriorly and laterally to the RN (Figure 5D). FIGURE 5. View largeDownload slide Perioculomotor zone. A, This entry zone (orange area) is located between the exit point of the oculomotor nerve medially and the corticospinal tract laterally. B to E, Neuronavigation in axial B, sagittal C, and coronal plane D, and fiber dissection of perioculomotor zone E. E, The pointer is located on the anterior wall of the RN just above the course of the intramesencephalic segment of the oculomotor nerve. CST, corticospinal tract; FPT, frontopontine tract; MB, mammillary body; ML, medial lemniscus; OPTPT, occipito-parieto-temporo-pontine tract; RN, red nucleus; III, oculomotor nerve; V, trigeminal nerve. FIGURE 5. View largeDownload slide Perioculomotor zone. A, This entry zone (orange area) is located between the exit point of the oculomotor nerve medially and the corticospinal tract laterally. B to E, Neuronavigation in axial B, sagittal C, and coronal plane D, and fiber dissection of perioculomotor zone E. E, The pointer is located on the anterior wall of the RN just above the course of the intramesencephalic segment of the oculomotor nerve. CST, corticospinal tract; FPT, frontopontine tract; MB, mammillary body; ML, medial lemniscus; OPTPT, occipito-parieto-temporo-pontine tract; RN, red nucleus; III, oculomotor nerve; V, trigeminal nerve. The peritrigeminal zone is located between the emergences of V and VII nerves (Figure 6A) and averaged 8.9 mm. Progressive removal of superficial transverse pontine fibers discloses the pontine nuclei and the deep transverse fibers. The CST is broken up into discrete bundles separated by the transverse fibers and is located medially to the peritrigeminal zone (Figures 6B-6E). The peritrigeminal zone is limited laterally by the intrapontine fibers of V, dorsally by the trigeminal motor nucleus and the trigeminal spinal tract, and inferiorly by the intrapontine fibers of VII (Figure 6E). The average distance between the emergence of V and its motor nucleus was 13.7 mm. Extending the dissection medially, there is the risk of damaging the CST that is located 6 mm medial to the intrapontine segment of the V. Enlarging the dissection behind the deep transverse fibers there is the risk to injury the ML, the spinothalamic tract, and the lateral lemniscus, which on MRI form paired “crescents” that arc dorsally (Figure 6C and 6E). FIGURE 6. View largeDownload slide Peritrigeminal zone. A, This entry zone (orange area) is located between the origin of trigeminal and facial nerves. B to D, Fiber-dissection of the peritrigeminal zone and neurovavigation in axial B, sagittal C, and coronal planes D. The peritrigeminal zone is bounded medially by the corticospinal tract, laterally by the intrapontine fibers of the trigeminal nerve, dorsally by the trigeminal motor nucleus and the trigeminal spinal tract, and inferiorly by the intrapontine fibers of the facial nerve. E, The pointer is located on the trigeminal motor nucleus. CST, corticospinal tract; CTT, central tegmental tract; LL, lateral lemniscus; MCP, middle cerebellar peduncle; ML, medial lemniscus; O, olive; SCP, superior cerebellar peduncle; TST, trigeminal spinal tract; III, oculomotor nerve; V, trigeminal nerve, VI, abducens nerve; VII, facial nerve; VIII, vestibulocochlear nerve; IX, glossopharyngeal nerve; X, vagal nerve; XII, hypoglossal nerve. FIGURE 6. View largeDownload slide Peritrigeminal zone. A, This entry zone (orange area) is located between the origin of trigeminal and facial nerves. B to D, Fiber-dissection of the peritrigeminal zone and neurovavigation in axial B, sagittal C, and coronal planes D. The peritrigeminal zone is bounded medially by the corticospinal tract, laterally by the intrapontine fibers of the trigeminal nerve, dorsally by the trigeminal motor nucleus and the trigeminal spinal tract, and inferiorly by the intrapontine fibers of the facial nerve. E, The pointer is located on the trigeminal motor nucleus. CST, corticospinal tract; CTT, central tegmental tract; LL, lateral lemniscus; MCP, middle cerebellar peduncle; ML, medial lemniscus; O, olive; SCP, superior cerebellar peduncle; TST, trigeminal spinal tract; III, oculomotor nerve; V, trigeminal nerve, VI, abducens nerve; VII, facial nerve; VIII, vestibulocochlear nerve; IX, glossopharyngeal nerve; X, vagal nerve; XII, hypoglossal nerve. The anterolateral sulcus is located in the ventral surface of the medulla along the anterolateral preolivary sulcus inferior to the roots of XII (Figure 7A). The caudal limit is represented by the rostral C1 rootlets. The MRI clearly depicted the gray-folded lamina of the inferior olivary nucleus indicating the upper limit of the dissection (Figures 7B-7D). The CST in the medulla is located anteromedially to the inferior olivary nucleus and defines the medial border of the entry zone (Figure 7E). FIGURE 7. View largeDownload slide Anterolateral sulcus. A, This entry zone (orange area) is located between the inferior roots of the hypoglossal nerve and the superior C1 rootlets. B to D, Fiber-dissection of the anterolateral sulcus and neuronavigation in axial (B), sagittal (C), and coronal plane (D). E, The pointer is located in the anterolateral sulcus just below the apparent origin of the hypoglossal nerve. CST, costicospinal tract; ML, medial lemniscus; V, trigeminal nerve; VI, abducens nerve; VII, facial nerve; VIII, vestibulocochlear nerve nerve; IX glossopharyngeal nerve; X, vagal nerve; XII, hypoglossal nerve. FIGURE 7. View largeDownload slide Anterolateral sulcus. A, This entry zone (orange area) is located between the inferior roots of the hypoglossal nerve and the superior C1 rootlets. B to D, Fiber-dissection of the anterolateral sulcus and neuronavigation in axial (B), sagittal (C), and coronal plane (D). E, The pointer is located in the anterolateral sulcus just below the apparent origin of the hypoglossal nerve. CST, costicospinal tract; ML, medial lemniscus; V, trigeminal nerve; VI, abducens nerve; VII, facial nerve; VIII, vestibulocochlear nerve nerve; IX glossopharyngeal nerve; X, vagal nerve; XII, hypoglossal nerve. DISCUSSION EETA for Brainstem Lesions In brainstem cavernomas, EETA provides some advantages over standard microsurgical approaches, including a direct midline surgical corridor to the lesion avoiding cerebral retraction.30–36 The entry zones described in the literature for microsurgical resection of ventral intrinsic lesions of the brainstem include the perioculomotor zone and the lateral mesencephalic sulcus in the midbrain, the peritrigeminal zone in the pons, and the anterolateral and postolivary sulci in the medulla.1–7 In this study, we investigated the extent of endoscopic transclival exposure of safe entry zones for the 3 surgical working areas described. The EETA allowed exposure of the perioculomotor zone at the midbrain level, the peritrigeminal zone at the pons level, and the anterolateral sulcus at the medulla level. The endoscopic transclival exposure of the ventral surface of midbrain at the upper level requires mobilization of the pituitary gland and offers a wide view of the interpeduncular cistern. The perioculomotor zone was visible in 60% of specimens, whereas the parasellar segment of the ICA limited the exposure of the lateral mesencephalic sulcus. Pituitary transposition is the key step when the exposure of interpeduncular cistern is planned through an EETA. Kassam et al29 described the intradural transposition of the pituitary gland to access tumors extending to the interpeduncular fossa.29 However, this surgical maneuver is associated with a nonnegligible risk of producing pituitary dysfunction.29 Extradural pituitary transposition,37 which consists of mobilization of the gland covered by both layers of dura (meningeal and periosteal), and interdural transposition,38 which involves mobilization of the gland covered by the medial wall of the cavernous sinus, minimize the risk of pituitary dysfunction and provide access to selected extradural lesions and tumors with parasellar–retrosellar–suprasellar extensions, respectively. Recently, He et al32 treated a symptomatic ventral midbrain cavernoma via EETA using pituitary transposition. Our study showed that the endoscopic transclival exposure of the ventral pons allows unobstructed view of BA, of anterior pontine segment of AICA, and of the cisternal portion of VI. Moreover, the emergences of V and VII were barely visible. The exposure of the peritrigeminal zone was obtained with an extradural anterior petrosectomy that required removal of the additional bone surrounding the inferomedial surface of the horizontal segment of the petrous ICA.19,22,39 EETA to ventral pontine cavernomas has been described in 5 case reports from different groups30,31,33,34,36: gross-total resection was achieved in 4 cases and subtotal resection in 1 case. Clinical improvement was described in 4 cases and no postoperative deficits occurred in the remaining case. In our study, EETA of the lower level allowed exposure of the ventral surface of the medulla cranially to the anterior arch of C1 and medially to the inferior olives. The anterolateral sulcus was generally visible, although its exposure can be obstructed by the variable course of the VA. A lower extension of the approach with removal of anterior arch of C1 can be performed when the exposure of ventral cervicomedullary junction is required.40 Recently, Nayak et al35 reported 1 case of anterior medullary cavernoma resected through an EETA and C1 removal. Although the clinical results of brainstem cavernomas resected via EETA seem to be promising; the risk of postoperative CSF-leak remains a concern. In fact, of the 5 pontine cavernomas reported, 2 presented postoperative CSF-leak and required surgical revision.33,36 Furthermore, the bleeding generally observed when the prepontine dura is incised can increase the complexity of the approach. Brainstem Fiber Dissection Combined With Ultra-High-Field MRI The anatomy of the ventral safe entry zones exposed using EETA was investigated using fiber-dissection technique and correlated with 7T-MRI of the same specimen. Ultra-high-resolution MRI allows improved visualization of tiny anatomic structures of brainstem and offers unique opportunity for a detailed study of safe entry zones.28,41 The perioculomotor zone was originally described as a surgical corridor located lateral to the emergence of the III and medial to the CST.2,7 Neurotomy in this area should be performed in a rostrocaudal direction parallel to the frontopontine fibers running through the medial one-fifth of the cerebral peduncle. This surgical corridor is minute and care must be taken to avoid injury of the intramesencepahalic segment of III medially, of the CST laterally, and of the RN that is located approximately 8 mm from the pial surface. The peritrigeminal zone is actually considered the safest entry zone for the pontine lesions.1,42 Some authors favor a transverse neurotomy respecting the course of the pontocerebellar fibers to minimize the damage.6,27 When a transverse incision is performed, care should be taken to avoid damage to the CST located approximately 6 mm medially to the intrapontine segment of the V. The neurotomy should remain medially to the emergences of V and VII to preserve their intrapontine segments and their nuclei. The approach through the anterolateral sulcus, proposed for lesions of the anterolateral medulla, requires a vertical incision between the inferior roots of the XII and the superior C1 rootlets.3 The resultant surgical corridor is extremely narrow and carries high risk of damaging the CST. Accordingly, lesions at this level should be resected only when come to the surface and provide a direct corridor of attack. Although the combination of fiber-dissection with MRI information using a neuronavigation system has been previously reported for the analysis of the central-core of the cerebrum28; to the best of our knowledge, this is the first work describing this multimethodological validation in the study of brainstem anatomy. The ultra-high-field MRI resulted extremely effective in localization of fiber tracts and nuclei adjacent to the safe entry zones studied. Limitations Because our investigation is based on findings from normal cadaveric specimens, the conclusions are not strictly applicable to clinical cases in which the anatomic structures can be displaced by the pathology. In addition, although we investigated the extent of exposure of different working areas, we did not analyze the degree to which the different anatomic areas are suitable for surgical maneuvers. Finally, Klinger's technique produces some degree of tissue dehydration reducing the accuracy of our morphometric data. CONCLUSION EETA allows the exposure of selected safe entry zones of the ventral brainstem. The perioculomotor zone, exposed at midbrain level, requires mobilization of the pituitary gland and can be hindered by the SCA. The peritrigeminal zone is exposed at pontine level after extradural removal of anterior petrous bone. The anterolateral sulcus is exposed at medullary level although the course of VA can complicate its access. The combination of high-definition anatomic information provided by ultra-high-field MRI and fiber-dissection of the same specimen resulted useful in understanding the internal architecture of the brainstem. Disclosures This work has been partly supported by the grant “Marató TV3 Project” [411/U/2011—title: Quantitative analysis and computer aided simulation of minimally invasive approaches for intracranial vascular lesions]. The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article. 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Sanborn MR , Kramarz MJ , Storm PB , Adappa ND , Palmer JN , Lee JY . Endoscopic, endonasal, transclival resection of a pontine cavernoma: case report . Neurosurgery . 2012 ; 71 ( 1 Suppl Operative ): 198 – 203 . 37. Silva D , Attia M , Kandasamy J , Alimi M , Anand VK , Schwartz TH . Endoscopic endonasal posterior clinoidectomy . Surg Neurol Int . 2012 ; 3 ( 1) : 1 – 35 (Epub) . 38. Fernandez-Miranda JC , Gardner PA , Rastelli MM Jr et al. Endoscopic endonasal transcavernous posterior clinoidectomy with interdural pituitary transposition . J Neurosurg . 2014 ; 121 ( 1 ): 91 – 99 . 39. Zanation AM , Snyderman CH , Carrau RL , Gardner PA , Prevedello DM , Kassam AB . Endoscopic endonasal surgery for petrous apex lesions . Laryngoscope . 2009 ; 119 ( 1 ): 19 – 25 . 40. Kassam AB , Snyderman C , Gardner P , Carrau R , Spiro R . The expanded endonasal approach: a fully endoscopic transnasal approach and resection of the odontoid process: technical case report . Neurosurgery . 2005 ; 57 ( ONS Suppl 1 ): ONS213 – ONS214 . 41. Duyn JH . The future of ultra-high field MRI and fMRI for study of the human brain . Neuroimage . 2012 ; 15 ; 62 ( 2 ): 1241 – 1248 42. Baghai P , Vries JK , Bechtel PC . Retromastoid approach for biopsy of brain stem tumors . Neurosurgery . 1982 ; 10 ( 5 ): 574 – 579 . COMMENTS The authors performed a detailed and richly illustrated anatomical study of the safe entry zones to the ventral brainstem provided via the endoscopic endonasal transclival approach. The anterior aspect of the brainstem is notoriously difficult to reach and expose adequately using complex transcranial skull base approaches due to the significant brain retraction required. The endonasal transclival trajectory provides a direct working angle to the ventral brainstem and represents a valid option for most of ventral brainstem locations except, in our opinion, for lesions of the peritrigeminal area which can be accessed using a less invasive presigmoid retrolabyrinthine approach. However, some lesions do not reach the surface of the brainstem and thus small neurotomies are required. Regardless of the approach, a comprehensive understanding of the brainstem's internal architecture is essential for any neurosurgeon working within this critical region. Surface points and surgical corridors that are less dense in eloquent neurovascular structures can be considered as safe entry zones and knowledge of these optimal entry zones along with knowledge of the anatomy of the most critical structures is key for minimizing surgery related morbidity and mortality. In this comprehensive anatomical study, the authors not only investigated endoscopic endonasal transclival access to the ventral brainstem but provided a good explanation of the anatomy in a methodologically novel and thorough manner that sets a high bar for anatomosurgical studies. Antonio Bernardo Alexander I. Evins New York, New York This paper presents the careful white fiber dissection and 7T MRI anatomic correlation of ventral corridors into the brainstem via and endoscopic endonasal approach (EEA). The study is meticulously done and demonstrates remarkable anatomic knowledge as well as feasibility of endonasal entry points into the brainstem. However, it is critical to recognize this as a purely anatomic study; access is based and graded on ‘exposure’ of structures such as sulci or cranial nerves. The EEA was developed as a midline corridor for access to medial, ventral skull base pathologies. Merely exposing or visualizing these structures does not equate with ability to surgically access or safely dissect them via EEA. Indeed, the white matter dissections performed in this paper were done via traditional approaches (eg, anterior petrosectomy) using ‘open’ microsurgical technique; this is demonstrated in several figures, as pointers are introduced via a non-EEA trajectory which can be confusing (Figure 6). Future studies would be useful to include endonasal dissection of the proposed entry points as well as MRI based hi definition fiber tracking to demonstrate access points. Paul A. Gardner Pittsburgh, Pennsylvania The authors present a series of 8 cadaveric endoscopic endonasal transclival dissections of whole heads, and describe 8 white matter dissections of explanted cadaveric brainstems guided by surgical navigation using 7T MRIs of these brain stem specimens. The endoscopic dissections are excellent and provide good detail of the anatomy identified through such approaches. The technique of white matter dissection of the brain stem using surgical navigation with 7T MRIs is performed beautifully, and appears to be a powerful technique for study of white matter anatomy. One challenge with regard to this work is that the true clinical relevance of this work is uncertain as it is based solely on cadaveric dissections and 7T MRIs without definite applicability to “real life surgery”. Nonetheless, it is an excellent investigation of this anatomy and these surgical approaches as we moved to advance these techniques. Michael Chicoine St. Louis, Missouri Copyright © 2018 by the Congress of Neurological Surgeons This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)

Journal

Operative NeurosurgeryOxford University Press

Published: May 10, 2018

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