Microsurgical approaches to the cerebellar interpeduncular region: qualitative and quantitative analysis

Juan Leonardo Serrato-AvilaDepartment of Neurology and Neurosurgery,
Laboratory of Microneurosurgery Anatomy, and

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Juan Alberto Paz ArchilaDepartment of Neurology and Neurosurgery,
Laboratory of Microneurosurgery Anatomy, and

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Marcos Devanir Silva da CostaDepartment of Neurology and Neurosurgery,
Laboratory of Microneurosurgery Anatomy, and

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Paulo Ricardo RochaLaboratory of Microneurosurgery Anatomy, and
Department of Morphology and Genetics, Universidade Federal de Sao Paulo, Brazil;

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Sergio Ricardo MarquesDepartment of Morphology and Genetics, Universidade Federal de Sao Paulo, Brazil;

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Luis Otavio Carvalho de MoraesDepartment of Morphology and Genetics, Universidade Federal de Sao Paulo, Brazil;

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Sergio CavalheiroDepartment of Neurology and Neurosurgery,
Laboratory of Microneurosurgery Anatomy, and

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Kaan YağmurluDepartments of Neurosurgery and
Neuroscience, University of Virginia Health System, Charlottesville, Virginia;

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Michael T. LawtonDepartment of Neurosurgery, Barrow Neurological Institute, Phoenix, Arizona; and

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Feres Chaddad-NetoDepartment of Neurology and Neurosurgery,
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Department of Neurosurgery, Hospital Beneficência Portuguesa de São Paulo, Brazil

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OBJECTIVE

The cerebellar interpeduncular region (CIPR) is a gate for dorsolateral pontine and cerebellar lesions accessed through the supracerebellar infratentorial approach (SCITa), the occipital transtentorial approach (OTa), or the subtemporal transtentorial approach (STa). The authors sought to compare the exposures of the CIPR region that each of these approaches provided.

METHODS

Three approaches were performed bilaterally in eight silicone-injected cadaveric heads. The working area, area of exposure, depth of the surgical corridor, length of the interpeduncular sulcus (IPS) exposed, and bridging veins were statistically studied and compared based on each approach.

RESULTS

The OTa provided the largest working area (1421 mm2; p < 0.0001) and the longest surgical corridor (6.75 cm; p = 0.0006). Compared with the SCITa, the STa provided a larger exposure area (249.3 mm2; p = 0.0148) and exposed more of the length of the IPS (1.15 cm; p = 0.0484). The most bridging veins were encountered with the SCITa; however, no significant differences were found between this approach and the other approaches (p > 0.05).

CONCLUSIONS

To reach the CIPR, the STa provided a more extensive exposure area and more linear exposure than did the SCITa. The OTa offered a larger working area than the SCIT and the STa; however, the OTa had the most extensive surgical corridor. These data may help neurosurgeons select the most appropriate approach for lesions of the CIPR.

ABBREVIATIONS

CIPR = cerebellar interpeduncular region; CN = cranial nerve; IPS = interpeduncular sulcus; LMS = lateral mesencephalic sulcus; MCP = middle cerebellar peduncle; OTa = occipital transtentorial approach; SCA = superior cerebellar artery; SCITa = supracerebellar infratentorial approach; SCP = superior cerebellar peduncle; SPS = superior petrosal sinus; STa = subtemporal transtentorial approach.

OBJECTIVE

The cerebellar interpeduncular region (CIPR) is a gate for dorsolateral pontine and cerebellar lesions accessed through the supracerebellar infratentorial approach (SCITa), the occipital transtentorial approach (OTa), or the subtemporal transtentorial approach (STa). The authors sought to compare the exposures of the CIPR region that each of these approaches provided.

METHODS

Three approaches were performed bilaterally in eight silicone-injected cadaveric heads. The working area, area of exposure, depth of the surgical corridor, length of the interpeduncular sulcus (IPS) exposed, and bridging veins were statistically studied and compared based on each approach.

RESULTS

The OTa provided the largest working area (1421 mm2; p < 0.0001) and the longest surgical corridor (6.75 cm; p = 0.0006). Compared with the SCITa, the STa provided a larger exposure area (249.3 mm2; p = 0.0148) and exposed more of the length of the IPS (1.15 cm; p = 0.0484). The most bridging veins were encountered with the SCITa; however, no significant differences were found between this approach and the other approaches (p > 0.05).

CONCLUSIONS

To reach the CIPR, the STa provided a more extensive exposure area and more linear exposure than did the SCITa. The OTa offered a larger working area than the SCIT and the STa; however, the OTa had the most extensive surgical corridor. These data may help neurosurgeons select the most appropriate approach for lesions of the CIPR.

In Brief

The authors compared the exposure of the cerebellar interpeduncular region (CIPR) provided by the supracerebellar infratentorial approach (SCITa), the occipital transtentorial approach (OTa), and the subtemporal transtentorial approach (STa). To reach the cerebellar interpeduncular region, the STa provided a more extensive exposure area and more linear exposure than the SCITa did. The OTa offered a larger working area than the SCITa and the STa; however, the OTa had the most extensive surgical corridor. These data may help neurosurgeons select the most appropriate approach for lesions of the CIPR.

The cerebellar interpeduncular sulcus (IPS) is the junction between the superior cerebellar peduncle (SCP) and middle cerebellar peduncle (MCP) and is situated in the lateral aspect of the cerebellomesencephalic fissure and the inferoposterior part of the ambient cistern. It has been described as an entry zone for removing the pathologies located in the dorsolateral pons and cerebellar interpeduncular region (CIPR).1–9 For reaching the CIPR, the supracerebellar infratentorial approach (SCITa), the occipital transtentorial approach (OTa), and the subtemporal transtentorial approach (STa) are commonly used to achieve excellent surgical outcomes with minimal morbidity.3–9 Despite its great surgical importance, to the authors’ knowledge a comparison of the main surgical approaches in this region (SCITa, OTa, and STa) has never been performed. We performed qualitative and quantitative analyses of the SCITa, OTa, and STa to compare these approaches for reaching the CIPR, evaluating the main surgical parameters of surgical interest.

Methods

The present laboratory investigation was conducted after institutional review board authorization was obtained. Dissections of the SCITa, OTa, and STa were performed on eight formalin-fixed and silicon-injected cadaveric heads. For each approach, detailed quantitative and qualitative comparative analyses were performed on the working area, area of exposure, depth of the surgical corridor, length of the IPS exposed, and encounter rates of the bridging veins.

Quantification and Statistical Analysis

The working area was defined as the surgical corridor that corresponds to the angle of attack and area of maneuverability. The area of exposure was defined as the area of the CIPR, which is located around the cerebellar IPS. The exposure and working areas were determined by assigning five peripheral anatomical key points to each approach to form an irregular pentagon (Supplemental Tables 1 and 2). The IPS was selected as a central reference to measure the exposure areas (Fig. 1). Each area was delineated using the triangulation method, which consists of dividing the pentagon into 5 triangles. Notably, each triangle formed part of one of the sides of the pentagon that converged at the same point inside the pentagon. After that, each triangle area was calculated based on its 3 sides using Heron’s formula. Finally, each of the 5 triangles’ area was added, resulting in the total area of the pentagon.

FIG. 1.
FIG. 1.

Microsurgical anatomy of the CIPR and IPS. A–C: Extrinsic anatomy and limits. A: The CIPR is limited by the wing of the central lobule, which is located below the quadrangular lobule of the cerebellum. B: The left upper half of the quadrangular lobule was removed to expose the wing of the central lobule. C: The wing of the central lobule was removed to expose the CIPR. The floor of the CIPR is composed of the SCP and MCP, and the IPS is the natural cleft formed between them. The IPS is located in the center of CIPR. CN IV is the rostral limit of the CIPR; the IPS continues superior to CN IV as the LMS in the mesencephalic peduncle. D: Intrinsic anatomy. The fiber tracts of the CIPR have been exposed. The LMS and IPS have been left for reference. In the anterior end of the IPS, the parieto-temporo-occipito-pontine fibers are located anteriorly. The lateral lemniscus (LL) is found anteromedially covering the SCP on its way to the inferior colliculus. The intrapontine segment of CN V is situated inside the MCP on its way toward the trigeminal spinal tract located below the middle third of the IPS. In the posterior end, the IPS is located laterally, and the dentate nucleus is located medially. 1 = inferior colliculus; 2 = quadrangular lobule; 3 = culmen of the vermis; 4 = choroid plexus; 5 = pulvinar; 6 = medial geniculate body; 7 = wing of the central lobule; 8 = brachium of the inferior colliculus; 9 = superior colliculus; 10 = SCP; 11 = MCP; 12 = IPS; 13 = LMS; 14 = parieto-temporo-occipito-pontine fibers; 15 = LL; 16 = inferior cerebellar peduncle; 17 = dentate nucleus; 18 = corticospinal tract. Juan Leonardo Serrato-Avila, MD, prepared dissections. Copyright Feres Chaddad-Neto. Published with permission. Figure is available in color online only.

The depth of the surgical corridor was measured from the inner table of the skull to the uppermost point of the IPS, and the length of the exposed IPS was calculated. All distances were measured using a 150-mm Vernier caliper (530-104b-10, Mitutoyo). The bridging veins that were found inside the working areas and needed to be cut to allow for instrument maneuverability were reported.

The chi-square test or Fisher’s exact test was used for qualitative variables. Quantitative variables were compared using the Kruskal-Wallis test, and for multiple comparisons Dunn’s test was used; α = 0.05 was considered indicative of statistical significance. Data were analyzed, and graphs were created with Prism 8 software for Mac OS, version 8.4.3 (GraphPad Software).

Surgical Approaches

The SCITa, OTa, and STa were performed bilaterally in the cadaveric heads (Figs. 2–4). The procedures were performed in the same order such that prior craniotomies would not affect measurements, replacement of the bone flaps, and closing of the scalp. The SCITa was performed first, followed by the OTa and the STa. The heads were fixed in a Mayfield head holder, and the dissections were carried out with standard neurosurgical instruments, including a microsurgical set and a high-speed drill. The microsurgical technique was used for intradural dissection under magnification from ×6.4 to ×40 with an M320 LEICA microscope (Leica Microsystems AG). The photographs were obtained with a Canon EOS 450D camera, an EF-5 18e55 mm 1:3.5e5.6 IS zoom lens, and an EFS 60 mm f/2.8 USM macro lens (Canon, Inc.).

FIG. 2.
FIG. 2.

Supracerebellar infratentorial approach. A: The head was flexed to align the inion with the cervical spine to place the tentorium in a plane parallel to the floor and obtain a direct and unobstructed surgical view. Thereafter, the skin incision was marked. B: The flap was reflected, and the bony landmarks, including the inion, asterion, and superior nuchal line, were exposed. C: The burr holes and the craniotomy were performed according to the anatomical landmarks. D: The dural incision was marked just below the transverse sinus. The dura was retracted, exposing the superior cerebellar cistern. F: The surgical corridor was exposed. 1 = transverse sinus; 2 = sigmoid sinus; 3 = tentorial surface of the cerebellum; 4 = CN IV; 5 = superior tentorial vein; 6 = midbrain tectum; 7 = SCA; 8 = superior petrosal vein. Juan Leonardo Serrato-Avila, MD, prepared dissections. Copyright Feres Chaddad-Neto. Published with permission. Figure is available in color online only.

FIG. 3.
FIG. 3.

Occipital transtentorial approach. A: The head was placed without flexion to allow direct visualization of the CIPR. Thereafter, the incision was marked. B and C: The bony landmarks, including the lambdoid and sagittal sutures, inion, and superior nuchal line, were exposed before performing the craniotomy. D: The dural incision was marked just lateral to the sagittal sinus and above the transverse sinus. E: The dura was retracted, and the fixed retractor was positioned to open the surgical corridor. The surgical corridor was exposed. 1 = occipital pole; 2 = sagittal sinus; 3 = transverse sinus; 4 = CN IV; 5 = SCA; 6 = SCP; 7 = straight sinus; 8 = superior tentorial vein; 9 = tentorial surface of the cerebellum; 10 = basal vein of Rosenthal; 11 = midbrain tegmentum. Juan Leonardo Serrato-Avila, MD, prepared dissections. Copyright Feres Chaddad-Neto. Published with permission. Figure is available in color online only.

FIG. 4.
FIG. 4.

Subtemporal approach. A: The head was flexed to the contralateral side to obtain an unobstructed view of the basal cisterns. B: The flap was reflected, exposing the bony landmarks to guide the craniotomy; these landmarks consist of the root of the zygomatic arch, superior temporal line, and asterion. C: The craniotomy was performed as basally as possible. D: The dural incision was marked. E: The fixed retractor was placed to open the surgical corridor. The arachnoid of the ambient cistern was exposed. The surgical corridor was exposed. 1 = floor of the middle fossa; 2 = tentorium; 3 = arachnoid of the ambient cistern; 4 = inferior temporal gyrus; 5 = tentorial vein; 6 = quadrangular lobule; 7 = SCA; 8 = CN IV; 9 = LMS; 10 = base of the cerebral peduncle. Juan Leonardo Serrato-Avila, MD, prepared dissections. Copyright Feres Chaddad-Neto. Published with permission. Figure is available in color online only.

For the SCITa, a horseshoe incision was made, and burr holes were placed above the midline, superior nuchal line, and asterion (Fig. 2). The dura was opened in a curved fashion parallel to the transverse sinus and retracted inferiorly. After that, retracting sutures were placed below the transverse sinus to increase the size of the surgical corridor, as described by Kulwin et al.7

For the OTa (Fig. 3), a horseshoe incision was made, and burr holes were placed above the superior nuchal line, lateral to the sagittal suture, and above the lambdoid suture. The dura was opened in a curved fashion parallel to the sagittal and transverse sinuses. The dural edges adjacent to the sinuses were stitched and retracted to increase the surgical window size. In this approach, a fixed retractor superior to the calcarine cortex was needed to provide adequate exposure. The tentorium was obliquely cut between the lateral and medial tentorial sinuses and retracted laterally with sutures.6

For the STa, the heads were placed in a lateral decubitus position. They were tilted 30° toward the floor to correct the tentorium’s natural inclination and allow the temporal lobe to fall with gravity (Fig. 4). A horseshoe incision was used, and the burr holes were placed above the root of the zygomatic arch, asterion, and superior temporal line. The floor of the middle fossa was flattened with a cutting burr. The dura was opened in an inferiorly based U-shaped incision and retracted inferiorly. In this approach, gravity was not enough to properly expose this area. Therefore, a fixed retractor was used under the inferior temporal gyrus to widen the surgical corridor. The cisternal segment of cranial nerve (CN) IV was localized. After that, the tentorium was widely cut obliquely from behind the CN IV entrance and parallel to the superior petrosal sinus (SPS).10

For all three approaches, the superior half of the quadrangular lobule and the wing of the central lobule of the cerebellum were removed in a subpial fashion to expose the CIPR. Finally, the lateral aspect of the cerebellomesencephalic fissure was dissected to identify all of the structures of the CIPR (Fig. 5).

FIG. 5.
FIG. 5.

Exposure areas to the CIPR. All left-side dissections. A: Posterior view. Surgical corridors of the compared approaches. OTA = occipital transtentorial approach; SITA = supracerebellar infratentorial approach; STempA = subtemporal approach. B: Surgical view of the SCITa. C: Surgical view of the OTa. D: Surgical view of the STa. 1 = CN IV; 2 = lateral mesencephalic vein; 3 = vein of the SCP; 4 = anterior end of the IPS; 5 = rostral trunk of the SCA; 6 = culmen of the vermis; 7 = superior petrosal vein; 8 = pontotrigeminal vein; 9 = tentorium; 10 = superior colliculus; 11 = inferior colliculus; 12 = basal vein of Rosenthal; 13 = posterior end of the IPS; 14 = SPS; 15 = CN V; 16 = main trunk of the SCA; 17 = caudal trunk of the SCA. Juan Leonardo Serrato-Avila, MD, prepared dissections. Copyright Feres Chaddad-Neto. Published with permission. Figure is available in color online only.

Results

Qualitative Analysis

Supracerebellar Infratentorial Approach

The SCITa provided a posterolateral direct route to the CIPR (Figs. 5A, 5B, 6A, and 6B). This approach provided the significant advantage of greater gravity retraction compared to other approaches.

FIG. 6.
FIG. 6.

Artistic illustrations showing the studied approaches. A: Panoramic view comparing the three surgical approaches. B–D: Limits of the approaches and exposed neurovascular structures. B: SCITa. The limits of the working area in the surface of the corridor are formed by the torcula and vermis in the midline and the transverse-sigmoid sinus junction and tentorial surface of the cerebellum in the lateral aspect. C: OTa. The working area limits are formed by the torcula and the posterior calcarine vein in the midline and by the occipitobasal vein and calcarine sulcus in the lateral aspect. D: STa. The limits of the STa working area are composed of the vein of Labbé posteriorly, the zygomatic root inferiorly, and the temporal lobe superiorly. 1 = transverse-sigmoid junction; 2 = transverse sinus; 3 = torcula; 4 = tentorium; 5 = basal vein of Rosenthal; 6 = lateral mesencephalic vein; 7 = inferior colliculus; 8 = vermis; 9 = CN IV; 10 = SCA; 11 = vein of the SCP; 12 = pontotrigeminal vein; 13 = superior petrosal vein; 14 = tentorial surface of the cerebellum; 15 = sagittal sinus; 16 = posterior calcarine vein; 17 = occipitobasal vein; 18 = occipital pole; 19 = root of the zygoma; 20 = SPS; 21 = CN V; 22 = vein of Labbé; 23 = cingulate gyrus; 24 = splenium of the corpus callosum; 25 = pulvinar; 26 = straight sinus; 27 = temporal lobe; black dotted line = IPS. Copyright Johns Hopkins University, Art as Applied to Medicine. Published with permission. Figure is available in color online only.

The cerebellum fell away from the tentorium, consequently opening the surgical corridor. At this stage, the superior and inferior hemispheric bridging veins going into the tentorial sinuses were the main obstacles as they limited cerebellar retraction and maneuverability. Nevertheless, it was possible to work around these veins. This approach provided a broad mediolateral surgical view over the tentorial surface of the cerebellum, thus allowing the microscope to be tilted and the CIPR to be approached from various angles. The most easily exposed anatomical structures were the superior petrosal vein, uppermost point of the IPS, cerebellar vermis, distal cisternal segment of CN IV, lateral mesencephalic vein, pontotrigeminal vein, SCP vein, and rostral trunk of the superior cerebellar artery (SCA) (Fig. 5B). The most difficult structures to observe were those in the posterior limits of the exposure, including the lowermost point of the IPS and the caudal trunk of the SCA.

Occipital Transtentorial Approach

The OTa offered a posterosuperior to anteroinferior route to the CIPR (Figs. 5A, 5C, 6A, and 6C). The main limitations of this approach are occipital lobe retraction that may cause the visual defect and a deeper surgical corridor, and the tentorium as an obstacle for the CIPR. This approach allowed a panoramic view of the posterior incisural space and a comprehensive anteroposterior surgical view of the CIPR parallel to the falx. The most easily seen anatomical structures were the uppermost point of the IPS, the quadrigeminal plate, the proximal cisternal segment of CN IV, Rosenthal’s basal vein, the vein of SCP, the rostral trunk of the SCA, and the lowermost point of the IPS (Fig. 5C). The most difficult structures to expose were the superior petrosal vein, pontotrigeminal vein, and SCA main trunk.

Subtemporal Approach

The STa provided a lateromedial route to the CIPR (Figs. 5A, 5D, 6A, and 6D). The temporal lobe retraction was limited by the vein of Labbé and the posterior temporal basal veins draining into tentorial sinuses. The next obstacle was the tentorium. This approach offered widespread surgical exposure by an extensive tentorial cut. It allowed complete visualization of the superior petrosal vein, pontotrigeminal vein, lateral mesencephalic vein, vein of the SCP, SPS, CNs V and IV, and the main trunk of the SCA, including its rostral and caudal branches, as well as the uppermost point of the IPS (Fig. 5D). The surgical view was limited for the inferior aspect of the CIPR and lowermost end of the IPS.

Quantitative Analysis

The anatomical landmarks that delineate the working area and exposure area, including the distances between those landmarks for each surgical approach, are shown in Supplemental Tables 1 and 2, respectively.

The working area (Fig. 7A) was 815.3 mm2 for the SCITa, 1421 mm2 for the OTa, and 692.9 mm2 for the STa (p < 0.0001). The difference favored the OTA, with statistical significance when compared to the SCITa and the STa (p = 0.0002 and p < 0.0001, respectively). The comparison between the SCITa and the STa revealed no significant difference (p = 0.9139).

FIG. 7.
FIG. 7.

Comparison of the studied surgical approaches to the CIPR shown as box-and-whisker plots. A: Working area. B: Exposure area. C: Depth of the surgical corridor. D: IPS length. Figure is available in color online only.

The exposure area was 158.3 mm2 for the SCITa, 168.7 mm2 for the OTa, and 249.3 mm2 for the STa (p = 0.0082) (Fig. 7B). There was a significant difference that favored the STa compared to the SCITa (p = 0.0148); however, there was no significant difference between STa and the OTa (p = 0.1197). The comparison between the SCITa and the OTa also revealed no significant difference (p > 0.9999).

The distance from the inner table of the skull to the uppermost point of the IPS was 5.6 cm for the SCITa, 6.75 cm for the OTa, and 5.7 cm for the STa (p = 0.0006) (Fig. 7C). The most considerable distance was for the OTa, with statistical significance compared to the SCITa and the STa (p = 0.014 and p = 0.0091, respectively). The comparison between the SCITa and the STa revealed no significant difference (p > 0.9999).

The length of the IPS exposure (linear exposure) (Fig. 7D) was 0.7 cm for the SCITa, 1.1 cm for the OTa, and 1.15 cm for the STa (p = 0.0355). Although the distance was similar in the three approaches, the differences favored the STa with statistical significance only compared to the SCITa (p = 0.0484). The comparison of the SCITa and OTa was not significantly different (p = 0.2201).

The bridging veins were found most frequently in the SCITa (Supplemental Table 1). Nevertheless, there was no significant difference between the approaches for the located veins versus the cut veins (p > 0.05). Moreover, no significant difference was found between the right and left sides (p > 0.05).

Two illustrative cases added for clinical correlation are shown in Fig. 8.

FIG. 8.
FIG. 8.

Illustrative cases. A–I: Images obtained from a 7-year-old boy with a low-grade glioma of the pons tegmentum. A and B: Preoperative MRI sagittal postcontrast T1 and axial T2-weighted images, respectively. The lesion was centered in the MCP causing dorsal displacement of the pons tegmentum and asymmetry of the fourth ventricle. C: Preoperative tractography showing the tumor (yellow mass) located between the SCP and MCP, and posterior to the CST (blue projection fibers). D–F: Intraoperative photographs. An SCITa was performed and the tumor removed through the IPS entry zone (white arrow). G–I: Postoperative MRI sagittal T1, axial postcontrast T1, and T2-weighted images, respectively, showing complete resection of the tumor (reprinted from World Neurosurgery, vol 138, Sergio Cavalheiro, Juan Leonardo Serrato-Avila, Richard Gonzalo Párraga, M. D. S. Da Costa, Jardel Mendoça Nicácio, Paulo Ricardo Rocha, and Feres Chaddad-Neto, Interpeduncular sulcus approach to the posterolateral pons, e795–e805, 2020, with permission from Elsevier). J–R: Images obtained from an 18-year-old female patient with a cerebellomesencephalic fissure arteriovenous malformation (AVM). J and K: Preoperative MRI axial and sagittal postcontrast T1-weighted images showing the AVM (red arrow) located in the right cerebellomecencephalic fissure, lateral to the SCP. L: Preoperative angiography showing the AVM nidus originating from the superior trunk of the SCA (red arrow). M–O: Intraoperative photographs. An SCITa was performed and the ipsilateral quadrangular lobule of the cerebellum was partially removed to gain exposure area. The dissection of the cerebellomesencephalic fissure, circumferential dissection, and resection of the AVM are shown, respectively. P and Q: Postoperative MRI postcontrast T1-weighted images showing complete resection of the AVM. R: Postoperative angiography showing total resection of the AVM nidus and preservation of the distal SCA. 1 = CN IV, 2 = tentorium, 3 = SCA, 4 = SCP; 5 = MCP, 6 = vermis, 7 = basal vein of Rosenthal. Figure is available in color online only.

Discussion

Several safe entry zones have been recently described to access intrinsic pathology in the dorsolateral pons and the CIPR.11,12 These entry points are the epitrigeminal zone located in the MCP just above CN V and the IPS between the SCP and MCP.8,9 Furthermore, several surgical approaches have been described to access safe entry zones or exophytic lesions of the CIPR.13–16 The CIPR can be accessed through posterior approaches such as the SCITa, which can be used for clipping SCA aneurysms, the vascular pathology, and tumors located in the SCP, MCP, and tectum.13,17 The primary concerns of this approach include the well-known potential for an air embolism due to the semisitting position. The bridging veins are also an obstacle for maneuverability and visibility through the surgical corridor. Results of several studies have supported coagulating and cutting the bridging veins without causing neurological deficits in the patient;7,18–20 however, different studies have reported otherwise.21,22 Therefore, in our clinical practice, we try to preserve these veins and work between them whenever possible. The authors of a cadaveric study reported an average number of 1.69 (range 0–3) hemispheric bridging veins, which was similar to our finding of an average of 1.25 (range 0–3) veins.23

The OTa is another posterior approach that can be used to access the CIPR.5,24–26 This approach has been modified by laterally retracting the occipital lobe using the interhemispheric corridor.27 Thereafter, the OTa was extended to reach the posterior incisural space lesions, from the cerebellomesencephalic fissure to the corpus callosum and including the atrium of the lateral ventricle, velum interpositum, third ventricle, and medial thalamus.5,6,24 Few bridging veins have been encountered with this approach, and these were located 5 cm superior to the occipital pole through the OTa.28 Care should be taken to preserve the visual cortex during the retraction.29,30 Another major disadvantage of this approach is that working between the crucial deep venous complex demands more experience and technical skills.24

Combined approaches such as the supra-infratentorial-transsinus31 and occipital transtentorial or falcine approaches24 have been proposed to enlarge the surgical corridor by increasing the space between the occipital lobes and increasing contralateral exposure of the quadrigeminal region and ambient cistern, respectively. These approaches are preferred for lesions extending contralaterally as well as above and below the venous complex.

Moreover, lateral approaches, particularly the STa with tentorial opening, have been used to approach this area.8,32 The STa has been used to treat posterior circulating aneurysms and tumors located in the tentorium, parahippocampal gyrus, lateral midbrain, and pons.4,10,33–35 Even the anterior incisural space and upper clivus can be accessed if CN IV is freed from its canal and the tentorial cut is extended toward Meckel’s cave.3,36 The main concern with this approach is temporal lobe retraction and the associated venous complications, such as injury of the vein of Labbé and temporal basal veins. Several strategies have been proposed to prevent these complications, such as performing a lumbar drainage procedure, removing a generous amount of bone from the middle fossa, and dissecting and detaching the vein of Labbé from the temporal lobe.34,37 The bridging veins of the temporal lobe can be dissected and preserved.3

Comparison of the SCITa, STa, anterior petrosal approach, and posterior petrosal approach to access the pontomesencephalic junction was performed in a cadaveric study by Jittapiromsak et al.32 In this study, linear exposures along the lateral mesencephalic sulcus (LMS), IPS, and pontomesencephalic sulcus were measured for each approach. The IPS exposed length was superior for the STa (13.2 mm), a finding similar to that in our study (11.15 mm). The only significant difference was between the STa and the SCITa, also in concordance with our results. Similar to our research, Jittapiromsak et al. reported better visualization of the anterior aspect and more insufficient visualization of the posteroinferior part of the SCITa. Nevertheless, these authors did not include working or exposure areas, and their study focused on the region of the anterolateral pontomesencephalic junction.

For the SCITa, we did not open the tentorium since it has been demonstrated that cutting the tentorium to approach lesions of the lateral pontomesencephalic junction does not offer additional benefits or increase exposure.32,38 Moreover, we combined the extreme lateral and paramedian corridors between the torcula and the transverse-sigmoid junction to increase instrument maneuverability between bridging veins and improve the attack angle of the surgical corridor. Ulm et al. noted that the OTa and SCITa have similar exposure outcomes between the perimesencephalic cisterns and their structures.39 This finding was consistent with the lack of a statistically significant difference in the exposure areas between those two approaches. These authors also reported that the transinsular transchoroidal approach provided adequate exposure of the inferior portion of the ambient cistern and the anterior P3 segment of the posterior cerebral artery. Nevertheless, through this approach it would be difficult to reach the posteroinferior aspect of the CIPR due to its narrow corridor and the large number of crossing vessels. Moreover, the scope of this study did not include the posterior and inferior aspects of the CIPR.

An essential surgical strategy to reach the floor and posterior aspect of the CIPR is sectioning the superior half of the cerebellum’s quadrangular lobule. Our group previously reported that when the SCITa is used this strategy increased the surgical corridor without clinical repercussions for the patient.9,40 Therefore, we decided to use this strategy regardless of the approach.

The SCITa variants and the Sta were compared as approaches for the LMS, and the authors concluded that the STa provides a larger surgical exposure, although the differences between the approaches were not significant.41 The CIPR was omitted in that cadaveric study.

In another cadaveric study, the SCITa, STa, occipital interhemispheric, and transchoroidal approaches were compared to access the ambient cistern.42 The authors found no significant differences between the areas of exposure among these approaches. Nevertheless, there was increased linear exposure along the posterior cerebral artery with the STa compared to the SCITa. Although the CIPR was adjacent to the studied region in this study, it was not included; this is thought to account for the differences in results between this reported study and our study.

Despite excellent descriptions available in the literature regarding anatomy and surgical approaches for the cerebellomesencephalic fissure and posterior incisural space,5,24,43 to our knowledge, there is still a lack of information regarding comparisons between the most commonly used approaches (the SCITa, OTa, and STa) to the cerebellomesencephalic fissure, specifically to the CIPR.

We observed a wider mediolateral area in terms of surgical exposure but restricted inferior view through the SCITa. The OTa provided an increased anteroposterior area but a restricted lateral view. Finally, the STa provided a wider exposure in the anteroposterior and mediolateral directions due to an extensive tentorial cut but provided a restricted inferior exposure to the CIPR. This limitation was caused by the visual obstruction of the temporal lobe when tilting the microscope, as noted previously.4,24,38,44

The significant statistical differences found for the working area in the OTa compared to the other approaches favor the use of the OTa when more maneuverability with the instruments is needed in the proximal part of the surgical corridor adjacent to the craniotomy. Moreover, the OTa provides more viewing angles through the microscope. The significant difference (p = 0.0148) found between the SCITa and STa for surgical exposure in the targeted area could support the use of the STa when more space is needed in the depth of the surgical corridor and for bigger lesions of the CIPR. Another parameter of surgical interest regarding the OTa that was found to have statistical significance (p = 0.0006) was the longest depth of the surgical corridor. These findings could serve the neurosurgeon in selection of the appropriate length of instruments and assist in the selection of the approach, according to the surgeon’s preference. If the IPS needs to be exposed in all of its length, for example, to remove a cavernoma or a glioma located in the pons tegmentum with dorsolateral extension, then according to our findings the most useful approaches could be the STa and the OTa.

We seemed to observe more bridging veins in the SCITa; nevertheless, there was no significant difference in the number of bridging veins between the approaches. Despite these findings, it is important to be aware that every approach has its own veins to be preserved and other veins that could be coagulated with relative safety. For the SCITa the veins encountered in the surgical corridor include the hemispheric bridging veins, the vermian veins, and the vein of the cerebellomesencephalic fissure. These veins can generally be sacrificed without clinical repercussions.1,7,18–20 Nevertheless, a few occurrences of ischemic and hemorrhagic venous infarction of the cerebellum have been described.21,22 A major advantage of the OTa is the low number of bridging veins around the occipital pole. In this approach the involved veins that can potentially limit the working area are the occipitobasal vein laterally and the posterior calcarine vein superiorly. Special care should be taken while retracting the occipital lobe laterally to preserve the posterior calcarine vein because it drains the calcarine cortex. Therefore, homonymous hemianopsia is prevented. Sacrifice of one or two occipitobasal veins has been reported without important clinical repercussions.29 However, long-term visual field deficits have been reported in up to 17% of patients due to either retraction or vein thrombosis.5 Other series have reported complete preservation of these veins using the three-quarter prone position.5,6 In the depth of the surgical corridor the internal cerebral vein and basal veins with their tributaries, including the vein of the cerebelomesencephalic fissure, are encountered and obstruct the superior surgical view. The former veins must be preserved, and the vein of the cerebellomesencephalic fissure can be safely coagulated in the majority of the cases without causing neurological deficits.5,24 In the STa the involved veins are the vein of Labbé in the external aspect of the surgical corridor and the temporobasal and sphenopetrosal veins in the deeper part of the working area. Care should be taken to prevent temporal infarction caused by occlusion of these vessels. In a previous study,45 careful preoperative planning with curved planar reconstruction in patients with preoperative CT venography was used to access venous anatomy and guide the tentorial cut. The authors preserved all veins and coagulated 7 of 14 isolated tentorial sinuses without causing any venous complications. The vein of Labbé usually anastomoses to the transverse sinus 1 to 2 cm posterior to the sinodural angle. Nevertheless, a complete understanding of this venous complex and its anatomical variants is mandatory, because in a few cases the vein of Labbé can drain into the superior petrosal or tentorial sinus.45 Moreover, it is necessary to establish how anteriorly the temporobasal veins are located, because the more anterior they are, the narrower the surgical corridor becomes.

Other strategies have been used to decrease the low but existing risk of venous infarction. These strategies include a careful study of the venous complex and collateral drainage of critical structures with MR venography or angiography in the venous phase. Another important strategy includes the use of intraoperative neurophysiological monitoring to detect changes while a temporary clip is placed on the vein to be coagulated.23

The increased exposure area in the STa and OTa compared with the SCITa could be mainly caused by the tentorial cut. The larger working area provided by the OTa in contrast to the SCITa and STa was strongly modified by the craniocaudal position of the posterior calcarine vein. On the other hand, the STa had a smaller working area because temporal lobe retraction was limited by the vein of Labbé. This limitation was compensated by the surgical corridor’s shallow depth and the increased exposure area.

Conclusions

We have reported what is to our knowledge the first study to compare access to the CIPR provided by the SCITa, OTa, and STa. The STa provides a larger area of exposure and a greater length of exposed IPS compared to the SCITa. The OTa has a larger working area than the SCITa and STa. However, the OTa has the most extensive surgical corridor. Moreover, when a better anteroposterior surgical view is needed, the OTa is preferred. When a wider laterolateral exposure is required, the SCITa is a better choice. If the surgical exposure needs to be broad and similar in the anteroposterior and laterolateral directions, the STa could be the better option. However, being a cadaveric study, this investigation lacks crucial clinical data and analysis of approach-specific risks, which should always be considered in addition to dimensions of exposure. All surgical approaches must be tailored for each patient because of normal variability of the anatomy and different types of pathology.

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: da Costa, Serrato-Avila, Paz Archila, Cavalheiro, Chaddad-Neto. Acquisition of data: Serrato-Avila, Paz Archila, Rocha. Analysis and interpretation of data: da Costa, Serrato-Avila, Paz Archila, Rocha, Yağmurlu, Chaddad-Neto. Drafting the article: da Costa, Serrato-Avila, Paz Archila. Critically revising the article: da Costa, Serrato-Avila, Marques, de Moraes, Cavalheiro, Yağmurlu, Lawton, Chaddad-Neto. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: da Costa. Statistical analysis: da Costa, Serrato-Avila, Chaddad-Neto. Administrative/technical/material support: Rocha, Marques, de Moraes, Chaddad-Neto. Study supervision: Cavalheiro, Chaddad-Neto.

Supplemental Information

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Supplemental material is available with the online version of the article.

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Illustration from Serrato-Avila (pp 1410–1423). Copyright Johns Hopkins University, Art as Applied to Medicine. Published with permission.

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    FIG. 1.

    Microsurgical anatomy of the CIPR and IPS. A–C: Extrinsic anatomy and limits. A: The CIPR is limited by the wing of the central lobule, which is located below the quadrangular lobule of the cerebellum. B: The left upper half of the quadrangular lobule was removed to expose the wing of the central lobule. C: The wing of the central lobule was removed to expose the CIPR. The floor of the CIPR is composed of the SCP and MCP, and the IPS is the natural cleft formed between them. The IPS is located in the center of CIPR. CN IV is the rostral limit of the CIPR; the IPS continues superior to CN IV as the LMS in the mesencephalic peduncle. D: Intrinsic anatomy. The fiber tracts of the CIPR have been exposed. The LMS and IPS have been left for reference. In the anterior end of the IPS, the parieto-temporo-occipito-pontine fibers are located anteriorly. The lateral lemniscus (LL) is found anteromedially covering the SCP on its way to the inferior colliculus. The intrapontine segment of CN V is situated inside the MCP on its way toward the trigeminal spinal tract located below the middle third of the IPS. In the posterior end, the IPS is located laterally, and the dentate nucleus is located medially. 1 = inferior colliculus; 2 = quadrangular lobule; 3 = culmen of the vermis; 4 = choroid plexus; 5 = pulvinar; 6 = medial geniculate body; 7 = wing of the central lobule; 8 = brachium of the inferior colliculus; 9 = superior colliculus; 10 = SCP; 11 = MCP; 12 = IPS; 13 = LMS; 14 = parieto-temporo-occipito-pontine fibers; 15 = LL; 16 = inferior cerebellar peduncle; 17 = dentate nucleus; 18 = corticospinal tract. Juan Leonardo Serrato-Avila, MD, prepared dissections. Copyright Feres Chaddad-Neto. Published with permission. Figure is available in color online only.

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    FIG. 2.

    Supracerebellar infratentorial approach. A: The head was flexed to align the inion with the cervical spine to place the tentorium in a plane parallel to the floor and obtain a direct and unobstructed surgical view. Thereafter, the skin incision was marked. B: The flap was reflected, and the bony landmarks, including the inion, asterion, and superior nuchal line, were exposed. C: The burr holes and the craniotomy were performed according to the anatomical landmarks. D: The dural incision was marked just below the transverse sinus. The dura was retracted, exposing the superior cerebellar cistern. F: The surgical corridor was exposed. 1 = transverse sinus; 2 = sigmoid sinus; 3 = tentorial surface of the cerebellum; 4 = CN IV; 5 = superior tentorial vein; 6 = midbrain tectum; 7 = SCA; 8 = superior petrosal vein. Juan Leonardo Serrato-Avila, MD, prepared dissections. Copyright Feres Chaddad-Neto. Published with permission. Figure is available in color online only.

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    FIG. 3.

    Occipital transtentorial approach. A: The head was placed without flexion to allow direct visualization of the CIPR. Thereafter, the incision was marked. B and C: The bony landmarks, including the lambdoid and sagittal sutures, inion, and superior nuchal line, were exposed before performing the craniotomy. D: The dural incision was marked just lateral to the sagittal sinus and above the transverse sinus. E: The dura was retracted, and the fixed retractor was positioned to open the surgical corridor. The surgical corridor was exposed. 1 = occipital pole; 2 = sagittal sinus; 3 = transverse sinus; 4 = CN IV; 5 = SCA; 6 = SCP; 7 = straight sinus; 8 = superior tentorial vein; 9 = tentorial surface of the cerebellum; 10 = basal vein of Rosenthal; 11 = midbrain tegmentum. Juan Leonardo Serrato-Avila, MD, prepared dissections. Copyright Feres Chaddad-Neto. Published with permission. Figure is available in color online only.

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    FIG. 4.

    Subtemporal approach. A: The head was flexed to the contralateral side to obtain an unobstructed view of the basal cisterns. B: The flap was reflected, exposing the bony landmarks to guide the craniotomy; these landmarks consist of the root of the zygomatic arch, superior temporal line, and asterion. C: The craniotomy was performed as basally as possible. D: The dural incision was marked. E: The fixed retractor was placed to open the surgical corridor. The arachnoid of the ambient cistern was exposed. The surgical corridor was exposed. 1 = floor of the middle fossa; 2 = tentorium; 3 = arachnoid of the ambient cistern; 4 = inferior temporal gyrus; 5 = tentorial vein; 6 = quadrangular lobule; 7 = SCA; 8 = CN IV; 9 = LMS; 10 = base of the cerebral peduncle. Juan Leonardo Serrato-Avila, MD, prepared dissections. Copyright Feres Chaddad-Neto. Published with permission. Figure is available in color online only.

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    FIG. 5.

    Exposure areas to the CIPR. All left-side dissections. A: Posterior view. Surgical corridors of the compared approaches. OTA = occipital transtentorial approach; SITA = supracerebellar infratentorial approach; STempA = subtemporal approach. B: Surgical view of the SCITa. C: Surgical view of the OTa. D: Surgical view of the STa. 1 = CN IV; 2 = lateral mesencephalic vein; 3 = vein of the SCP; 4 = anterior end of the IPS; 5 = rostral trunk of the SCA; 6 = culmen of the vermis; 7 = superior petrosal vein; 8 = pontotrigeminal vein; 9 = tentorium; 10 = superior colliculus; 11 = inferior colliculus; 12 = basal vein of Rosenthal; 13 = posterior end of the IPS; 14 = SPS; 15 = CN V; 16 = main trunk of the SCA; 17 = caudal trunk of the SCA. Juan Leonardo Serrato-Avila, MD, prepared dissections. Copyright Feres Chaddad-Neto. Published with permission. Figure is available in color online only.

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    FIG. 6.

    Artistic illustrations showing the studied approaches. A: Panoramic view comparing the three surgical approaches. B–D: Limits of the approaches and exposed neurovascular structures. B: SCITa. The limits of the working area in the surface of the corridor are formed by the torcula and vermis in the midline and the transverse-sigmoid sinus junction and tentorial surface of the cerebellum in the lateral aspect. C: OTa. The working area limits are formed by the torcula and the posterior calcarine vein in the midline and by the occipitobasal vein and calcarine sulcus in the lateral aspect. D: STa. The limits of the STa working area are composed of the vein of Labbé posteriorly, the zygomatic root inferiorly, and the temporal lobe superiorly. 1 = transverse-sigmoid junction; 2 = transverse sinus; 3 = torcula; 4 = tentorium; 5 = basal vein of Rosenthal; 6 = lateral mesencephalic vein; 7 = inferior colliculus; 8 = vermis; 9 = CN IV; 10 = SCA; 11 = vein of the SCP; 12 = pontotrigeminal vein; 13 = superior petrosal vein; 14 = tentorial surface of the cerebellum; 15 = sagittal sinus; 16 = posterior calcarine vein; 17 = occipitobasal vein; 18 = occipital pole; 19 = root of the zygoma; 20 = SPS; 21 = CN V; 22 = vein of Labbé; 23 = cingulate gyrus; 24 = splenium of the corpus callosum; 25 = pulvinar; 26 = straight sinus; 27 = temporal lobe; black dotted line = IPS. Copyright Johns Hopkins University, Art as Applied to Medicine. Published with permission. Figure is available in color online only.

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    FIG. 7.

    Comparison of the studied surgical approaches to the CIPR shown as box-and-whisker plots. A: Working area. B: Exposure area. C: Depth of the surgical corridor. D: IPS length. Figure is available in color online only.

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    FIG. 8.

    Illustrative cases. A–I: Images obtained from a 7-year-old boy with a low-grade glioma of the pons tegmentum. A and B: Preoperative MRI sagittal postcontrast T1 and axial T2-weighted images, respectively. The lesion was centered in the MCP causing dorsal displacement of the pons tegmentum and asymmetry of the fourth ventricle. C: Preoperative tractography showing the tumor (yellow mass) located between the SCP and MCP, and posterior to the CST (blue projection fibers). D–F: Intraoperative photographs. An SCITa was performed and the tumor removed through the IPS entry zone (white arrow). G–I: Postoperative MRI sagittal T1, axial postcontrast T1, and T2-weighted images, respectively, showing complete resection of the tumor (reprinted from World Neurosurgery, vol 138, Sergio Cavalheiro, Juan Leonardo Serrato-Avila, Richard Gonzalo Párraga, M. D. S. Da Costa, Jardel Mendoça Nicácio, Paulo Ricardo Rocha, and Feres Chaddad-Neto, Interpeduncular sulcus approach to the posterolateral pons, e795–e805, 2020, with permission from Elsevier). J–R: Images obtained from an 18-year-old female patient with a cerebellomesencephalic fissure arteriovenous malformation (AVM). J and K: Preoperative MRI axial and sagittal postcontrast T1-weighted images showing the AVM (red arrow) located in the right cerebellomecencephalic fissure, lateral to the SCP. L: Preoperative angiography showing the AVM nidus originating from the superior trunk of the SCA (red arrow). M–O: Intraoperative photographs. An SCITa was performed and the ipsilateral quadrangular lobule of the cerebellum was partially removed to gain exposure area. The dissection of the cerebellomesencephalic fissure, circumferential dissection, and resection of the AVM are shown, respectively. P and Q: Postoperative MRI postcontrast T1-weighted images showing complete resection of the AVM. R: Postoperative angiography showing total resection of the AVM nidus and preservation of the distal SCA. 1 = CN IV, 2 = tentorium, 3 = SCA, 4 = SCP; 5 = MCP, 6 = vermis, 7 = basal vein of Rosenthal. Figure is available in color online only.

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