OBJECTIVE: A common approach to lesions of the pineal region is along the midline below the torcula. However, reports of how shifting the approach off midline affects the surgical exposure and relationships between the tributaries of the vein of Galen are limited. The purpose of this study is to examine the microsurgical and endoscopic anatomy of the pineal region as seen through the supracerebellar infratentorial approaches, including midline, paramedian, lateral, and far-lateral routes.

METHODS: The quadrigeminal cisterns of 8 formalin-fixed adult cadaveric heads were dissected and examined with the aid of a surgical microscope and straight endoscope. Twenty CT angiograms were examined to measure the depth of the pineal gland, slope of the tentorial surface of the cerebellum, and angle of approach to the pineal gland in each approach.

RESULTS: The midline supracerebellar route is the shortest and provides direct exposure of the pineal gland, although the culmen and inferior and superior vermian tributaries of the vein of Galen frequently block this exposure. The off-midline routes provide a surgical exposure that, although slightly deeper, may reduce the need for venous sacrifice at both the level of the veins from the superior cerebellar surface entering the tentorial sinuses and at the level of the tributaries of the vein of Galen in the quadrigeminal cistern, and require less cerebellar retraction. Shifting from midline to off-midline exposure also provides a better view of the cerebellomesencephalic fissure, collicular plate, and trochlear nerve than the midline approaches. Endoscopic assistance may aid exposure of the pineal gland while preserving the bridging veins.

CONCLUSIONS: Understanding the characteristics of different infratentorial routes to the pineal gland will aid in gaining a better view of the pineal gland and cerebellomesencephalic fissure and may reduce the need for venous sacrifice at the level of the tentorial sinuses draining the upper cerebellar surface and the tributaries of the vein of Galen.

Supracerebellar infratentorial approaches are commonly used for lesions involving the pineal gland.^{1,6, 10,13,32} Although the midline route is frequently selected, there is the potential for several off-midline routes between the torcula medially and the asterion at the junction of the transverse and sigmoid sinuses laterally. The midline and off-midline routes differ with respect to depth and angle of approach, area of exposure, and risk to vascular structures along the approach. This study examined the microsurgical and endoscopic anatomy of the various infratentorial routes to the pineal gland, including midline, paramedian, lateral, and far-lateral supracerebellar infratentorial approaches. In addition, this study also defined the depth of the pineal gland and angle of the tentorial surface of the cerebellum through each infratentorial route.

The posterior incisural spaces of 8 formalin-fixed adult cadaveric heads were examined in this study. The arteries and veins of 6 of the 8 formalin-perfused adult cadaveric heads were injected with red and blue colored silicone. All cadaveric heads were examined using 3–40× magnifications provided by an operating microscope and the straight endoscope. Bone dissection was done with a high-speed drill. The dissections followed the steps of the surgical procedures.

The distance to the pineal gland, slope of upper cerebellar surface, and angle of approach were measured on CT angiography (CTA) images obtained in 20 consecutive adult patients (6 men and 14 women) who underwent CTA for evaluation of unruptured intracranial aneurysms. The mean age of the patients was 62.7 years (range 40–82 years).

The CTA studies were obtained using a 64-slice Toshiba Aquilion 64 system (Toshiba Medical Systems) in 12 cases and a 320-slice Toshiba Aquilion One system in the remaining 8 cases. All imaging studies were performed at Kyushu University Hospital. None of the patients had mass effect due to an intracranial lesion.

The imaging data were analyzed with OsiriX imaging software version 5.9 (http://www.osirix-viewer.com) and observed using 2D multiplanar reconstruction with axial view; all axial planes were confirmed to be parallel to the orbitomeatal line.

In examining the different supracerebellar infratentorial approaches (routes), the distance between the inion and junction of the transverse and sigmoid sinuses was divided into thirds as previously reported.¹¹ The midline route was directed along the midline below the torcula, the paramedian route along the junction of the medial and intermediate (middle) thirds, the lateral route along the junction of the intermediate and lateral thirds, and the far-lateral above the cerebellum adjacent to the junction of the transverse and sigmoid sinuses (Fig. 1A and B). An axial plane was adjusted to intersect the junction of the transverse and sigmoid sinuses (Fig. 1A). Before measurement, the approach point for each route, the point just below the transverse sinus and on the inner surface of the occipital bone was determined (Fig. 1C–F). For each route, a sagittal plane, perpendicular to the axial plane, that intersected the pineal gland and approach point was used to measure the depth of the pineal gland, slope of the surface of the cerebellum, and angle of approach to the pineal gland (Fig. 1C–F). The distance between the pineal gland and each approach point was measured to establish the depth of the pineal gland for each route. The steepest angle between the orbitomeatal line and the line through the approach point and highest point in the tentorial surface was measured to define the slope of the tentorial surface of the cerebellum (Fig. 1C–F). The angle between the orbitomeatal line and the line through the approach point and the pineal gland was measured to define the approach angle (Fig. 1C–F).

The pineal gland is positioned inferior to the anterior part of the splenium, posterior to the third ventricle, above the collicular plate, anterior to the vein of Galen, and between the pulvinars. This deep region, also referred to as the posterior incisural space, is located posterior to the midbrain and corresponds to the region of the pineal gland and vein of Galen (Figs. 2 and 3).

The posterior incisural space is surrounded by neural tissue in all directions except posteriorly. The anterior wall is formed by the pineal gland, superior and inferior colliculi, lingula of the vermis, and superior cerebellar peduncle in order from rostral to caudal (Figs. 2A, 2D, 2E, and 3). The habenular commissure forms the upper and the posterior commissure the lower attachment of the gland to the posterior part of the third ventricle (Fig. 3B). The median part of the anterior wall inferior to the collicular plate is formed by the lingula of the vermis, the uppermost division of the vermis, and the lateral part by the superior cerebellar peduncle (Figs. 2E and 3A). The roof of the posterior incisural space consists of the inferior surface of the splenium, the terminal part of the crura of the fornices, and the hippocampal commissure, which courses between the crura (Figs. 2A, 2D, 2E, 3A, and 3B). The floor of the posterior incisural space is formed by the culmen of the vermis and central lobule medially and by the quadrangular lobules of the hemispheres laterally (Figs. 2D, 2E, and 3A). The posterior incisural space extends inferiorly into the cerebellomesencephalic fissure (Fig. 1F). The lateral wall is formed by the pulvinar, crus of the fornix, and the medial surface of the cerebral hemisphere below the splenium (Fig. 3B). The pulvinars are located just lateral to the pineal body (Fig. 3C). The crura of the fornix forms the lateral walls posterior to the pulvinars (Fig. 3B and C). The posterior part of the lateral wall is formed by the parahippocampal and dentate gyri (Fig. 3B and C).²⁴

Both the posterior cerebral artery and superior cerebellar artery and their branches course through the posterior incisural space. The posterior cerebral artery arises at the basilar bifurcation and encircles the midbrain, passing through the crural and ambient cisterns to reach the posterior incisural space, and usually bifurcates into its terminal branches, the calcarine and parieto-occipital arteries, near where it crosses above the free edge of the tentorium (Fig. 2D).^24,34 The superior cerebellar artery arises from the basilar artery near its apex, passes below the oculomotor nerve, and encircles the brainstem (Fig. 2A–C). The artery courses below the trochlear nerve and above the trigeminal nerve to enter the cerebellomesencephalic fissure (Fig. 2C). After leaving the fissure, the artery gives rise to the branches that supply the tentorial surface of the cerebellum (Fig. 2D and E). The superior cerebellar artery usually arises as a single trunk but may also arise as a duplicate trunk (Fig. 2A–C).²¹ The posterior cerebral arteries supply the structures above the level of the lower margin of the superior colliculus, and the superior cerebellar arteries supply the structures below the upper margin of the inferior colliculus.²⁴

The internal cerebral and basal veins and the vein of Galen and their tributaries pass through the posterior incisural space (Fig. 2A, B, D, and E). The internal cerebral vein originates from just behind the foramen of Monro and passes through the velum interpositum to enter the posterior incisural space where the vein joins its contralateral partner to form the vein of Galen (Fig. 2A, B, D, and E). The basal vein originates from the union of the anterior cerebral and deep Sylvian veins (Fig. 2B). The basal vein courses posteriorly between the midbrain and temporal lobe and reaches the posterior incisural space to empty into the internal cerebral vein or vein of Galen (Fig. 2A, B, D, and E).²² The anterior calcarine vein, also known as the internal occipital vein, drains the anterior part of the cuneus and lingula, and empties into the vein of Galen.²² The posterior pericallosal vein, which drains the posterior part of the cingulate gyrus, and passes around the splenium to empty into the vein of Galen or internal cerebral vein in the quadrigeminal cistern (Fig. 2D and E).²² The collicular veins drain the collicular plate and course backward to empty into the vein of the cerebellomesencephalic fissure, vein of Galen, or superior vermian vein (Figs. 4C, 4D, and 5).2 The pineal veins originate near the habenular trigone, and course backward superior or inferolateral to the pineal gland to empty into the internal cerebral vein or vein of Galen (Figs. 4C, 4D, and 5).² The vein of Galen courses below the splenium to empty into the straight sinus at the tentorial apex (Figs. 2A, 2B, 2D, and 2E). The junction of the vein of Galen with the straight sinus varies from being nearly flat if the tentorial apex is located below the splenium to forming a sharp angle if this apex is located above the level of the splenium, so that the vein of Galen must turn sharply upward to reach the straight sinus at the tentorial apex.²²

The depth of the pineal gland at the midline below the torcula was the shortest among the 4 routes (mean [± SD] 5.9 ± 0.4 cm, range 4.7–6.5 cm; Table 1). The depths of the 3 off-midline routes are almost identical, and all are more than 5 mm deeper than the approach along the midline (Table 1). The mean value of the slope of the tentorial surface in the midline approach was 35.2° ± 6.9° (range 21.0°–46.8°), the steepest of the mean slope values obtained for the 4 approaches. The angle decreased as the approach shifted laterally (Table 2). The mean value of the approach angle in the midline approach was 20.3° ± 5.8° (range 7.6°–30.1°), which is almost identical to that of the paramedian and lateral approaches, whereas the mean approach angle of the far-lateral approach was largest among of the 4 approaches (24.0° ± 3.3°, range 17.1°–29.6°; Table 3).

The infratentorial approach is directed between the posterior cerebral artery trunks above and the superior cerebellar artery trunks below (Figs. 4 and 5). The posterior cerebral artery trunks are largely supratentorial but overlap the incisural space from above, and the superior cerebellar artery trunk courses largely below the pineal gland in the cerebellomesencephalic fissure and on the tentorial surface. These vessels do not cross posterior to the pineal gland unless they are tortuous or elongated. The small neural branches of the posterior cerebral, superior cerebellar, and choroid arteries supplying the walls of the posterior incisural space, including the colliculi, thalamus, and pineal gland are at greater risk than the major arterial trunks during removal of pineal lesions.

Significant venous trunks are encountered at 2 levels in the infratentorial approach. The first is at the level of the veins draining the cerebellum that cross the infratentorial space to empty into the tentorial sinuses draining into the torcula and straight and transverse sinuses. The second is at the level of the quadrigeminal cistern where multiple large tributaries of the vein of Galen surround the gland (Figs. 4, 5, and 6).

After the dura mater is opened, the bridging veins crossing the infratentorial space between the tentorial surface of the cerebellum and the tentorial sinuses usually come into view (Fig. 6).²⁶ Dividing even a limited number of these veins may cause serious cerebellar swelling and complications such as hemorrhagic infarction because of the large areas drained.^1,7,19 In the midline approach, bridging veins directed to the torcula and straight sinus may need to be retracted or obliterated in order to reach the quadrigeminal cistern and gland. Upon reaching the quadrigeminal cistern, the tributaries of the vein of Galen from the superior vermis and cerebellomesencephalic fissure are encountered directly below the pineal gland and may block the exposure of the gland along the midline (Fig. 4A and B).^18,23,26 In the off-midline approaches, the superior hemispheric veins, which drain the anterior part of the tentorial cerebellar surface, and the inferior hemispheric veins from the suboccipital surface, which ascend and cross the margin of the occipital and tentorial cerebellar surfaces, frequently join to form bridging veins that drain a large part of the cerebellum. These large bridging veins commonly drain into the tentorial sinus in the intermediate third of the tentorium along the lateral off-midline infratentorial route (Fig. 6B–F).^15,26 These bridging veins would be less likely to be encountered in the paramedian and far-lateral off-midline approaches than in the lateral route. However, there is considerable variability in the site of these bridging veins, and the off-midline routes are most likely to allow their preservation.^17,26,29 Selecting from among the off-midline routes may avoid or reduce the need for venous sacrifice.^17,29

Dissecting the arachnoid mater surrounding the quadrigeminal cistern exposes the second tier of veins formed by the tributaries of the vein of Galen, which block access to the pineal region. These tributaries of the vein of Galen, including the superior vermian and vein of the cerebellomesencephalic fissure, approach the vein of Galen from the inferior direction in the midline, and others like the internal cerebral and basal vein reach the vein of Galen from near the midline superiorly (Figs. 2A, 2B, 2D, 2E, 4, and 5). In the midline approach, the superior vermian and cerebellomesencephalic veins are aligned one above the other below the pineal gland and may need to be retracted or sacrificed if the approach is directed strictly along the midline (Figs. 4 and 5). Shifting the approach slightly laterally off the midline may avoid the need for sacrifice of these veins. An advantage of the off-midline approaches, as they move farther laterally, is that they open the angle between the galenic tributaries exiting the cerebellomesencephalic fissure below and the internal cerebral veins from above and provide access to the gland, often without venous sacrifice except for possibly the small tributaries, such as the pineal vein, draining directly from the pineal gland and adjacent neural structures (Figs. 4 and 5).

It is well established that in the midline approaches the prominence of the cerebellar culmen and quadrangular lobules limits the working angle available for instruments and interferes with adequate illumination at the pineal gland’s depth and that the depth and slope of the upper surface of the cerebellum through each route can affect surgical maneuverability. However, these differing depths and slopes have not been previously established. We found that the differences in depth among off-midline routes are only a few millimeters, although the off-midline routes are more than 5 mm deeper than the midline approach, which provides the shortest approach. On the other hand, the slope of the upper cerebellar (tentorial) surface of each route changed dramatically as the approaches shifted from medial to lateral. Among infratentorial approaches, the midline route is approximately twice as steep as the lateral and far-lateral routes. We also found that the slope of the cerebellar (tentorial) surface in the midline and paramedian routes is larger than the angles of these approaches. In contrast, the slope of the cerebellar (tentorial) surface in the lateral and far-lateral routes is smaller than the angles of these approaches. Thus, midline and paramedian routes require greater retraction of the cerebellum to approach the pineal gland than do the lateral and far-lateral routes. The off-midline routes, especially through the intermediate or lateral third of the tentorium, require less retraction of the cerebellum to reach the pineal gland. However, based on our previous studies, the routes through the intermediate third carry a higher risk of needing to sacrifice bridging veins from the upper cerebellar surface to the tentorial sinuses.^15,26

Supracerebellar infratentorial approaches are commonly selected for lesions of the pineal gland.^6,10,13,32 The traditional infratentorial approach to the pineal gland is along the midline below the torcula,²⁵ but it requires greater cerebellar retraction than off-midline approaches due to the height of the culmen of the vermis. The off-midline infratentorial supracerebellar approaches, namely the paramedian, lateral, and far-lateral routes, have been developed to minimize the need for cerebellar retraction and facilitate exposure of different parts of the posterior incisural space.^{8,12,14,17,19,20,28,30,31} The paramedian and lateral routes have been selected for pineal lesions, and the far-lateral route has been selected for lesions in posterolateral mesencephalon rather than the pineal gland.^14,30 Komune et al.¹¹ reported the far-lateral supracerebellar infratentorial approach to the inferior colliculus, which included a lateral suboccipital craniotomy without tentorial incision. In that study, we found that the pineal gland could also be accessed through a far-lateral approach directed adjacent to the transverse and sigmoid sinuses. The off-midline approaches also have the advantage of providing a more direct view of the structures along the anterior wall of the cerebellomesencephalic fissure, such as the collicular plate and the fourth cranial nerve. A disadvantage of the more lateral approaches is that the pulvinar may hide part of the pineal region and prevent access to lesions extending forward in the midline from the pineal gland between the 2 halves of the thalamus in the roof of the third ventricle.

The trunks of the superior cerebellar and posterior cerebral arteries supplying the pineal region are usually not at as great a risk in an approach to the pineal region as the veins because these arteries do not cross posterior to the pineal gland as do the veins that are at greater risk in approaches to the pineal region. The main arterial risk is to the small perforating branches of the posterior cerebral, superior cerebellar, and choroidal arteries that enter the borders of the quadrigeminal cistern.

Sacrificing the superior vermian, hemispheric, or vermian bridging veins has been considered relatively safe.^5,6,10,20 Kodera et al.¹⁰ reported that these veins can be sacrificed if the collateral circulation of each vein is preserved. However, Page et al.¹⁸ reported a case of severe cerebellar swelling after sacrifice of the hemispheric and vermian bridging veins through the midline approach. Jakola et al.⁷ reported that sacrificing even a limited number of tentorial bridging veins may cause venous infarction or hemorrhage in the cerebellum.¹⁴ Although the anatomical relationship of the venous system of the cerebellum and tentorium has been well investigated, it is impossible to determine which veins can be sacrificed before or during an operation.^15,16,23,26 Even preoperative venography identifies only half the number of these veins seen in a cadaveric study.⁴ To avoid hazardous complications, the goal of limiting sacrifice of bridging veins to the smallest number and to veins of the smallest size should be one consideration in directing the approach. Commonly, these smaller veins join to form bridging veins entering the tentorial sinuses, and if occluded may sacrifice large areas of cerebellar drainage. Brain retraction combined with venous sacrifice entails a higher risk of brain damage than either alone.⁹ To avoid hazardous complications, reducing the need for brain retraction should be one consideration in directing the approach. Endoscopic supracerebellar infratentorial approaches require less cerebellar retraction and may aid in accessing pineal lesions without sacrificing bridging veins.

A common surgical exposure for a pineal lesion is through a vertical suboccipital midline incision. With this incision, the bony exposure below the transverse sinus and adjacent to the midline can be extended laterally to access the paramedian and adjacent lateral approach on either side. Another common approach for accessing the far-lateral part of the upper surface of the cerebellum is the retrosigmoid approach, through which the bone exposure can be extended medially to take advantage of a lateral approach, depending on the venous architecture related to the veins entering the tentorial sinuses. In addition, the retrosigmoid incision can be shifted medially away from its usual position centered below the asterion for the para median and lateral approaches. Another approach taking advantage of the paramedian, lateral, and far-lateral approaches on one side is a horseshoe-type flap that extends from the mastoid area upward along the superior nuchal line to the torcula and then downward in the midline. Most pineal tumors are accessed through a midline incision. There are, however, distinct advantages to having access to the off-midline approaches, which reduce the possible need for sacrifice of veins at the level of the tentorial bridging veins and the quadrigeminal cistern.

The endoscopic infratentorial supracerebellar approach has been applied for lesions such as pineal cysts, epidermoids, and astrocytomas,^3,27 and it is considered an alternative to the microscopic approaches to the pineal gland.³³ Recently, Hasan et al.³³ investigated the endoscopic and microsurgical supracerebellar infratentorial approaches quantitatively by measuring surgical freedom. They reported that their lateral route, which we call far-lateral in the present study, provides the largest surgical exposure and the most vertical attack angle, and the midline route provides the largest horizontal angle when approaching the pineal gland through the endoscopic supracerebellar infratentorial approaches.³³ Endoscopic supracerebellar infratentorial approaches require less cerebellar retraction and may aid in accessing pineal lesions without sacrificing bridging veins (Figs. 4B, 4D, 5B, and 5D).

The supracerebellar infratentorial approaches, including the median, paramedian, lateral, and far-lateral routes, provide access for the removal of most tumors involving the pineal gland. Understanding the difference among supracerebellar infratentorial routes, including the differences in depth and angle of the approach, and selecting the route that requires division of the least number of bridging veins at the level of both the infratentorial space above the cerebellum and at the quadrigeminal cistern may reduce postoperative complications. Endoscopic supracerebellar infratentorial approaches may also be helpful in approaching the pineal gland, especially in defining a route that minimizes venous sacrifice.

Contributors: Satoshi Matsuo, MD, Serhat Baydin, MD, Abuzer Güngör, MD, Koichi Miki, MD, Noritaka Komune, MD, PhD, Ryota Kurogi, MD, Koji Iihara, MD, PhD, and Albert L. Rhoton, Jr, MD

Content from Matsuo S, Baydin S, Güngör A, Miki K, Komune N, Kurogi R, Iihara K, Rhoton AL, Jr. Midline and off-midline infratentorial supracerebellar approaches to the pineal gland. J Neurosurg 2017;126:1984–1994. doi.org/10.3171/2016.7.JNS16277.

The Neurosurgical Atlas is honored to maintain the legacy of Albert L. Rhoton, Jr, MD.