ANATOMY

Surgical Anatomy and Technique

MICROSURGICAL ANATOMY OF THE SAFE ENTRY ZONES ON THE ANTEROLATERAL BRAINSTEM RELATED TO SURGICAL APPROACHES TO CAVERNOUS MALFORMATIONS
Rodolfo J. Recalde, M.D.
Universidad de Buenos Aires, Hospital Nacional Prof. A. Posadas, Buenos Aires, Argentina

Eberval G. Figueiredo, M.D.

Department of Neurological Surgery, University of So Paulo School of Medicine, So Paulo, Brazil

Evandro de Oliveira, M.D., Ph.D.

Department of Neurological Surgery, State University of Campinas, Instituto de Cincias Neurolgicas, So Paulo, Brazil Reprint requests: Evandro de Oliveira, M.D., Ph.D., Instituto de Cincias Neurolgicas, Praa Amadeu Amarau, 27, 5 andar, CEP 01327-010, So PauloSP, Brazil. Email: icne@uol.com.br Received, February 22, 2007. Accepted, July 10, 2007.

OBJECTIVE: To study the microanatomy of the brainstem related to the different safe entry zones used to approach intrinsic brainstem lesions. METHODS: Ten formalin-xed and frozen brainstem specimens (20 sides) were analyzed. The white fiber dissection technique was used to study the intrinsic microsurgical anatomy as related to safe entry zones on the brainstem surface. Three anatomic landmarks on the anterolateral brainstem surface were selected: lateral mesencephalic sulcus, peritrigeminal area, and olivary body. Ten other specimens were used to study the axial sections of the inferior olivary nucleus. The clinical application of these anatomic nuances is presented. RESULTS: The lateral mesencephalic sulcus has a length of 7.4 to 13.3 mm (mean, 9.6 mm) and can be dissected safely in depths up to 4.9 to 11.7 mm (mean, 8.02 mm). In the peritrigeminal area, the distance of the fth cranial nerve to the pyramidal tract is 3.1 to 5.7 mm (mean, 4.64 mm). The dissection may be performed 9.5 to 13.1 mm (mean, 11.2 mm) deeper, to the nucleus of the fth cranial nerve. The inferior olivary nucleus provides safe access to lesions located up to 4.7 to 6.9 mm (mean, 5.52 mm) in the anterolateral aspect of the medulla. Clinical results conrm that these entry zones constitute surgical routes through which the brainstem may be safely approached. CONCLUSION: The white ber dissection technique is a valuable tool for understanding the three-dimensional disposition of the anatomic structures. The lateral mesencephalic sulcus, the peritrigeminal area, and the inferior olivary nucleus provide surgical spaces and delineate the relatively safe alleys where the brainstem can be approached without injuring important neural structures.
KEY WORDS: Brainstem, Brainstem surgery, Cavernous malformation, Safe entry zones, Surgical anatomy, Surgical approaches, White ber dissection
Neurosurgery 62:ONS9ONS17, 2008
DOI: 10.1227/01.NEU.0000297062.52433.3F

www.neurosurgery-online.com

avernous malformations of the central nervous system account for 8 to 15% of all vascular malformations (12, 13). Their occurrence within the brainstem is estimated to be between 9 and 35%, and their surgical treatment poses several risks. The brainstem presents a dense concentration of nuclei and bers, and their unintentional manipulation may produce neurological morbidity. The presence of functionally intact parenchyma that are in close proximity to the lesions is responsible for such signicant morbidity. Criteria for surgical indications include a symptomatic lesion that reaches a pial or ependymal surface and that may be approached without the need to traverse eloquent brainstem tissue (12, 13). However, intrinsic symptomatic lesions may be reached through small neurotomies in safe entry zones on

the brainstem surface (9, 13, 14, 19, 20). These zones represent small regions in which the brainstem may be incised with relative impunity and correspond to areas where critical neural structures are sparse and no perforating arteries are encountered. The elements of the internal anatomy are related to topographic structures on the brainstem surface. Thus, a profound knowledge of both the external and internal anatomy of the cranial motor nuclei and fibers is necessary to optimize the surgical approaches and preserve functionally important brainstem structures. Previous reports have studied safe entry zones in the posterior aspect of the brainstem (1, 2, 9, 17). However, no anatomic assessments have been performed to study safe entry zones in its anterolateral aspect. Many authors have rou-

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tinely used anatomic landmarks such as the lateral mesencephalicum sulcus (LMS), peritrigeminal area, and olivary body as safe entry zones on the anterolateral surface of the brainstem to approach brainstem cavernous malformations (BCMs). In this study, we performed an evaluation of the intrinsic anatomy of the brainstem using the white ber dissection technique as related to these safe entry zones. Using this methodology, the successive layers of the intrinsic anatomy of the brainstem are peeled away, and the anatomic relationships are consecutively revealed.

MATERIALS AND METHODS

Ten fresh formalin-xed and frozen brainstems were analyzed (20 halves). Anatomic characteristics of the extrinsic elements as well as white ber dissection using Ludwig and Klingers technique (11) were used to study the intrinsic microsurgical anatomy of the brainstem. Magnication from 3 to 40 was used. Once the pia-arachnoid was removed, we proceded with dissection, using microsurgical tools and wooden tongue depressors as spatulas. The anterolateral mesencephalon was dened as the portion of the midbrain located ventral to the LMS, whereas the two anterior quadrants and the part the medulla ventral to the retro-olivary sulcus dened the anterolateral surface of the pons and medulla, respectively. Anatomic landmarks easily recognized on the brainstem surface were selected in the mesencephalon (LMS), pons (peritrigeminal area), and medulla (olivary body). The consecutive layers of the intrinsic anatomy of the brainstem were peeled away to successively expose and allow description of the anatomic relationships. Additionally, surgically relevant measurements were obtained on each level studied.

FIGURE 2. Cross-section of the midbrain showing the cerebral peduncles (CP) separated from the tegmentum by the substantia nigra (SN). The medial lemniscus (ML) is located posteriorly to the SN. The intrinsic trajectory of the third cranial nerve is dissected bilaterally. There is an alley between the SN and the ML that can be safely approached through the LMS before the optic nerve bers may be damaged. The black line represents the distance from the LMS to the intrinsic CN III bers.

FIGURE 3. The descending fibers have been cut at the level of CN V and resected rostrally. The SN as well as the intraneural projection of CN III may be seen. The superior and inferior cerebellar peduncles have been cut. The CN V trajectory up to its nucleus may be appreciated. The white line represents the distance from the LMS to the fibers of CN III.

RESULTS
Mesencephalon
After performing a myelotomy in this sulcus, we proceeded deeper in the disection, in the direction of the emergence of CN III. The dissection passes through an alley limited laterally by the substantia nigra and medially by the medial lemniscus (Figs. 2 and 7). The red nucleus and the decussation of the superior cerebellar peduncle are reached as the white fiber dissection goes FIGURE 4. Ventral view showdeeper. The fibers of CN III ing the specimen depicted in cross this alley in an almost Figure 3. The crus cerebri (CC) perpendicular fashion, from have been dissected and elevated; the red nucleus to the subthe relationship of CN III with the stantia nigra, and this point SN may be observed. The black corresponds to the anterior line corresponds to the distance limit of a safe surgical from the LMS to the bers of CN III. approach (Figs. 2, 3, and 4). Going further might damage the CN III bers. The depth of this corridor is shown in Table 1. The measurements on the mesencephalon were obtained at the level of the LMS. The LMS extends 7.4 to 13.3 mm (9.6 1.41 mm) (Figs. 2, 3, and 4; Table 1) from the medial geniculate body located superiorly to the interpeduncular sulcus. A sec-

Mesencephalon
FIGURE 1. The lateral mesencephalic sulcus (LMS) and its relationship with adjacent neural structures are shown. The LMS is located in the posterior aspect of the mesencephalon between the cerebral peduncles and the collicular area. It extends longitudinally from the medial geniculate body superiorly and up to the pontomesencephalic sulcus inferiorly. CN, cranial nerve. The length of the LMS (Fig. 1) and the distance between the pial surface of the LMS to the point where Cranial Nerve (CN) III penetrates the substantia nigra were measured (Figs. 2, 3, and 4).

Pons

After resection of the transverse fibers, the distance between the fth cranial nerve and the pyramidal bers as well as the distance between the apparent origin of CN V up to its pontine nucleus were measured (Figs. 3, 4, and 5). The width of the descending bers was evaluated at three different points: at the level of the pontomesencephalic sulcus, at the level of CN V, and at the level of the pontomedullary sulcus (Figs. 3 and 4).

Medulla
In the medulla, the distance of the inferior olivary nucleus from the pia mater to the point where the white bers enter and exit the nucleus was evaluated (Fig. 6). In addition, the craniocaudal, transverse, and anterodorsal diameters of the olivary bodies were assessed.

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ond measurement in the mesencephalon from the LMS to the rootlets of CN III might be found in the depth of the mesencephalon. This distance varied between 4.9 and 11.7 mm (8.2 1.76 mm) (Figs. 2 and 3). According to these data, the LMS offers a mean of 9.6 mm that may be opened, and the surgeon may dissect 8.2 mm deeper without damaging CN III (Fig. 4). However, the lower limit of dissection (4.9 mm) may also be considered as the safest distance when approaching this region (Table 2).

FIGURE 5. Cross-section showing the pons at the level of CN V. The peritrigeminal area (PtrA) is depicted medially to the bers of CN V, laterally to the pyramidal tract (PT), and ventrally to the motor nucleus (MN CN V) and sensory nucleus (SN CN V) of CN V.

Pons
As one proceeds with the myelotomy in the peritrigeminal area, CN V may be seen emerging from the pons as a compact

group of bers, and continuing its trajectory toward its nucleus (Fig. 5). As the dissection of the transverse bers of the middle cerebellar peduncle progresses, the bers of CN V are revealed and might be followed to the nucleus (Figs. 3 and 4). FIGURE 7. Dissection at the level Further dissection consecuof the LMS. The ML bers may be tively revealed the nucleus seen posteriorly and the CC venof CNs VI, VII, and VIII trally. located posteriorly and medially to the nucleus of CN V. The descendent trajectory of the bers of CNs VI, VII, and VIII might be disclosed to reach the pontomedullary sulcus. These bers are located posterior to CN Vs nucleus. The pyramidal tract was also dissected, and the measurements were obtained (Figs. 8 and 9). The distance between the pyramidal bers and CN V ranged between 3.8 and 5.6 mm (4.64 0.68 mm). Therefore, one can access lesions located medial to CN V by up to 4.64 mm without injuring the pyramidal bers. The dissection may be carried out 9.5 to 13.1 mm (11.2 1.29 mm) deeper to the nucleus of CN V (Figs. 8 and 9) (Table 1). However, the lower limits of dissection (3.8 and 9.5 mm) may also be considered as the safest distances when approaching this region (Table 2).

Medulla
In the medulla, transverse sections were performed through the inferior olivary nucleus at the most protruding point in the anterior aspect. Its craniocaudal axis averaged 13.5 mm, the transverse axis 7.0 mm, and anterodorsal axis 2.5 mm. Our measurements revealed that the length from the pial surface of the olivary body to the point where the different groups of bers enter the olivary body ranged between 4.7 and 6.92 mm (5.52 0.5 mm) (Fig. 6). However, the lower limit of dissection (4.7 mm) may be also considered as the safest distance to approach this region (Table 2).

FIGURE 6. Cross-section showing the medulla at the level of the inferior olivary nucleus (ION). The olivary bodies are surrounded by eloquent anatomic structures ventrally, dorsally, and medially. The PT is located anteriorly to the olivary body, at the ventral surface of the brainstem. The PT is separated from the olivary body by intrinsic bers of CN XII. The olivary body is bordered medially by the medial lemniscus and the intrinsic bers of CN XII and posteriorly by the reticular, vestibulospinal, and tectospinal tracts (TT). Dorsally, the olivary bodies are limited by the spinocerebellar tract, descending trigeminal tract, and spinothalamic tract (TST). The nucleus ambiguous (NA) and dorsal motor nucleus (DMN) of CN X lie farther posteriorly. The continuous line illustrates the distance from the pia to the entry and exit points of the bers in the ION (hilum). This intricate architecture implies that the safest entry zone in the anterolateral surface of the medulla is the ION. HN, hypoglossal nucleus; MLF, medial longitudinal fascicle.

TABLE 1. Measurements in the mesencephalon and ponsa Measurement LMS length LMS to CN III Descending bers of pons Mean 9.6 8.02 12.2 8.84 5.6 11.2 4.64 SD (mm) 1.41 1.76 0.97 0.98 0.95 1.29 0.68 Range (mm) 13.37.4 4.911.7 10.813.7 7.510.6 4.27.5 9.1513.1 3.15.6

Superior one-third Medial one-third Inferior one-third

Deep CN V CN V to PT
a

SD, standard deviation; LMS, lateral mesencephalic sulcus; CN, Cranial Nerve; PT, pyramidal tract.

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TABLE 2. Summary of the brainstem safe entry zones and their working distancesa Brainstem level Midbrain Pons Medulla
a

Safe entry zones Lateral mesencephalic sulcus Peritrigeminal area Olivary body

Minimum working distance (mm) 4.9 9.5 4.7

Maximum working distance (mm) 11.7 13.1 6.92

Mean 8.2 11.2 5.52

SD (mm) 1.76 1.29 0.5

SD, standard deviation.

FIGURE 8. Anterior view of the brainstem. The transverse fibers have been dissected away and CN V as well as the PT can be observed. CNs VII and VIII present an inferior trajectory coming through the pontomedullary sulcus. The white line shows the distance from the PT to the bers of CN V. The gray line indicates the distance of the intrinsic trajectory of CN V from the nucleus to the surface of the pons.

DISCUSSION

Surgery of the BCM represents a formidable surgical challenge. This region shares the passage of afferent and efferent bers, the reticular system, cranial nerves, and extrapyramidal nuclei, and their surgical manipulation may confer high levels of surgical morbidity (2, 1214, 18). Several clinical series have reported acceptable rates of surgical morbidity and mortality for BCMs in the brainstem (9, 10, 13, 14, 17, 20). As more experience has been acquired in treating these lesions, it has become apparent that surgical resection is possible with acceptable risks of postoperative morbidity and mortality when compared with the higher risks of neurological deficits that have been demonstrated after multiple bleedings in this delicate region (2, 12). A better understanding of the surgical anatomy allied with more accurate preoperative studies, including magnetic resonance imaging and frameless stereotactic systems, are factors that have contributed to the contemporary management of BCMs. Surgical treatment is a valuable option for symptomatic patients, particularly when the lesion abuts the pial or ependy-

FIGURE 9. Lateral view showing the brainstem after white ber dissection. The PT without the transverse bers as well as the intraneural trajectory of CN V and its nucleus are depicted. The inferior cerebellar peduncle has been cut and, medial to it, the trapezoid body. SCP, superior cerebellar peduncle; ICP, inferior cerebellar peduncle; DN, dentate nucleus; TT, tectospinal tract.

mal surface. In these cases, the lesion itself provides the surgical access route. Conversely, when only a thin layer of parenchyma separates the lesion from the surface, excision may also be considered if such a rim is situated along the path of a safe entry zone. These areas correspond to regions where critical neural structures are sparse and no perforating arteries are present. Additionally, a safe entry zone should provide satisfactory surgical room and should be located at an appropriate distance from vital structures. With a clear mental image of the internal architecture of the brainstem, a safe entry zone may be used to approach intrinsic lesions, thereby avoiding more perilous areas. The anatomic studies related to surgical access to the brainstem are mostly related to approaches through the oor of the fourth ventricle (1, 2, 10, 12). Numerous reports have described the different cranial base approaches used to reach different regions of the brainstem (12, 15). Although safe entry zones in the anterolateral aspect of the brainstem have been described and used by different authors (1, 2), to the best of our knowledge, no study has practically evaluated the intrinsic microsurgical anatomy of the brainstem related to the safe entry zones on its anterolateral aspect. A comprehensive analysis of the intrinsic anatomy of the brainstem provides a better knowledge of these safe entry areas and their relationships with eloquent internal anatomic structures. The brainstem is densely packed with many vital structures such as long ascending and descending pathways and specic nuclear groups. The core of the brainstem is occupied by the reticular formation. In general, the internal architecture may be divided into two functional regions. During embryogenesis, the neural tube is divided into a dorsal sensory portion (the alar plate) and a ventral motor portion (the basal plate) by a longitudinal indentation along the wall of the neural tube, the sulcus limitans. In maturity, this sulcus continues to be recognizable in the walls of the third and fourth ventricles and the cerebral aqueduct, and it still demarcates a border between sensory and motor structures. The safe entry zones analyzed in this article correspond roughly to the supercial projection of the transition between these two zones. In these regions, the distances between eloquent structures within the brainstem are the largest and provide an optimized surgical working space.

Mesencephalon
The midbrain is limited cranially from the diencephalon by the sulcus between the optic tracts and the cerebral pedun-

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cles, and separated from the pons by the pontomesencephalic sulcus. It is formed by the cerebral peduncles, the tegmentum, and the tectum. A narrow channel, the aqueduct of Sylvius, traverses the midbrain from top to bottom and divides it into two portions (Fig. 2). The dorsal part is formed by the tectum and the ventral part by the cerebral peduncles. The tegmentum, which is predominantly cellular, is separated from the peduncles by the substantia nigra. The substantia nigra delineates two sulci on the surface of the midbrain: the LMS and the medial sulcus of the cerebral peduncles (Fig. 2). These two sulci indicate the limits between the peduncles and tegmentum on the brainstem surface. The LMS is located in the posterior aspect of the mesencephalon, between the crus cerebri and the collicular area (Fig. 1). It extends vertically from the medial geniculate body superiorly, to the pontomesencephalic sulcus inferiorly. The length of this sulcus is described in Table 1. Lateral to the LMS, the bulging made by the parieto-occipitotemporopontine fibers may be identied. Posteromedially, the lateral lemniscus and the brachium conjunctivum are located inferior and superior, respectively, to the LMS (Figs. 2 and 7). Incision in this entry zone provides a working space that is limited ventrally by the substantia nigra, dorsally by the medial lemniscus, and medially by the fibers of CN III (Figs. 2 and 3). The surgeon may select an extension of nearly 1.0 cm (range, 7.413.3 mm) to do the myelotomy and work up to 8.2 mm deeper (range, 4.911.7 mm) without injuring the fibers of CN III and keeping a comfortable distance from the motor tracts. However, the lower limit of dissection (4.9 mm) may also be considered as the safest distance when approaching this region. Additionally, this entry zone route is located in a border area of the anterolateral and anteromedial vascular areas as described by Duvernoy (3). It provides a line of access in a hypovascularized region without compromising any important perforator (Fig. 10).

Pons
The pons is limited superiorly by the pontomesencephalic sulcus and inferiorly by the pontomedullary sulcus. Its ventral aspect has a convex shape from side to side and from top to bottom and presents horizontal striae resulting from the presence of many transverse bers (Figs. 5 and 11). These bers converge ventrally to form a voluminous bundle, the medial cerebellar peduncles, from which emerge the roots of the trigeminal nerve. The apparent origin of CN V is considered to be the limit between the pons and the medial peduncles (Figs. 35 and 11). The corticonuclear and pyramidal tracts may be projected onto the surface of the pons. Two imaginary lines project the trajectory of the motor tracts onto the surface of the brainstem. The rst line links the most medial point of the pontomesencephalic sulcus to the point where the medial border of the pyramid and the pontomedullary sulcus meet (Fig. 12). The second line links

the intersection between the lateral aspect of the crus cerebri and the pontomesencephalic sulcus to the point where the lateral border of the pyramid in the medulla and the pontomedullary sulcus meet (Fig. 12). The safe area may be FIGURE 10. Vascular topogradened in a similar fashion. phy showing the mesencephalon This surgical area, called the with the anteromedial area in peritrigeminal area, has a tridark gray, the anterolateral area angular shape with the base in white, the lateral area in gray, located inferiorly. The medial and the posterior area in light limit is formed by the pyramgray. The relative hypovascularidal tract, the base by the ponized area corresponds to the LMS tomedullary sulcus from the in the surface. lateral aspect of the pyramid to the occulus, and the lateral limit by a line that goes from Point A and passes through CN V. This triangle is wider in the base and stretches as it extends superiorly (Fig. 12). The oor of the triangle is formed by the most posterior bers of the middle cerebellar peduncle. Myelotomy in this area carFIGURE 11. Brainstem anterior ries a lower risk of injury to aspect. P, pyramid. any vital structure because one will find the transverse bers of the middle cerebellar peduncle. The nuclei of CNs VI, VII, and VIII are located posterior and medial to the nucleus of CN V. The trajectory of bers of CNs VI, VII, and VIII has a descendent direction toward the pontomedullary sulcus. The transverse bers of the FIGURE 12. On the left side pons are mostly horizontal or (horizontal lines), the PT may be slightly oblique; thus, myeloprojected onto the surface of the tomies in the anterolateral pons. On the right side (vertical aspect of the pons should be lines), the peritrigeminal area performed in a horizontal may be projected with the pondirection to preserve the tomedullary sulcus as the inferior fibers. This area provides a limit, the projection of the pyramsurgical window that measidal tract medially, and a tangenures 4.64 mm (range, 3.85.6 tial line passing posterior to CN V laterally. mm) horizontally and 11.2 mm (range, 9.513.1 mm) vertically. However, the lower limits of dissection (3.8 and 9.5 mm) may be also considered as the safest distances when approaching this region.

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Medulla
The medulla has paired elongated elevations on its ventral aspect, the pyramids, separated by a longitudinal groove, the anterior median ssure. Oval protuberances, the olivary bodies, are found lateral to the pyramids and to the anterolateral sulcus. Ventral to the olivary bodies, CN XII originates from the anterolateral sulcus. The posterolateral sulcus on the dorsal margin of the olivary bodies gives rise to the rootlets of the accessory nerve, whereas CNs IX and X emerge from the pontomedullary sulcus, lateral to the olivary bodies. The medulla has an oval shape with a hilum located in its inferomedial aspect (17). It has afferent bers, mostly from the reticular system, and gives rise to axons that cross the midline and course toward the contralateral cerebellum through the inferior cerebellar peduncle, forming the olivocerebellar bers. The afferents emerge from the reticular formation and pass through the central tegmental fascicle. The medulla also has connections with the spinal cord and the cerebrum through the central tegmental fascicle. The specic function of the inferior olivary nucleus is controversial, and it is thought to be related to some of the functions of the cerebellum. The olivary bodies are limited ventrally by the corticospinal tract, medially by the medial lemniscus and fibers of the hypoglossal nerve, and dorsally by parasympathetic nuclei and bers (Fig. 6). A group of bers formed by the reticular and vestibulospinal tracts are placed posterior to the olivary body, and the bers of the medial and lateral spinocerebellar tract may be found dorsal to them. Between these tracts, the bers of CN X are encountered coursing toward the retro-olivary sulcus. The reticular and vestibulospinal tracts are interposed between the inferior olivary nucleus and the CN X nucleus. This architecture of the medulla makes a surgical approach quite dangerous because these important structures are densely concentrated in such a small area. There is no evidence demonstrating that isolated lesions of the olivary body may cause permanent decits. Hence, the retro-olivary sulcus corresponds to the safest approachable area in the anterolateral surface of the medulla. The olivary body offers a surgical space of approximately 13.5 mm in the craniocaudal axis, 7 mm in the transverse diameter, and 2.5 mm in its anterodorsal axis. Our data suggest that the surgeon can reach lesions located in the anterolateral aspect of the medulla up to two-thirds of its transverse diameter.

rience in using these techniques. Additionally, frameless stereotactic systems and physiological monitoring may assist in surgical resection and reduce postoperative morbidity.

CONCLUSION
Intrinsic BCMs constitute a formidable surgical challenge, and their approach has been considered a journey to terra incognita (16). It requires a meticulous technique and a perfect understanding of the inherent anatomy of the brainstem. Although such anatomy may suffer distortion after a hemorrhage, it is still important to recognize areas where the initial myelotomy will provide enough surgical working space, will not damage vital structures, and will not compromise perforator vessels. This study has demonstrated that a signicant extent of the brainstem anatomy may be safely accessed through three entry zones. Use of these accesses does not damage any vital structures located deeper below or perforators, and these entry zones afford satisfactory surgical working space because the local arrangement of the brainstem anatomy provides adequate distances between important neural elements. In the mesencephalon, the LMS confers access to lesions in its posterior twothirds. In the pons, the peritrigeminal area provides a satisfactory approach for anterolateral and deep lesions located up to 10 mm from the pial surface. In the medulla, the olivary nucleus offers an adequate entry zone to reach lesions in its anterolateral aspect. The mean depth that can be safely accessed through the olivary body with a low morbidity rate is 5.52 mm. White fiber dissection improves the understanding of the microsurgical anatomy of the brainstem and offers a better comprehension of this complex structure. This knowledge and its clinical application may help to reduce the surgical morbidity associated with BCMs.

REFERENCES
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Surgical Considerations
The safe entry zones studied here are usually approached using standard surgical accesses (48). The LMS may be approached through subtemporal or supracerebellarinfratentorial routes. The peritrigeminal area may be reached through a subtemporal, retrosigmoid, pretemporal transcavernous approach or through transpetrosal techniques, whereas the olivary bodies are usually approached through a far lateral transcondylar technique. Preoperative magnetic resonance imaging studies may help to select the appropriate approach, which will also depend on the surgeons familiarity and expe-

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9. Fritschi JA, Reulen HJ, Spetzler RF, Zabranski JM: Cavernous malformations of the brain stem. Acta Neurochir (Wien) 130:3546, 1994. 10. Kyoshima K, Kobayashi S, Gib H, Kuroyanagi T: A study of safe entry zones via the floor of the fourth ventricle for brain-stem lesions. J Neurosurg 78:987993, 1993. 11. Ludwig E, Klingler J: Atlas Cerebri Humani. Basel, S. Karger, 1956. 12. Porter RW, Detwiler PW, Spetzler RF: Surgical technique for resection of cavernous malformations of the brain stem. Oper Tech Neurosurg 3:124130, 2000. 13. Porter RW, Detwiler PW, Spetzler RF, Lawton MT, Baskin JJ, Derksen PT, Zabramski JM: Cavernous malformations of the brainstem: Experience with 100 patients. J Neurosurg 90:5058, 1999. 14. Samii M, Eghbal R, Carvalho GA, Matthies C: Surgical management of brainstem cavernomas. J Neurosurg 95:825832, 2001. 15. Sarma S, Sekhar LN: Brain stem cavernoma excised by subtemporalinfratemporal approach. Br J Neurosurg 16:172191, 2002. 16. Spetzler RF: Cavernous malformations of the brainstem. Presented at the Brazilian Congress of Neurosurgery, Florianopolis, Santa Catarina, Brazil, September 1419, 2006. 17. Strauss C, Lutjen-Drecoll E, Fahlbusch R: Pericollicular surgical approaches to the rhomboid fossa. Part I. Anatomical basis. J Neurosurg 87:893899, 1997. 18. Testut L: Human Anatomy Treaty [in Spanish]. Barcelona, Salvat, 1964, pp 689692. 19. Wang CC, Liu A, Zhang J, Sun B, Zhao Y: Surgical management of brain-stem cavernous malformations: Report of 137 cases. Surg Neurol 59:444454, 2003. 20. Ziyal IM, Sekhar LN, Salas E, Sen C: Surgical management of cavernous malformations of the brain stem. Br J Neurosurg 13:366375, 1999.

Acknowledgments
We thank Pushpa Deshmukh, Ph.D. for help with editing the manuscript and Israel M. de Oliveira for excellent technical assistance.

COMMENTS

s our understanding of the microsurgical anatomy of the brainstem improves, neurosurgeons are reconsidering the treatment of lesions once considered inoperable. This article represents a valuable complement to available clinical experience with brainstem cavernous malformations. To be sure, the corridor created by the cavernoma represents the safest entry point (1). However, when lesions do not abut the pia, other corridors need to be considered. In our experience, the lateral entry points between the motor and sensory nuclei described in this manuscript are well tolerated. An important limitation of this study is that the unique anatomy of a brainstem with pathological changes cannot be modeled in a cadaveric analysis. Cranial nerve nuclei and tracts are often distorted. Consequently, the limits of dissection presented in this article represent rough estimates of safe zones and should not be applied strictly. In the future, magnetic resonance imaging tractography may provide detailed information about the location of white matter tracts and assist with preoperative planning for brainstem lesions. We look forward to a follow-up review of the groups clinical experience. Andrew Little Pushpa Deshmukh Robert F. Spetzler Phoenix, Arizona
1. Porter RW, Detwiler PW, Spetzler RF, Lawton MT, Baskin JJ, Derksen PT, Zabramski JM: Cavernous malformations of the brain stem: Experience with 100 patients. J Neurosurg 90:5058, 1999.

bers dissection technique in frozen human brainstem specimens. The study is focused on three anatomical landmark zones of the ventrolateral surface of the brainstem, namely the lateral mesencephalic sulcus, the pretrigeminal area, and the olivary bodies. Starting from the surface of these areas, they penetrate into the brainstem by dissecting in a three-dimensional way, being able to establish the distance from the surface and the locations of eloquent neurostructures. Now, with the data coming from this study, we know, for example, that by using the lateral mesencephalic sulcus as an entry zone, we nd a space limited ventrally by the substantia nigra, dorsally by the median lemniscus, and medially by the third ocular nerve that we can meet at a median distance of 8.2 mm deep, but it is necessary not to go beyond 5 mm to be sure to avoid surgical injury to the ocular motor nerve, because in one case they found the third cranial nerve at a depth of 4.9 mm. The same can also be said of the other functionally important structures that we can meet using the other two safe entry zones that are the subjects of this study. We should be grateful to the authors for this straightforward, well-designed, and carefully executed study that allows us to follow the possibility of new paths and know in advance the expected distances of the obstacles to be encountered more precisely, hence certainly helping the surgeon when entering the brainstem. Regarding the clinical application of these data, i.e., direct surgery for removal of purely intrinsic lesions, one must keep in mind, however, that not infrequently the lesion itself, whether an astrocytoma or cavernoma, can move the eloquent structures away from their original site while growing, and therefore the surgeon may nd them in a different place from that of the predicted normal anatomy. Although it may be useful to have knowledge of the normal distribution of anatomy as the authors explain to us, for the surgeon to move safely in a place anatomically distorted by a space-occupying lesion, there is also a need to identify the same structures functionally by using intraoperative neurophysiological motor monitoring and mapping (1). With technical advances in magnetic resonance imaging tractography in identifying even corticobulbar tracts, the surgeon will have another form of assistance in performing safe surgery in this risky setting. Albino Bricolo Verona, Italy

1. Sala F, Lanteri P, Bricolo A: Motor evoked potential monitoring for spinal cord and brain stem surgery. Adv Tech Stand Neurosurg 29:133169, 2004.

ecalde et al. report the microanatomy of the brainstem related to the different safe entry zones used to approach intrinsic brainstem lesions. They point out three anatomic landmarks on the anterolateral brainstem surface: lateral mesencephalic sulcus, peritrigeminal area, and olive. They assessed the characteristics of this region in detail using frozen brainstem specimens. In addition, they presented clinical application of this anatomical knowledge. This is an important report to add novel information regarding the surgical treatment for brainstem lesions. We agree with their concept. The lateral mesencephalic sulcus, peritrigeminal area, and olivary body can provide surgical spaces and the relatively safe alleys through which the brainstem can be approached without injuring important neural structures. Yasushi Takagi Nobuo Hashimoto Kyoto, Japan

he authors have made an important contribution to our knowledge of intrinsic microsurgical anatomy of the brainstem by using a

his is an elegant anatomic demonstration with relevant clinical implications by Recalde et al., reflecting the senior author s

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anatomic school, in the best Rhotonesque tradition. Others had commented on brainstem safe entry zones, including the dorsolateral midbrain, the anterolateral pons just caudal to the fth nerve root entry zone, and the anterolateral medulla at the anatomic olivary body. The authors describe these areas with supreme anatomic detail, including demonstration of the relative paucity of eloquent tracks and nuclei, and arterial perforator groups, in the vicinity of one of the most expensive real estates in the human brain. With regard to surgical exposure of these zones, the authors mention the supracerebellar infratentorial approach to the lateral midbrain. We have more recently favored the far posterior subtemporal approach, with tentorial section, as described by Smith et al. (1). Like the authors, we also use the presigmoid transpetrosal approach with tentorial section to reach the anterolateral pontomesencephalic region and the far lateral transcondylar approach to reach the medullary olivary body. However, the overriding choice of surgical route to brainstem cavernous malformations must remain the area wherein the lesion reaches pial or ependymal surfaces, especially if exophytic, so that there is little or no invasion of any unaffected brainstem. These so-called safe entry zones are not a substitute for choosing the area where as little brainstem parenchyma as possible is perturbed to reach the cavernoma. Internal decompression of the lesion is performed and then definition of the perlesional plane and gradual delivery of the lesion, in fragments, through as little a pial or ependymal opening as possible. Yet, when the lesion presents nearest to the surface in more than one area, we have also preferred such lateral safe routes whenever possible, posterolateral to the descending motor tracks, as an alternative to dorsal midline or paramedian approaches, which tend to result in disabling gaze and sensory morbidity. The authors are congratulated on their exquisite demonstration of anatomic subtleties, which will help in identifying the relevant landmarks at surgery, and their boundaries. Detailed anatomic imaging, including the advent of 3-T magnetic resonance will assist in the identication of related landmarks (sulci, nuclei, and tracks) when the surgical approach is planned. Frameless stereotactic image guidance can further enhance the delity of intraoperative orientation and navigation in reference to these structures as well as to the lesion. To complement the pathological and anatomic boundaries of the surgical approach, we and others have used a variety of functional monitoring techniques (motor, sensory, and auditory evoked potentials and cranial nerve electromyography) to further enhance the safety of these approaches. However, the alteration or loss of an electrophysiological response should not result in necessarily abandoning the task of lesion excision, nor does it totally predict permanent neurological decit. But such changes do result in the alteration of specic microsurgical maneuvers during the resection, such as dissection in a specic subzone. This article adds a substantive reference to the seminal literature on brainstem surgery. It will be a much used guide in last-minute planning before execution of these delicate procedures. Issam A. Awad Evanston, Illinois

medulla. In practice, the majority of brainstem cavernomas are operated on through the area of the brainstem where it comes closest to the pial surface, although this may not always be the safest approach. When the cavernoma comes close to the surface, one may assume that many of the neighboring tracts and nuclei are displaced, similar to what is found with brain mapping of cortical and subcortical lesions. However, at present, we have no reliable way of locating the displaced nuclei and ber tracts, although advances are being made with diffusion tensor magnetic resonance imaging. The practical difficulty is caused by the presence of the hemosiderin ring around the cavernoma. In the future, I am optimistic that this problem will be solved. The other problem is that the precision of surgery within the brainstem is currently limited by what is possible by human hands and existing microsurgical techniques. We have also not developed techniques for intraoperative monitoring of many of the tracts inside the brainstem. The last issue concerns neural plasticity inside the brainstem. There denitely appears to be some potential for this, as evidenced by the recovery of our patients with brainstem lesions. Perhaps we will nd ways of repairing the damaged neural tracts and nuclei in the future. Nevertheless, the results of surgery for brainstem cavernomas are acceptably good (unpublished personal data) in the hands of many expert neurosurgeons. Further advances in technology and biological knowledge will be needed to improve the current results and reduce the patients postoperative disabilities. Laligam N. Sekhar Seattle, Washington

1. Smith ER, Chapman PH, Ogilvy CS: Far posterior subtemporal approach to the dorsolateral brainstem and tentorial ring: Technique and clinical experience. Neurosurgery 52:364368, 2003.

n this article, the authors have studied the microsurgical anatomy of three safe entry zones into the brainstem for the purpose of removing cavernous malformations of the brainstem in the midbrain, pons, and

ecalde et al. present a very important anatomical study of the brainstem that is based on the long-term experience of the senior author, Evandro de Oliveira, with numerous surgical interventions in this area. A modern study designexamination of the macroscopic external and internal anatomy of the brainstem strictly from the microsurgical point of viewhas been combined with an old but very efcient method, the white fiber dissection technique. The chief merit of this systematic anatomical study is, in my opinion, the fact that the authors have not only elegantly conrmed the previous empirical experience of other neurosurgeons, namely that surgical manipulation within the brainstem is well-tolerated particularly in the transition zone between sensory and motor structures, but have also provided detailed measurement results that can be useful during surgery. These accurate distance measurements may also be valuable for the planning of the surgical procedure as they can be compared with similar measurements obtained from the magnetic resonance imaging of a specic patient undergoing surgery and later, adjusted to this specic patient, be used intraoperatively. Such measurements can be of great importance when an intrinsic cavernoma has distorted or displaced the local anatomical structures, particularly in patients with a large intralesional hematoma. My own experience with lesions involving the brainstem comprises 103 surgical cases of intrinsic cavernomas and 50 cases of intrinsic gliomas of the brainstem, apart from numerous other extraaxial lesions such as schwannomas, meningiomas, and hemangioblastomas. In a signicant number of the patients I have operated on for intrinsic brainstem cavernomas, the vascular malformation was not visible on the surface of the brainstem and in some patients not even a bulging or slight discoloration was present. I consider these the most challenging cases. Moreover, these are the real cases that require a safe entry zone because an apparently healthy brainstem has to be opened as closely as possible to a lesion that is invisible on its surface. It is obvious that the decision of where exactly to open the brainstem in such patients requires great experience, profound anatomical knowledge, and careful analysis of preoperative imaging studies before surgery. Computer-

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assisted neuronavigation may be of some help in these situations, but the accuracy of this method is not always sufciently high for complete reliance on this tool. As I have previously mentioned, the anterolateral aspect of the pons that corresponds to one of the three safe entry zones of this studythe peritrigeminal areatolerates surgical manipulation without the consequence of permanent neurological decits (1). I have also used other entry zones to the brainstem that turned out to be safe as well, for instance, a restricted area at the level of the pontomedullary sulcus between the exit of the rootlets of cranial nerves VII and IX or on the anterior aspect of the crus cerebri just lateral to the oculomotor nerve. It is important to mention, however, that with only very few exceptions I do not incise the brainstem in the sense of using a knife or microscissors. In my opinion, a true myelotomy may easily be harmful and should be avoided whenever possible. Instead of incising the brainstem, I just puncture its surface with the thinnest bipolar forceps and then gradually dilate this opening up to 5 or 6 mm in diameter, which may be sufcient to rst expose and then remove the underlying intraaxial lesion. Small cottonoids of approximately 3 mm width are helpful for this step. With this technique, supercial structures of the brainstem such as longitudinal or transverse bers can be temporarily

displaced (dilated) without completely sectioning them. A similar displacement and dilatation of intrinsic anatomical structures is also produced by the cavernoma and intralesional hematoma itself, and, apparently, this is a reversible process as can be seen on many postoperative images. Permanent parenchymal damage may only occur when either a signicant number of neurons or bers are mechanically destroyed by surgical manipulation or important perforating arteries or draining veins (including branches from an associated venous malformation) have been coagulated during surgery. In summary, I consider the present study a most valuable contribution to our knowledge of brainstem anatomy. The results presented here may be of signicant help to many neurosurgeons who operate on difcult lesions such as intraaxial vascular malformations or gliomas of the brainstem. Helmut Bertalanffy Zurich, Switzerland
1. Bertalanffy H, Benes L, Miyazawa T, Alberti O, Siegel AM, Sure U: Cerebral cavernomas in the adult: Review of the literature and analysis of 72 surgically treated patients. Neurosurg Rev 25:153, 2002.

The Anatomical Theater at Leiden, (1610), copper engraving. From: Wolf-Heidegger G, Cetto AM: Die Anatomische Sektion in Bildlicher Darstellung. Basel, Karger, 1967.

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