Childs Nerv Syst (2015) 31:1815–1840

DOI 10.1007/s00381-015-2799-y

SPECIAL ANNUAL ISSUE

Surgical approaches for brainstem tumors in pediatric patients

Sergio Cavalheiro 1,5 & Kaan Yagmurlu 2 & Marcos Devanir Silva da Costa 4 &
Jardel Mendonça Nicácio 1 & Thiago Pereira Rodrigues 4 & Feres Chaddad-Neto 3 &
Albert L. Rhoton 2

Received: 18 June 2015 / Accepted: 19 June 2015

# The Author(s) 2015. This article is published with open access at Springerlink.com

Abstract Keywords Pediatric brainstem gliomas . Brainstem surgery .

Purpose To analyze the pathways to brainstem tumors in Safe entry zone . White fiber anatomy . Supratrigeminal
childhood, as well as safe entry zones. approach . Low-grade astrocytoma
Method We conducted a retrospective study of 207 patients
less than 18 years old who underwent brainstem tumor resec-
tion by the first author (Cavalheiro, S.) at the Neurosurgical Introduction
Service and Pediatric Oncology Institute of the São Paulo
Federal University from 1991 to 2011. The brainstem is one of the most complex structures in the
Results Brainstem tumors corresponded to 9.1 % of all pedi- human body and contains the most complex intracranial anato-
atric tumors operated in that same period. Eleven previously my [55]. This compact, midline organ is protected anteriorly by
described Bsafe entry zones^ were used. We describe a new the clivus, laterally by the petrous part of temporal bone, supe-
safe zone located in the superior ventral pons, which we riorly by the diencephalon, and posteriorly by the cerebellum.
named supratrigeminal approach. The operative mortality All motor, sensory, sympathetic, and parasympathetic brain
seen in the first 2 months after surgery was 1.9 % (four pa- functions are integrated and travel through the brainstem. The
tients), and the morbidity rate was 21.2 %. structural complexity of the brainstem makes surgical proce-
Conclusions Anatomic knowledge of intrinsic and extrinsic dures there in extremely difficult and require a perfect technique.
brainstem structures, in association with a refined neurosurgi- Brainstem tumors are more common in children and represent
cal technique assisted by intraoperative monitoring, and sur- up to 18 % of childhood brain tumors and 25 % of posterior
gical planning based on magnetic resonance imaging (MRI) cranial fossa tumors. There is no gender predilection. The mean
and tractography have allowed for wide resection of brainstem age incidence for these tumors occurs around age 5 to 10 years
lesions with low mortality and acceptable morbidity rates. [54]. A second peak of incidence is seen in adults between 30 to
40 years of age. In recent years, several articles have been pub-
lished on brainstem anatomy and Bsafe entry zones.^ Most of
* Sergio Cavalheiro these are related to cavernoma surgery and few are related to
sergiocavalheironeuro@gmail.com
brainstem tumor surgical approaches in children [9, 19, 22, 26,
53]. The aim of this study was to review the described surgical
1
Department of Neurosurgery, Pediatric Oncology Institute, Federal approaches and those conducted by the first author (Cavalheiro,
University of Sao Paulo, Sao Paulo, Brazil S.) of this article on the basis of 207 patients aged less than
2
Department of Neurosurgery, University of Florida, College of 18 years who underwent brainstem tumor surgery.
Medicine, Gainesville, FL, USA
3
Department of Neurosurgery, Vascular Division, Federal University
of Sao Paulo, Sao Paulo, Brazil Classification
4
Department of Neurosurgery, Federal University of Sao Paulo, Sao
Paulo, Brazil The various arrangements of fibers, Virchow-Robin spaces,
5
Rua Botucatu, 591, conj 41, CEP: 04023-062 Sao Paulo, SP, Brazil and structures comprising the brainstem occasionally allow
1816 Childs Nerv Syst (2015) 31:1815–1840

tumors to grow considerably with few symptoms. This may local lesions have well-delimited borders. Less edema is asso-
permit diffuse pontine tumors to grow within the pons without ciated with focal tumors, which are mainly low-grade gliomas.
infiltrating the mesencephalon or medulla. When midbrain They are usually hypointense on T1, with diffuse tumoral
tumors grow, they spread towards the thalamus and do not enhancement. Impregnation with gadolinium varies in focal
infiltrate the pons. Tumors of the medulla tend to grow into tumors; however, homogeneous enhancement is highly sug-
the fourth ventricle without invading the pons, or grow cau- gestive of pilocytic astrocytoma [29].
dally towards the spinal cord. If the tumor is superficial, surgery is advised; however, if it
Many classifications have been proposed for brainstem tu- is deep, the treatment should be conservative, in the expecta-
mors. We used that proposed by Choux et al.: type I, diffuse tion that the tumor itself may provide an “opening door” for its
brainstem gliomas; type II, focal intrinsic tumors (solid or resection. The use of tractography has allowed for better
cystic); type III, exophytic; and type IV, cervicomedullary choices regarding surgical approaches to these tumors.
[14, 15, 17]. Tumors in the quadrigeminal plate are usually focal and most-
ly pilocytic astrocytomas [33].
Diffuse tumors (type I)
Exophytic tumors (type III)
Diffuse tumors are the most common, representing up to 80 %
of brainstem tumors. They simultaneously affect multiple nu- Exophytic tumors are more accessible surgically. They tend to
clei and pathways, and characteristically cause bilateral paral- be large tumors with a large component out of the brainstem,
ysis of cranial nerves VI and VII, progressing to hemiparesis facilitating surgery. They may have a cystic component, an-
and tetraparesis. They present with rapid clinical evolution, other factor that facilitates its resection. They are mostly low-
and as far as histopathology is concerned, most are malignant grade astrocytomas [48].
astrocytomas (WHO) grade III or IV. Radiologically, they are
characterized by pontine enlargement with an entrapped bas-
ilar artery. They are hypointense on T1 magnetic resonance Cervicomedullary junction tumors (type IV)
imaging (MRI), hyperintense on T2, hyperintense on FLAIR,
and exhibit minimal contrast enhancement [6, 44]. Cervicomedullary junction tumors often present as an
Survival of these patients is short, and most die within the exophytic growth, allowing surgeons direct access without
first 2 years after diagnosis. However, a few cases may re- incising the brainstem. These lesions usually do not infiltrate
spond to chemotherapy and radiation. There is no difference the pons and grow cranially into the fourth ventricle. They
in prognosis using conventional or multi-fractionated radio- may extend caudally into the spinal cord. When growing to-
therapy. Metastases of the neuraxis may occur in 5 to 30 % of ward the fourth ventricle, hydrocephalus may occur early on.
cases [10, 18, 25]. When growing towards the spinal cord, they may produce
Stereotactic biopsy of diffuse brainstem tumors has been syringomyelia, due to changes in cerebrospinal fluid dynam-
performed in a few centers. Its use is important mainly for ics. Although surgical approaches are facilitated by topogra-
molecular biology studies [52, 57, 62]. However, biopsies phy, these are cases that most often progress with serious
are associated with some complications. Pincus et al. (2006) morbidity. Postoperatively, these patients may have difficulty
[49] conducted a retrospective study of 182 stereotactic biopsy breathing, resulting in long periods of assisted mechanical
cases from 13 published reports of diffuse pontine lesions in ventilation, and swallowing difficulties, which in turn may
children. They noted that tumor diagnosis was verified in 75 cause severe aspiration pneumonia. Patients may require tra-
to 100 % of cases. In 87 % of cases, the lesions were gliomas, cheostomy and gastrostomy, necessitating speech therapy.
while the remaining 13 % were primitive neuroectodermal The use of electrophysiological monitoring during surgery
tumors, neurocytomas, ependymomas, and demyelinating le- has helped to prevent those complications [16].
sions. Morbidity ranged from 0 to 16 %, and mortality reached
5 %. Therefore, biopsy is indicated only in cases with non-
characteristic images or in molecular biology research centers Patients and methods
[32, 59]. Stereotactic biopsies can be performed through entry
points in the frontal region or through the posterior fossa. From 1991 to 2011, 303 patients younger than 18 years with
brainstem tumors were treated by the Neurosurgical Service
Focal tumors (type II) and Pediatric Oncology Institute of the Federal University of
Sao Paulo. Of these, the first author of this article surgically
Focal tumors behave differently from diffuse tumors. They are treated 207. The remaining 96 cases were diffuse tumors.
slow-growing lesions, and the symptomatology is indolent. Here, we describe the surgical approaches and relevant
They may be solid or cystic and, contrary to diffuse tumors, extrinsic/intrinsic anatomical points used.
Childs Nerv Syst (2015) 31:1815–1840 1817

The brainstem is divided into three segments: the midbrain, cerebellar artery and by collicular arteries, and they form a
pons, and medulla. In order to choose the most effective and plexus involving the quadrigeminal plate [55].
safe approaches for removal of the lesions, we divided the
brainstem into seven portions (Fig. 1e). Anterior midbrain
The midbrain was divided into three parts: anterior, central,
and posterior. The anterior segment is delimited posteriorly by Tumors in the anterior portion of the midbrain usually grow in
the substantia nigra. The central midbrain extends from the two directions: toward the third ventricle and toward the
substantia nigra to the aqueduct. The posterior part is restricted interpeduncular cistern. For tumors growing into the third
to the quadrigeminal plate. The pons was divided into two ventricle, an interfornicial, transcallosal, transchoroidal, or
segments: anterior and posterior, or ventral and dorsal. transforaminal approach is used. When the lesion is less than
Similarly, the medulla was divided into anterior and posterior, 2 cm in size, a neuroendoscope coupled to an ultrasonic aspi-
or ventral and dorsal, partitions. Detailed knowledge of the rator can be used for removal of the tumor, most of which are
brainstem extrinsic and intrinsic anatomy is essential to avoid low-grade astrocytomas (Fig. 3). When these tumors grow
morbidity during the surgical approaches. toward the interpeduncular cistern, they usually present with
Weber syndrome (third cranial nerve impairment and contra-
lateral hemiparesis) (Fig. 4).
Midbrain Anterior and anterolateral lesions of the midbrain can
be approached by the transsylvian pathway with a classic
The midbrain is separated from the diencephalon by a sulcus pterional, orbito-fronto-zygomatic, or temporal route.
between the optic tract and cerebral peduncle, and from the Through those routes, it is possible to combine ap-
pons by the pontomesencephalic sulcus. Anatomically, three proaches via a temporopolar approach (pre-temporal or
structures should be widely recognized in the midbrain: the transtentorial subtemporal). The temporopolar approach
pyramidal tract located in the anterolateral portion of the mid- was described by Sano in 1980 [58]. It allows for an
brain, nuclei of the third and fourth cranial nerves [63] (Figs. 1 opening over the temporal lobe in the posterior-superior
and 2a). The level of the nucleus of the third cranial nerve is at d i r e c t i on a n d v i s u a l i z a t i o n of th e a n t e r o l a t e r a l
the lower half of the superior colliculus and the upper half of interpeduncular fossa. Another approach to be used is
the inferior colliculus. The trochlear nucleus lies caudal to the the subtemporal transtentorial, as described by Krause in
inferior half of the inferior colliculus. These nuclei are posi- 1911 [36]. This approach increases the risk of venous
tioned adjacent to the midline and on average 9.5 mm medial infarct due to the injury to the vein of Labbe complex,
to the surface of the lateral mesencephalic sulcus. The mesen- and ophthalmoparesis due to third and fourth cranial
cephalic lateral sulcus runs from the medial geniculate body nerve injury along the tentorial incisure. On the other
superiorly to the pontomesencephalic sulcus inferiorly. This hand, this approach allows an excellent view of the
sulcus is considered the posterior limit of the ventral lateral incisural space. The incision ensures good exposure of
midbrain. The third cranial nerve has a long course along all the basilar artery, interpeduncular cistern, brainstem, and
the central portion of the mesencephalon while the fourth cra- rostral ventral surface of the pons. A Bfairly safe^ entry
nial nerve has a smaller intrinsic portion and runs through the zone into the anterolateral midbrain, described by Bricolo
contralateral cerebellomesencephalic fissure. The third cranial and Turazzi [7], has been proposed since the fibers of the
nerve exits at the medial sulcus of the midbrain peduncle and corticospinal tract occupy only the intermediate three-
goes toward the oculomotor triangle, towards its entry into the fifths of the peduncle (Fig. 2c). This narrow window is
cavernous sinus. The midbrain receives its blood supply delimited above by the posterior cerebral artery, below by
through mesencephalic perforating basilar artery branches. the superior cerebellar artery, medially by the emergence
They are divided into anteromedial, anterolateral, lateral, and of cranial nerve III and the basilar artery, and laterally by
posterior branches. The anteromedial branches are divided the pyramidal tract (Fig. 5). Tumors here are often
into lateral and medial. The medial branches supply the red exophytic, making it unnecessary to enter the brainstem,
nucleus, periaqueductal gray matter, and the third and fourth and the tumor can be incised at the exit point of the le-
cranial nerve nuclei. The lateral branches supply the medial sion. In cases of focal tumors, where it is necessary to
lemniscus, substantia nigra, and superior cerebellar peduncle. incise the brainstem, a diamond-tipped scalpel is used.
The anterolateral midbrain arteries are called peduncular Bipolar coagulation is not used. Incisions parallel and
branches, and supply the crus, substantia nigra, and medial lateral to the third cranial nerve are made to prevent py-
lemniscus. They arise from many arteries, including the ramidal tract injury. Access in this way is termed
collicular, medial posterior choroidal, posterior communicat- perioculomotor. Great care must be taken with this strat-
ing artery, superior cerebellar artery, and anterior choroidal egy to avoid injury of the red nucleus, pyramidal tract,
artery. Posterior arteries are formed by branches of superior and the oculomotor nerve.
1818 Childs Nerv Syst (2015) 31:1815–1840

Fig. 1 a. The brainstem surface anatomy. The brainstem is divided into tentorial, petrosal, and suboccipital. The suboccipital surface of the
three parts: the midbrain, pons, and medulla. The midbrain is limited cerebellum and medulla is supplied by the posteroinferior cerebellar
superiorly by the sulcus between optic tract (OT) and crus cerebri, and artery (PICA). The petrosal surface of the cerebellum and pons are
inferiorly by the pontomesencephalic sulcus (Pon. Mes. Sulc.). The pons supplied by AICA and basilar artery perforators, while the midbrain
is positioned between the pontomesencephalic sulcus above and and tentorial surface of the cerebellum is supplied by the superior
pontomedullary sulcus (Pont. Med. Sulc.) below. The medulla extends cerebellar artery (SCA) branches. e Another division of the brainstem
from the pontomedullary sulcus to the exit zone of the C1 nerve root. b, c, into seven compartments: the ventral, central, and dorsal midbrain;
d The brainstem vascularization. The vertebral arteries (VA) meet to form ventral and dorsal pons; and ventral and dorsal medulla. f Anatomical
the basilar artery at the level of the pontomedullary sulcus. The basilar division of the brainstem according to course of the medial lemniscus
artery (BA) gives rise to posterior cerebral arteries (PCA) at the level of (ML). In front of the ML can be considered the ventral brainstem, and
the pontomesencephalic sulcus. The cerebellum has three surfaces: behind the medial lemniscus as the dorsal brainstem
Childs Nerv Syst (2015) 31:1815–1840 1819

Fig. 2 a Schematic representation of the midbrain at the level of the oculomotor and trochlear nuclei is positioned between medial lemniscus
oculomotor nerve. The substantia nigra and medial lemniscus is the and aqueduct. The dorsal (posterior) midbrain composed of superior (SC)
border between ventral (anterior) and central parts of the midbrain, and inferior colliculi (IC) is positioned behind the cerebral aqueduct. The
while the level of the cerebral aqueduct is the border between central nuclei of the CN III and IV are located just ventral to the aqueduct. c
(blue) and dorsal (posterior) midbrain (green). The corticospinal tract Anterior view of midbrain. 1 Perioculomotor entry zone is bordered
(yellow) in the ventral midbrain (red); nuclei and courses of the CN III medially by exit point of the CN III and laterally by the corticospinal
(yellow) and IV (red) in the central (blue) and dorsal midbrain. b Lateral tract (CST). d The perioculomotor zone is limited by the posterior
view of the midbrain. The ventral (anterior) midbrain, which contains the cerebral artery (PCA) superiorly and by the superior cerebellar artery
corticospinal tract (CST), is situated in front of the medial lemniscus (SCA) inferiorly
(ML) and substantia nigra. The central midbrain containing the red,

Central midbrain cranial nerve is directly below the inferior colliculus. With
exophytic lesions, there is no need to incise the brainstem,
Tumors located in the intermediate midbrain can also grow in and we can directly approach the tumor, except for small
two directions: toward the pineal region or into the fourth cavernomas for which we used three access routes: upper
ventricle. When they grow toward the fourth ventricle, the and lower pericollicular, and through the lateral mesencephal-
suboccipital telovelar approach is used. When they grow to- ic sulcus.
wards the pineal region, we use the path suggested by Krause From the pericollicular access point, two Bsafe zones^ can
in 1911 [37] and popularized by Stein [60], which is the be accessed: an incision made in the midbrain below the infe-
suboccipital infratentorial supracerebellar route (Figs. 6 and rior colliculus, or infracollicular access, and above the troch-
7), further divided into median or paramedian. Patients are lear nerve, or supracollicular access. In the supracollicular
usually in the sitting position for this approach. An extensive approach, a transverse incision is made just above the superior
posterior fossa craniotomy with removal of the C1 arch is colliculus and should be limited by the aqueduct. Further ex-
performed. This approach allows for wide movement of the tension in this approach can damage the nuclei of cranial
cerebellum. After coagulation of the vermian veins, the cere- nerves III and IV, as well as the medial longitudinal fasciculus.
bellum drops to allow access to the midbrain. When lesions With infracollicular access, a transverse incision between the
are medial, we also coagulate the precentral cerebellar vein. trochlear nerve and the lower edge of the inferior colliculus is
When lesions are lateral, there is no need to coagulate this vein performed. As for the supracollicular route, an incision deeper
(Fig. 8). Care should be taken in this region as the fourth than the cerebral aqueduct will damage the nuclei of the third
1820 Childs Nerv Syst (2015) 31:1815–1840

Fig. 3 a Endoscopic access to

tumors located in the anterior and
superior portion of the midbrain.
b An 8-year-old patient with
intracranial hypertension. A
lesion is present in the anterior
and superior topography of the
midbrain. c 3-year follow-up after
complete removal of the lesion by
endoscopy, with patency of the
cerebral aqueduct. Diagnosis was
low-grade astrocytoma. d.
Intraoperative endoscopic view of
the exophytic tumor in the
midbrain and after complete
resection. After passing through
the foramen of Monro, the lesion
was seen and removed at the floor
of the third ventricle

and fourth cranial nerves and the medial longitudinal fascicu- superior cerebellar peduncle, the trigeminal mesencephalic
lus. More lateral extensions of this incision will damage the tract, and the decussation of the superior cerebellar peduncle.

Fig. 4 a, b 4-year-old girl

admitted with a right Weber
Syndrome with a solid/cystic
anterior mesencephalic lesion
with expansion towards the
interpeduncular cistern. c, d
6-year follow-up showing total
resection by fronto-orbito
zygomatic approach (pilocytic
astrocytoma)
Childs Nerv Syst (2015) 31:1815–1840 1821

Fig. 5 a. A 7-year-old patient

with diplopia and paresis of the
oculomotor nerve on the right
side. MRI shows a focal and
intrinsic lesion parallel to the
intrinsic course of the third nerve
in the midbrain. b. Follow-up
5 years after gross total resection
showing no residual lesion

For lesions extending towards the fourth ventricle, we can of the fibers, as well as on the tumor texture and circulation.
incise the quadrangular lobe of the cerebellum for greater access Tumors are usually softer than the normal brain stem and also
to the cerebellar mesencephalic fissure. In this approach, it is more vascularized, which makes it easier to remove them.
essential to have a spatial imagination of the third and fourth
nerves nuclei, as well as of their course inside the midbrain. Posterior (dorsal) midbrain
The ultrasonic aspirator is extremely important in that situa-
tion, and the color of the tumor is also most helpful in achieving Posterior midbrain or quadrigeminal plate is the name given to
total resections. Some tumors, however, are the same color as the portion of the midbrain that is posterior to the cerebral
the brainstem, and then the surgeon has to rely on the position aqueduct. The tumors of the quadrigeminal plate are the

Fig. 6 a. Tumors located at the

central portion of the midbrain
and growing towards the pineal
region. b Infratentorial
supracerebellar approach. c
Anatomical view of pineal region
via the infratentorial
supracerebellar route. SC superior
colliculus, IC inferior colliculus
1822 Childs Nerv Syst (2015) 31:1815–1840

Fig. 7 a, b A solid cystic tumor

at the central portion of the
midbrain with gadolinium
enhancement growing towards
the pineal region was removed by
a central infratentorial
supracerebellar approach. c, d 10-
year follow-up shows no
evidence of the lesion, which was
a pilocytic astrocytoma

smallest brain tumors liable to kill the patient from hydroceph- a three-quarters prone body position, the side with the lesion
alus. They account for approximately 5 % of pediatric tumors turned down, the coronal plane at a 45-degree angle with the
of the brain stem [24]. They are usually indolent lesions and floor, and the head at 30-degree flexion and 15-degree eleva-
the treatment is limited to the treatment of hydrocephalus. tion. This allows the occipital lobe to drop by force of gravity,
Most of the time, these tumors are isointense on T1- and so there is less need of cerebral retraction, and the risk of
weighted and hyperintense on T2-weighted images. Up to homonymous hemianopsia as a consequence of retraction of
19 % of cases may have gadolinium-enhanced MRI [23]. the occipital lobe. This approach enables an excellent view of
The hydrocephalus is best treated by endoscopic third the pineal region, postero-lateral surface of mesencephalon,
ventriculostomy [38]. Endoscopic biopsy should be avoided tentorial surface of the cerebellum, splenium of the corpus
due to the possibility of a hemorrhage, distal from the biopsy callosum, and posterior third of the third ventricle.
area (Fig. 9), most of such lesions being low-grade astrocyto- This approach is mainly recommended for tumors having a
mas such as pilocytic and non-pilocytic astrocytomas, mixed large superior and lateral extension, with the displaced venous
gliomas, and rarely more aggressive tumors as anaplastic as- complex impairing the view of the tumor through a posterior
trocytomas [50]. medial pathway.
Some tumors may grow and require surgery. In such cases, In this approach, an occipital craniotomy is performed in-
two types of approach have been used: when they grow to- volving the occipital suture and bordering the transverse and
wards the third ventricle, the supracerebellar infratentorial superior sagittal sinus. The dura can be opened in a C-shape
route is chosen (Fig. 11); however, if they grow towards the with the base facing the superior sagittal sinus, or by two
superior part of the fourth ventricle, the transtentorial occipital triangles with the bases facing the superior sagittal and trans-
approach proposed by Poppen [51] and modified by Ausman verse sinuses. The cerebellar tentorium is opened parallel to
[3] (Fig. 10) has been preferred. The transtentorial occipital the straight sinus for 1.5 to 2 cm. A small incision in the
approach was first described by Horrax in 1937 [28], modified splenius of the corpus callosum may also be performed to
by Poppen in 1968 [51], and popularized by Jameson in 1971 enlarge the view of the tumors extending go the posterior third
[30]. Several surgical positions have been described, such as of the III ventricle. When the tumor grows towards the third
sitting, prone, concorde, and three-quarter prone. Ausmann ventricle and the superior part of the fourth ventricle, that
(1988) [3] described the transtentorial occipital approach with region becomes a Bblind^ region—and therefore, we use the
Childs Nerv Syst (2015) 31:1815–1840 1823

Fig. 8 a Lateral view of the midbrain. The lateral mesencephalic sulcus and inferior colliculus in the posterior (dorsal) midbrain. The oculomotor
(LMS) runs on the surface of the midbrain extending from the medial nucleus is positioned at the level of the inferior half of the superior
geniculate body (MGB) above to the pontomesencephalic sulcus (Pont. colliculus and superior half of the inferior colliculus in the midline, and
Mes. Sulc.) below. The LMS extends along the lateral edge of the medial the trochlear nucleus is positioned at the level of the inferior half of the
lemniscus (ML). b The ML divides the midbrain into ventral (anterior) and inferior colliculus in the midline. c Lateral lesion in the central midbrain
dorsal (posterior) parts. Neurocritical structures at entry through the LMS approached via infratentorial supracerebellar route along the lateral sulcus
are the corticospinal tract in the anterior midbrain, the red, oculomotor and of the mesencephalon. d Five-year follow-up after complete resection
trochlear nuclei in the central (tegmentum) midbrain, nuclei of the superior showing no evidence of the lesion, a pilocytic astrocytoma

infratentorial supracerebellar, associated to the suboccipital

telovelar approach in order to reach the fourth ventricle [4]
(Fig. 11).
Therefore, for midbrain surgery, we have four “safe zones”:
through the perioculomotor area for anterior region lesions,
supracollicular access, infracollicular access, and through the
lateral mesencephalic sulcus to the intermediate midbrain.
Lesions of the posterior midbrain are usually exophytic, not
requiring brainstem incision.

Pons

Most pontine tumors are diffuse; therefore, resective sur-

gery is not beneficial and chemotherapy/radiotherapy is
indicated. Neurosurgeons must differentiate between fo-
Fig. 9 Intraventricular hemorrhage after endoscopic biopsy of a cal, low-grade exophytic, and diffuse tumors for patients
quadrigeminal plate lesion—pilocytic astrocytoma to benefit from surgery.
1824 Childs Nerv Syst (2015) 31:1815–1840

Fig. 10 a Tumor in the quadrigeminal plate growing towards the fourth operated via transtentorial-occipital approach. e. Postoperative imaging
ventricle. b Transtentorial occipital approach. c Right occipital 9 years after gross total resection of the lesion, showing no evidence of
transtentorial view. The pineal gland and splenium are exposed. d. tumor, which was a pilocytic astrocytoma
Quadrigeminal plate tumor growing towards the fourth ventricle,

The pons is located between the superior pontomesencephalic tumors are approached via the rhomboid fossa. Three ar-
and inferior pontomedullary sulci. The pons is divided in two at terial groups provide blood to the pons: anteromedial,
the level of the medial lemniscus into anterior and posterior, or lateral, and dorsal. The anteromedial arteries are derived
ventral and dorsal. The pons contains the pyramidal tract, which from the basilar artery and terminal vertebral artery
is more medial and anterior than in the midbrain, as well as the branches. These arteries nourish the paramedian tegmen-
trigeminal, abducens, facial, and vestibulocochlear nerves and tum (including the pyramidal tract fascicles), medial lem-
nuclei. Therefore, it is imperative to know the intrinsic and ex- niscus, medial longitudinal fasciculi, reticular formation,
trinsic anatomy of the fifth, sixth, and seventh cranial nerves in and abducens nucleus. Perforating lateral branches arise
the pons (Fig. 12). from the superior cerebellar artery (SCA), anterior inferior
The facial nerve courses around the sixth nerve nucle- cerebellar artery (AICA), and long pontine arteries. They
us. This relationship must be very well established when supply the superior cerebellar peduncle, central tegmental
Childs Nerv Syst (2015) 31:1815–1840 1825

Fig. 11 a Posterior (dorsal)

midbrain is composed of pair
superior (SC) and inferior
colliculi (IC). The transverse
supracollicular incision (1) is
made just above the upper edge of
the superior colliculus. The
infracollicullar incision (2) is
directed transversely between the
CN IV and the lower edge of the
inferior colliculus. b Further
dissection of dorsal (posterior)
midbrain. The important
landmark is the cerebral aqueduct,
which is located just behind the
medial longitudinal fasciculus
(MLF), oculomotor, and trochlear
nuclei at the midline. The red
nucleus extends from the
midlevel of the inferior colliculus
to the lateral wall of the third
ventricle. c Cartoon of a large
tumor growing towards third and
fourth ventricle which can be
approached by combined
infratentorial supracerebellar
followed by subocciptal telovelar
approach. d A large pilocytic
astrocytoma of the quadrigeminal
plate in a 5-year-old patient,
growing towards the third
ventricle and fourth ventricle,
approached via combined
supracerebellar-infratentorial and
telovelar pathway through the
rhomboid fossa. e Postoperative
MRI scan shows gross total
resection

tract, lemniscus side, locus ceruleus, motor and sensory Anterior pons
main trigeminal nuclei, abducens nucleus, facial nucleus,
superior olivary nucleus, pontine reticular nucleus, lem- Tumors of the anterior and upper pons can be accessed
niscus side, and pyramidal tract. Terminal SCA branches using an orbito-fronto-zygomatic route, which is a modi-
comprise the posterior arterial supply of the pons. They fication of the supraorbital craniotomy described by Jane
perfuse the superior cerebellar peduncle, mesencephalic et al. in 1982 [31]. The third cranial nerve is a key refer-
nucleus of the trigeminal nerve, and the locus ceruleus ence point in this approach. To expose the upper portion
[55] (Fig. 13). of the pons, it is necessary to dissect the interpeduncular
1826 Childs Nerv Syst (2015) 31:1815–1840

Fig. 12 a. Topography of the corticospinal tract in the pons (yellow). ventral pons. The supratrigeminal incision is made 4 mm below the
Nuclei and courses of the VI (green) and VII (orange/ red) cranial pontomesencephalic sulcus at the same sagittal level as the exit point of
pairs. b Lateral view. The ventral pons located in front of the medial the CN III. The peritrigeminal incision is made medial to the entry zone of
lemniscus (ML) and the dorsal pons located behind the ML have been the CN V and between CN V and CN VII. d Lateral view of the ventral
exposed. c Anterior view of the pons. The supratrigeminal (1) and pons. Neurocritical structures at risk are the corticospinal tract, trigeminal
peritrigeminal (2) safe entry zones are used for lesions located in the motor nucleus, and intrapontine segment of the CN V–VIII

and pre-pontine cisterns with durotomy of the free edge of is made longitudinally between the points of emergence of
the tentorium. The entry point is supratrigeminal. A 4-mm the fifth and seventh cranial nerves. However, this corri-
vertical incision is made below the mesencephalo-pontine dor is too narrow, good only for biopsies or for removal
sulcus in a line from the third to the fifth cranial nerve; of cavernomas therein. This approach can be achieved
thus, we named this access route Bsupratrigeminal.^ We through a paramedian occipital pathway or through the
have used this route for superior ventral lesions without petrosal route. In the anterior approach of the pons, the
additional patient morbidity (Fig. 14). region around the emergence of the fifth nerve is a safe
For lesions located in the anterior and inferior portions area to be opened 1 cm wide at 1 cm from the midline,
of the pons, or for ventrolateral lesions, the pre-sigmoid but one should be careful not to go very anterior to avoid
approach has been used (Fig. 15). The incision in the pons the corticospinal tract.

Fig. 13 a The retrosigmoid approach can be used for supra- and peri-trigeminal entry zones. b The presigmoid approach provides good exposure for
supra- and peritrigeminal entry zones
Childs Nerv Syst (2015) 31:1815–1840 1827

Fig. 14 a, b 8-month-old patient

with a large lesion in the anterior
and superior portion of the pons,
approached via orbito-fronto
zygomatic via the supratrigeminal
entry zone. c, d 6-month
postoperative follow-up after
complete resection of the lesion

Posterior pons This topography accepts a little retraction in the superior

and lateral direction, while retraction in the caudal direction
Posterior pontine lesions are accessed via the rhomboid should be as far as possible avoided (Fig. 17).
fossa (Fig. 16). Superior and posterior pontine lesions are For posterior and inferior lesions, the infracollicular route is
a c ce s s e d b y a t e l o v el a r ro u t e , a l s o k n o w n a s a used, through the infrafacial triangle (Fig. 18), which has as a
cerebellomedullary fissure approach [42, 43, 46]. The medial border, the medial longitudinal fasciculus, and is bor-
opening to the brainstem above the facial nerve is called dered caudally by the medullary striae and laterally by the
the suprafacial triangle, which is defined medially by the facial nerve.
medial longitudinal fasciculus (i.e., the median sulcus), This is a much smaller triangle and the safe distances are
caudally by the facial nerve (having the facial colliculus not always the same, so that intraoperative monitoring is man-
as reference), and laterally by the upper cerebellar pedun- datory. The safe area to access the infracollicular triangle as
cles. This triangle is approximately 1 cm2. Although it is a described by Kyoshima et al. [39] would begin on average
safe entry triangle, prudence recommends bipolar stimula- 6.5 mm above the obex and would extend for 9.2 mm in the
tion on the surface in order to localize the course of the cranial-caudal direction; the supracollicular triangle would be
facial nerve, which might have been deviated due to the on average 22.5 mm above the obex, with an extension of
growth of the tumor. Entry to this zone must always be 13.6 mm.
2 mm from midline to preserve the medial longitudinal We have used a third approach, when no space is found in
fasciculus. However, recovery after injury of this fascicle the rhomboid fossa, namely the interfacial approach. Bricolo
is very fast compared to partial facial nerve involvement. and Turazzi [7] have described the midline access in the
1828 Childs Nerv Syst (2015) 31:1815–1840

Fig. 15 a, b 10-year-old patient

with tetraparesis. Tumor operated
with a pre-sigmoid approach. c, d
Postoperative control 10-year
after gross total resection,
showing no evidence of tumor

rhomboid fossa as being possible at the level of the facial peduncle extending to the midline. This technique is best used
colliculi, next to the nucleus of the sixth nerve, since the fibers with the aid of neuronavigation.
of the medial longitudinal fasciculi are not yet crossed at this Therefore, for the pons, we have the following Bsafe
level. In this approach, the medial longitudinal fasciculus is zones^: supratrigeminal, peritrigeminal, suprafacial,
damaged, which may disturb the conjugate movement of the infrafacial, interfacial, and through the lateral sulcus
eyes. From the surgical point of view, we have used a bilateral limitans.
telovelar approach, with coagulation of the choroid plexus of
the fourth ventricle, which allows for ample access from the Medulla
obex to the cerebral aqueduct without need to harm the cere-
bellar vermis. The medulla is the most caudal portion of the brain stem,
More lateral lesions have been approached through the lat- and it is separated from the pons by the bulbopontine
eral sulcus limitans, also via a telovelar approach [40]. sulcus (Fig. 19). The inferior limit of the medulla is the
Lawton et al. [40] have proposed a supratonsillar approach pyramidal decussation and foramen magnum in the ven-
to the inferior cerebellar peduncle, without the need to open tral surface. The posterior surface is the obex. It receives
the IV ventricle and perform an expanded telovelar approach. blood supply from the vertebral artery and branches of the
This route has been described for cavernomas, but it can be anterior spinal artery. The anterolateral perforating arteries
sufficient for tumoral lesions of the inferior cerebellar perfuse the pyramidal tract and the inferior olivary nuclei.
Childs Nerv Syst (2015) 31:1815–1840 1829

Fig. 16 a Topography of the

corticospinal tract in the pons
(yellow). Nuclei and courses of
the CN VI (green) and VII
(orange/red) cranial pairs. b The
facial colliculus, which is
produced by the CN VI nucleus
and intrapontine segment of CN
VII, is the most important
landmark on the floor of the
fourth ventricle. c There are four
important structures avoiding
their damage: the medial
longitudinal fasciculus (MLF),
central tegmental tract (CTT), and
trigeminal mesencephalic (TMT)
and spinal (TST) tracts. d
Posterior brain stem safe zones: 1
pericollicular, 2 suprafacial, 3
interfacial, 4 lateral sulcus
limitans, 5 infrafacial, and 6
middle. e The suprafacial entry
zone (2) is bordered superiorly by
frenulum veli containing the CN
IV, inferiorly by the facial
colliculus (FC), medially by
medial longitudinal fasciculus
(MLF), and laterally by sulcus
limitans, a lateral sulcus. f
Superior fovea, is a depression
formed by sulcus limitans, has a
triangular shape (green triangle).
The apex of this triangle is at the
same axial level as the uppermost
margin of the facial colliculus.
The trigeminal motor nucleus
(yellow circle) is located at a
deeper point of the superolateral
edge of this triangle. g The
infrafacial entry zone is bordered
superiorly by facial colliculus,
inferiorly by hypoglossal (CN
XII) triangle, medially by medial
longitudinal fasciculus (MLF),
and laterally by the CN VII
nucleus and nucleus ambiguus. h.
Median subcoccipital approach is
used to reach the floor of the
fourth ventricle. i Telovelar
junction is incised. j Exposure of
the floor of the fourth ventricle
1830 Childs Nerv Syst (2015) 31:1815–1840

Fig. 17 a, b Superior and

posterior pontine tumor
approached via suboccipital
telovelar approach with the point
of entry into the pons through the
suprafacial triangle. Astrocytoma
grade II. c, d Postoperative
control showing gross total
resection

The lateral arteries are branches of the posteoinferior cer- approaches to the craniovertebral junction. There are
ebellar artery (P.I.C.A.), anteroinferior cerebellar artery many variations of approaches according to the part of
(A.I.C.A.), and vertebral and basilar arteries, and they condyle to be removed: transcondylar, supracondylar,
perfuse the inferior cerebellar peduncle, the spinothalamic and paracondylar exposure [56]. In children, it is possible
tract, spinocerebellar tract, spinal trigeminal nucleus, cen- to access the anterior portion of the medulla without re-
tral reticular formation, dorsal motor nucleus of the vagus, moving the condyles (Fig. 20). The section of the dentate
nucleus and tractus solitarius, and the hypoglossal, vestib- ligament next to the entry of the vertebral artery facilitates
ular, cochlear, cuneate and ambiguous nuclei. The gracile mobility of the medulla, and so the lateral access becomes
and cuneate nuclei, area postrema, and vagal, solitary, and easier, as it avoids opening the condyle. Access to the
medial vestibular nucleus are supplied by these branches brainstem may be anterior to the olive, posterior to the
[55]. olive, or sometimes through the olivary body, preferably
in the postero-olivary sulcus (Figs. 20 and 21). It is pos-
Anterior medulla sible to enter the medulla via the anterolateral sulcus. This
entry zone is along the pre-olivary sulcus, between the
The medulla is perhaps the most difficult structure to be caudal hypoglossal and the rostral C1 rootlets. It lies very
approached, due to the high density of nuclei located near the pyramidal tract, next to its decussation, and
therein, the cranial nerve pairs from IX to XII. Lesions should be used only for exophytic lesions [9]. The retro-
located in the anterior portion of the medulla are accessed olivary sulcus is a safe entry area. According to Recalde
via a far-lateral approach. This approach was initially de- et al. [53], the olivary body offers a surgical space of
scribed by Heros [27] and by George et al. [21] among approximately 13.5 mm in the craniocaudal axis, 7 mm
Childs Nerv Syst (2015) 31:1815–1840 1831

Fig. 18 a, b 5-year-old patient

with pontine lesion approached
by infrafacial entry point. c,
d 8-year follow-up. Pilocytic
astrocytoma

in the transverse axis, and 2.5 mm in the anterodorsal of medullary lesions on the right side and bradycardia for
axis. The entry zone is through the post-olivary sulcus medullary lesions on the left side.
located between the olive and the inferior cerebellar pe-
duncle ventral to the glossopharyngeal and vagus rootlets
[53]. Results

From 1991 to 2011, we evaluated 303 patients less than

Posterior medulla 18 years old with tumors located in the brainstem treated in
the Pediatric Neurosurgery Service and Institute of Pediatric
Intrinsic lesions in the posterior part of the medulla are diffi- Oncology of São Paulo Federal University. Ninety-six cases
cult to approach due to the huge quantity of nuclei in that were diffuse tumors that underwent chemotherapy/radiother-
region. On the other hand, most of lesions therein have an apy. The first author of this article operated on the remaining
exophytic component, which facilitates the access. These tu- 207 patients, which corresponds to 9.1 % of all patients oper-
mors are called cervico-medullary. Medullary lesions inferior ated by this service in the same period (2015 patients). Ages
to the obex may be accessed via the midline through the pos- ranged from 8 months to 18 years, with a mean age of 10 years.
terior median sulcus, as are the intramedullary lesions. All Bsafe zones^ previously described were used in these pa-
In the intraoperative period, severe vegetative alterations tients, and a new Bsafe zone,^ termed supratrigeminal, was
may occur, such as hypertension and tachycardia in the case used in three patients for tumors of the anterior and superior
1832 Childs Nerv Syst (2015) 31:1815–1840

Fig. 19 a Schematic representation of the medulla at the olive level, with vestibulocochlear nerves with the brainstem. The glossopharyngeal,
the presence of the IX, X (green and pink), XI, and XII (red) cranial pairs vagus, and accessory nerves exit the medulla just dorsal to the
nuclei and topography of the corticospinal tract (yellow), which is much postolivary sulcus, which is located between the olive and inferior
nearer to the midline as compared to the pons and the midbrain. b Ventral cerebellar peduncle (ICP). The hypoglossal rootlets exit the medulla
medulla. The safe entry zones in the ventral medulla are the preolivary along the preolivary sulcus. c The far lateral approach used for pre- and
and postolivary sulci. The preolivary sulcus is located between the olive post-olivary sulci. d Dorsal medulla. The posterior median (PMS),
and the pyramid, which houses the CST. The depression rostral to the intermediate (PIS), and posterolateral (PLS) sulci have been proposed
olive, the supraolivary fosette, is just below the junction of the facial and as the safe entry zones. The suboccipital median approach

pons. One hundred patients were operated without intraoper- was lateral to the third nerve (perioculomotor access).
ative monitoring, while 107 cases were monitored. The 207 Regarding the central midbrain (59 cases), 53 patients were
operated cases are summarized in the Table 1. approached using a supracerebellar infratentorial entry in the
Eighty-four patients had midbrain tumors. Sixteen were sitting position, with 41 cases median and 12 paramedian. In
located in the anterior portion of the midbrain, 59 in the central six patients, access was achieved through a combined median
midbrain, and nine in the quadrigeminal plate. Six patients supracerebellar infratentorial route with sub-occipital telovelar
with tumors located in the anterior portion extending to the access through the rhomboid fossa. For the medial
third ventricle were operated on by pure neuroendoscopy, supracerebellar infratentorial approaches, the pre-central cer-
coupled with an ultrasonic aspirator device (Sonoca 300 and ebellar vein was coagulated in all the cases, and no complica-
92–030 micro handpiece—Söring). All of the lesions were tion ensued. In the paramedian access, coagulation of the pre-
exophytic, and there was no need to incise the brainstem. central cerebellar vein was not necessary, and the entry point
The tumors did not bleed much and could be easily aspirated to the brainstem was through the lateral mesencephalic sulcus.
with the ultrasonic aspirator at low power. The main clinical Two patients had air embolisms, and aspiration through a cen-
manifestation in these patients was intracranial hypertension tral venous catheter was needed to resolve the issue. The air
due to hydrocephalus. All tumors were pilocytic astrocyto- entry point was in the transverse sinus adjacent to the sigmoid
mas, and removal was completed with no case requiring a sinus, which is the highest and most lateral point of opening in
ventricular shunt. Ten patients with tumors in the anterior t h e d u r a m a t e r. Te n p a t i e n t s h a d h y p e r t e n s i v e
portion of the midbrain extending to the interpeduncular fossa pneumoventricles, of which two underwent neuroendoscopy
were operated via the transsylvian approach. Six accesses for treatment. Two patients had rubral tremors controlled with
were achieved via classic pterional for exophytic tumors and clonazepam. Nine patients had tumors in the quadrigeminal
four via fronto-orbito-zygomatic, and access to the brainstem lamina, eight of whom were operated via three-quarters prone,
Childs Nerv Syst (2015) 31:1815–1840 1833

Fig. 20 a, b 2-year-old patient

evolving to tetraparesis. A large
tumor anterior to the medulla is
present. The far lateral approach
and trans-olivary point of entry
was used for resection of a
pilocytic astrocytoma. c, d
Eleven-year follow-up, showing
no evidence of tumor

and one via a combined infratentorial supracerebellar and sub- through the rhomboid fossa with patients in the prone posi-
occipital telovelar approach. All tumors of the midbrain were tion. Forty-five tumors in the superior and posterior pons were
low-grade astrocytomas, most of them pilocytic astrocytomas. approached by a suprafacial pathway, and three cases using an
Of 168 patients presenting with pontine tumors, 96 were interfacial pathway above the facial colliculus. In six patients
diffuse and not operated upon. Seventy-two tumors in this operated using a suprafacial route, there was injury of the
topography were operated. Four cases had tumors located in medial longitudinal fasciculus and facial paresis in three cases.
the anterior and superior pons, seven in the anterior and infe- In all cases, the symptoms regressed 6 months after surgery.
rior pons, 48 in the superior and posterior pons, and thirteen in One patient developed acute hydrocephalus and died 3 days
the inferior and posterior portion later. In the three cases operated on using the interfacial path-
Three tumors located in the anterior and superior pons were way, two developed symptoms of medial longitudinal fascic-
operated on using a fronto-orbital-zygomatic route with the ulus injury that disappeared within 6 months. No facial nerve
brainstem entry point being supratrigeminal, between the third involvement was observed. Thirteen patients had tumors in
cranial nerve and trigeminal nerve, 4 mm below to the the posterior and inferior portion of the pons and were oper-
mesencephalon-pontine sulcus. One case was operated on ated on via the infrafacial route. Eight of these patients had
using the pre-sigmoid approach. None of these patients with facial paralysis, with five cases resulting in permanent paral-
tumors in the anterior and superior portion of the pons had ysis. Twenty-two cases were grade III and grade IV astrocy-
morbidity. In seven cases, the tumors were situated in the tomas, while 50 cases were low-grade astrocytomas.
anterior and inferior portion of the pons and were accessed Fifty-one patients had medullary tumors, with 11 located in
via a presigmoid route. Forty-eight tumors were located in the the anterior and 40 at the so-called cervicomedullary junction.
posterior and superior pons, while thirteen were located in the Anterior tumors were accessed using a far-lateral approach
posterior and inferior pons. All tumors located in the dorsal with an entry point through the olivary medullary route, or
part of the pons were operated on using a telovelar route where the exophytic tumor resided. Dentate ligament
1834 Childs Nerv Syst (2015) 31:1815–1840

Fig. 21 a, b Cervico-medullary
tumor with exophytic extension in
the fourth ventricle. c, d MRI at
5 years after surgery shows no
evidence of tumor

resection was performed in all cases using this route. grade gliomas was 18 months. Table 1 summarizes the pa-
Cervicomedullary junction tumors were operated on using a tients and the safe zone entrance used in the 207 patients.
telovelar route with the medulla incised longitudinally in the
midline. Nine patients showed worsened breathing and
swallowing. Three patients remained in respiratory failure
and died of pneumonia within 2 months of surgery. Two pa- Discussion
tients required permanent tracheostomy due to vocal cord in-
coordination. Of the medullary tumors, eight were Tumors of the brainstem are more common in children than in
gangliogliomas, three were hemangioblastomas, 29 were as- adults. Few publications address surgical approaches to
trocytomas, eight were grade III and IV astrocytomas, and 21 brainstem tumors in children. Most of them are related to
were low-grade astrocytomas. brainstem approaches for surgical treatment of cavernomas.
For the entire series of 207 surgically treated tumors of the Surgery for removal of a cavernoma in this location is far
brainstem, operative mortality seen in the first 2 months after different from surgery to remove a brainstem tumor. A pecu-
surgery was 1.9 % (four patients) and surgical morbidity oc- liar feature of cavernomas is that the cavity produced by wid-
curred in 21.2 % (45 cases). All tumors of the midbrain in our ening Virchow-Robin spaces and the consolidation of clots
series were low-grade astrocytomas. In the pons, 50 had low- causes a large space after the removal of the clot, facilitating
grade astrocytomas, and 22 were high-grade tumors. Of 51 cavernoma resection. Therefore, small incisions at the surface
medullary tumors, only eight were high-grade astrocytomas. of the brainstem are sufficient to remove bulky cavernomas. In
Thus, of 207 children with tumors of the brainstem, 30 pediatric tumors of the brainstem, the first disadvantage is
(14.4 %) were high-grade tumors, while 177 were of low working on a very small structure compared to the brainstem
grade of malignancy. The follow-up ranged from 3 to 20 years of an adult, except with rare cystic lesions. On the other hand,
with a mean of 13 years. The disease-free survival (5 years) many tumors are exophytic, allowing for complete removal
for benign tumors was 92 %, while median survival for high- without incising the brainstem.
Childs Nerv Syst (2015) 31:1815–1840 1835

Table 1 Distribution of the 207 operated cases according to topography, approach, safe zone entry point, and morbidity/mortality

Topography Division Approach Safe zone entry point Morbidity/mortality

Midbrain (84) Anterior (16) Transventricular transforaminal Exophytic lesion None

endoscopic approach (6)
Pterional or fronto-obito zygomatic transylvian Peri-oculomotor (10) None
approach (10)
Median (59) Infratentorial supracerebellar (53) Median (41) Supracollicular and/or -Air embolism (2)
infracollicular -Hypertensive
Paramedian (12) Lateral mesencephalic sulcus Pneumoventricles (10)
-Rubral tremor (2)
Infratentorial supracerebellar combined with Supracollicular and/or None
telovelar approach (6) infracollicular
Posterior (9) Occipto-transtentorial (8) Exophytic lesion None
Infratentorial supracerebellar combined with
telovelar approach (1)
Pons (72) Anterior (11) Fronto-obito zygomatic transylvian approach (3) Supratrigeminal (3) None
Presigmoid (8) Peritrigeminal (8) None
Posterior (61) Suboccipital craniotomy with telovelar approach (61) Suprafacial (45) -MLFI (6)
-Facial paresis (3)
-Death (1)
Interfacial (3) -MLFI* (2)
Infrafacial (13) Facial paresis (9)
Bulb (51) Anterior (11) Far-Lateral Approach (11) Transolivar None
Posterior (40) Suboccipital craniotomy with Telovelar approach (40) Midline -Death (3)
-Breathing and swallowing
impairment (9)
-Vocal cord incoordination (2)

MLFI medial longitudinal fasciculus injury

Improvements in diagnosis, with high resolution MRI Cantore et al. [9] divided the brain stem into two surgical
combined with tractography, are very helpful for surgical de- planes—the anterior and the posterior. Thus, they classify six
cisions as well as for the choice of the safest and more precise regions in the brain stem. Our reason for dividing the mesen-
surgical approach. Advances of neuroanesthesiology, intraop- cephalon into three portions is because the quadrigeminal
erative electrophysiological monitoring, and intensive postop- plate tumors characteristics are different from those of the
erative care, give more security, allowing for more aggressive anterior and central midbrain. Most tumors in the
surgical excisions and preventing damage [61]. quadrigeminal plate are indolent and rarely have to be operat-
Neurosurgical instruments have also evolved signifi- ed upon, restricting treatment to hydrocephalus control [13].
cantly. Today, we have microscopes with high brightness Four Bsafe entry zones^ for the midbrain have been de-
and such definition as to allow improved recognition of scribed. The most complex and anterior, called the
where the tumor ends and normal tissue begins. Lighter perioculomotor zone, has been described by Bricolo et al.
and more delicate instruments with diamond tip scalpels [8] There is a space between the oculomotor nerve and the
allow precise incisions of the brainstem. The routine use pyramidal tract which can be accessed through an incision
of ultrasonic surgical aspirators with 1-mm tips allows us parallel and lateral to the oculomotor nerve. The presence of
to remove large lesions through small openings in the a tumor may increase this distance, facilitating surgery. When
brainstem. Surgical planning of the most appropriate tumors have an exophytic component, the brainstem can be
means of access, associated with intrinsic and extrinsic directly entered through the tumor. Clinically, these patients
knowledge of brainstem anatomy, is also key to achieving present preoperatively with third cranial nerve paralysis and
success in surgery. contralateral pyramidal involvement (Weber syndrome) that
The brainstem is routinely divided into three parts: mid- usually disappears quickly after lesion removal. Small tumors
brain, pons, and medulla [41]. We further divided the only cause diplopia.
brainstem into seven parts: anterior, central, and posterior In our series, 16 tumors were located in the anterior portion
midbrain; anterior and posterior pons; and anterior and poste- of the mesencephalon. Six were growing towards the III ventri-
rior medulla, which helped us to choose the best surgical ap- cle and were operated on by pure neuroendoscopy, coupled with
proaches [11, 12]. an ultrasonic aspirator device. We found few literature reports of
1836 Childs Nerv Syst (2015) 31:1815–1840

brainstem tumor resection using purely neuroendoscopic preventing further exposure of the cerebellum to avoid possi-
methods. Miki et al. have used the neuroendoscopic trans-third ble herniation. In our series, we had no cerebellar herniation.
ventricle approach in six cases for lesions of the ventral The vermian veins, which are bridging veins between the
brainstem surface [45], but just in one case for brainstem tumor. tentorial face of the cerebellum and the tentorial and transverse
In ten patients of our series, tumors grew towards the sinus, were coagulated without any complication [55]. When
interpeduncular cistern. Six of these tumors were exophytic, necessary, we also coagulated the precentral cerebellar vein
large, and were approached by a classic pterional route with without any clinical repercussions. In two cases, the patients
opening of the Sylvian fissure and lesion removal. Wide open- had a symptomatic air embolism which was resolved with
ing of the Sylvian fissure in young children is sometimes blood aspiration though the central line and identification of
difficult, and simple delicate manipulation can cause vaso- the venous opening in the apex of the dura mater incision
spasm, thus papaverine is often used. In four patients, the close to the transverse sinus.
tumors were intrinsic, and the brainstem was approached Nine patients with quadrigeminal plate tumors underwent
through the perioculomotor route. In all the cases, a fronto- surgery, eight via the occipital transtentorial route and one
orbito-zygomatic approach was used. We may also use the through combined infratentorial supracerebellar and
temporopolar access described by Sano in 1980 [58], which suboccipital telovelar routes. In four cases, entries were
provides an anterolateral view of the interpeduncular fossa. supracollicular, and five were infracollicular, above the fourth
These are the access routes we use for the anterior portion of cranial nerve. For tumors of the central or posterior portion of
the midbrain, entering through the third ventricle, or through the midbrain growing in the direction to the third ventricle, we
the perioculomotor space. Konovalov and Kadyrov [35] pro- used the supracerebellar infratentorial approach. For tumors
posed a transchoroidal temporal access to these anterolateral growing into the fourth ventricle, we use a transtentorial oc-
lesions located in the midbrain, especially on the dominant cipital access in the three-quarter position. When the lesions
side and when tumors extend to the ambient cistern. The fact grew into the third and fourth ventricles, we used the com-
is these lesions are quite rare in this topography. In our series, bined access route.
only 7 % of the tumors considered surgical were located in the Ogata and Yonekawa [47] proposed a paramedian
anterior portion of the midbrain. Although Albright 1993 [2] infratentorial supracerebellar access route for lesions of the
reported that only 7 to 8 % of brainstem tumors are located in superior, intermediate, and lower cerebellar peduncle. They
the midbrain, in Yasargil’s [64] series of 167 brainstem tu- demonstrated that it is possible to open the surface of the
mors, 26 (15.5 %) were located in the midbrain, double that intermediate cerebellar peduncle lateral to the cerebellar mes-
reported by Albright [2]. Garzon et al. [20] found that 33.8 % encephalic fissure.
of brainstem tumors were located in the midbrain. In our series The approaches to the anterior portion of the pons are the
of 207 cases considered surgical, 84 were located in the mid- most difficult. Bagahai et al. [5] have described a safe entry
brain (40.5 %), but if we consider all cases of brainstem tu- zone to the ventrolateral portion of the pons between the out-
mors treated by our service, this rate drops to 27.7 %. We put points of the fifth and seventh cranial nerves. This corri-
believe this is because we are a neurosurgical center of refer- dor, however, is very narrow and is good only for biopsy or
ence, not being forwarded cases of diffuse pontine tumors. removal of cavernomas in that region. This access can be
Of 59 patients with central midbrain tumors operated reached via an occipital paramedian approach or through a
through an infratentorial supracerebellar routes described by petrous access. In other access routes to the anterior pons,
Krause in 1911 [36], 41 had a median and 12 a paramedian the region around the emergence of the fifth cranial nerve is
route. When approaching via the paramedian route, we used a Bsafe^ area that may be opened 1 cm wide and 1 cm from the
the same access as the median approach; the only difference midline. However, one should be careful not to go further
being that the brainstem is accessed via the lateral mesence- anterior to avoid the corticospinal tract.
phalic sulcus. Six patients had tumors growing not only to- Eleven of our patients had tumors in the anterior pons. Four
wards the third ventricle but also towards the fourth ventricle, were anterior and superior, and seven were anterior and infe-
and they were operated on, via a combined approach, namely rior. Three anterior and superior tumors were accessed via a
an infratentorial-supracerebellar followed by a suboccipital fronto-orbito-zygomatic approach, and the point of entry into
telovelar approach across the fourth ventricle. All patients the lesion was a vertical incision, 4 mm inferior to the
were operated on in the sitting position with the head bent. mesencephalopontine sulcus in the same direction as the third
Wide craniotomy of the posterior fossa was performed and the nerve. In three patients operated using this route, there was no
dura opened to avoid the occipital sinus, which is usually increased morbidity. This approach does not have a similar
patent in young children. The C1 arch was removed in all description in the literature, and we prefer to call it
cases. Yasargil [64] advocates a different access to this region Bsupratrigeminal access^ to differentiate it from peritrigeminal
by not removing the arch of C1 and opening the dura mater access between the fifth and seventh cranial nerves. In fact,
2 cm below and parallel to the transverse sinus, thus this new entry point is between the third and fifth cranial
Childs Nerv Syst (2015) 31:1815–1840 1837

nerves medial to the pyramidal tract. Other tumors of the ven- longitudinal fasciculus was injured in two patients.
tral pons were approached using a pre-sigmoid route, with Thirteen patients with inferior pons tumors were operated
ligature of the superior petrosal sinus. on through the infrafacial triangle. Eight patients operated
Sixty-one tumors were located in the posterior pons, 48 by this route developed facial paralysis, which was perma-
of them being superior and 13 inferior. The superior tumors nent in five of them. We believe that this route should be
were approached either via the suprafacial triangle as pro- reserved only for small exophytic tumors or cavernomas.
posed by Kyoshima et al. [39], or, in lateral cases, through Access through the rhomboid fossa, below the medullary
the lateral sulcus limitans. In three patients, because of striae, should also be avoided as this region has a high
distortion caused by the tumor in the rhomboid fossa, it density of cranial nerve nuclei. All access to the rhomboid
was extremely difficult to locate an entry point by stimu- fossa was performed using a suboccipital route with the
lating the facial nerve. Therefore, the entry point was an removal of the C1 arch and telovelar approach, sometimes
interfacial access superior to the facial colliculus, as de- bilaterally, to avoid opening the cerebellar vermis. The
scribed by Bricollo and Taruzzi [7]. However, the medial patient’s position was ventral decubitus.

Transventricular
transforaminal
Exophytic Lesion
endoscopic approach
(6)
Anterior (16)
Pterional or Fronto-
Orbito zygomatic Peri-Oculomotor
approach (10)

Supracollicular and or
Median (41)
Infracollicular
Infratentorial
Supracerebellar
approach (53)
Midbrain Lateral Mesencephalic
Paramedian (12)
(84) Sulcos
Median (59)

Infratentorial
Supracerebellar Supracollicular and/or
combined with telovelar Infracollicular
approach (6)

Infratentorial
Supracerebellar
Exophytic Lesion
combined with telovelar
approach (1)
Posterior (9)

Occipto-transtentorial
Exophytic Lesion
(8)

Fronto-orbito
Zygomatic Transsylvian Supratrigeminal
approach (3)
303 Patients Anterior (11)

Presigmoid (8) Peritrigeminal

Non-Difuse Pontine
Suprafacial
Gliomas (72)
Pons
(168)
Difuse Pontine Gliomas
Interfacial
(96)
Subocciptal craniotomy
Posterior (61) with telovelar approach
(61)
Infrafacial

Far Lateral Approach

Anterior (11) Transolivar
(11)
Medulla Limitans Lateral Sulcus
(51) of the rhomboid fossa
Subocciptal craniotomy
Posterior (40) with telovelar approach Midline
(40)

Fig. 22 The algorithm to approach the safe zones

1838 Childs Nerv Syst (2015) 31:1815–1840

Medullary tumors present the same technical difficulty as tumors are more frequent in childhood than in adult life.
the tumors of the pons. The anterior ones were approached via Although imaging with tractography has evolved significant-
suboccipital far lateral craniotomy with removal of the C1 ly, they still do not show the nuclei and nerve pathways inside
arch and section of the dentate ligamentum which is close to the brainstem. Anatomic dissection by the Klingler’s tech-
the vertebral artery entry into the skull. That section of the nique to study white fibers has helped neurosurgeons in plan-
ligament has permitted further mobility of the medulla, facil- ning the three-dimensional architectural design of surgical ap-
itating identification of the olivary body and entry into the proaches [1, 34]. There are eleven previously described Bsafe
brain stem through the posterior olivary sulcus (or transolivary entry zones^ in the brainstem: perioculomotor, the lateral mes-
entry). Right-sided medullary access usually produced intra- encephalic sulcus, infracollicular access, supracollicular ac-
operative hypertension and tachycardia, whereas access from cess, peritrigeminal, suprafacial, interfacial, infrafacial, lateral
the left side produced bradycardia. These natural alarms must sulcus limitans, periolivary, and the posterior median sulcus.
not be suppressed with drugs, such as atropine or hypotensive A new safe entry zone has been used in three of our patients,
drugs, because they reveal that we are manipulating the the Bsupratrigeminal^ zone, for approaching anterior and su-
brainstem too aggressively. These are indirect physiological perior pontine lesions. Fig. 22 summarizes the algorithm to
alarm that requires attention. Usually, these vegetative storms approach the safe zones. Maybe in the near future, with the
occur when the lesion is under traction, which should be improvement of high- resolution 7 Tesla MRI, or another
avoided. Instead, we should remove the tumor using an ultra- type of imaging able to show the precise deviations caused
sonic aspirator, avoiding traction. These small vegetative in the brain stem structures by effect of the tumors, coupled
storms are not reasons to interrupt procedures, because they with a more efficient electrophysiological monitoring sys-
cease immediately upon stopping the traction and irrigation tem, this kind of surgery may become simpler with less
with warm saline. morbidity. Currently, more accurate knowledge about
Lesions situated in the posterior portion of the medulla intrinsic/extrinsic anatomy of the brainstem associated
were also operated via occipital telovelar approach, the me- with more sophisticated tools, like high-resolution micro-
dulla being reached opening the midline below the obex, scopes and ultrasonic aspirators with thinner tips, have
through the posterior medial sulcus. allowed us to remove a large number of brainstem tumors
There are eleven previously described Bsafe^ entry zone with acceptable mortality and morbidity rates from any
areas in the brainstem. In this article, we describe another topography in this wonderful cerebral structure.
zone, the Bsupratrigeminal,^ for anterior and superior pons
lesions. This route was used in three patients and showed no Acknowledgments The authors wish to thank Mrs Blanche Torres for
morbidity. It is therefore a reasonable access route. However, a helping us to write this manuscript and Mr. StharMar de Vasconcelos
fronto-orbito-zygomatic access is needed for wide visualiza- Silva for the artistics drawings.
tion of the mesencephalopontine sulcus and the third cranial
Conflict of interest The authors declare that they have no competing
nerve. interest.
It is up to neurosurgeons to choose correctly pathways for
complete lesion resection with a minimum morbidity. Financial and material support None.
However, morbidity is still high (22 % in our series).
Open Access This article is distributed under the terms of the Creative
Hydrocephalus is always a catastrophic complication in the
Commons Attribution 4.0 International License (http://
postoperative period of brainstem tumors, and the neurosur- creativecommons.org/licenses/by/4.0/), which permits unrestricted use, dis-
geon should always be aware of this possibility. One of our tribution, and reproduction in any medium, provided you give appropriate
patients died of hydrocephalus. Thus, whenever possible, we credit to the original author(s) and the source, provide a link to the Creative
Commons license, and indicate if changes were made.
place an external ventricular drain that is removed in the first
48 h postoperatively.
The brainstem does not permit either traction or coagula-
tion; thus, we routinely use ultrasonic aspirators with little References
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