Surgical approaches for brainstem tumors in pediatric patients
- 3.4k Downloads
To analyze the pathways to brainstem tumors in childhood, as well as safe entry zones.
We conducted a retrospective study of 207 patients less than 18 years old who underwent brainstem tumor resection by the first author (Cavalheiro, S.) at the Neurosurgical Service and Pediatric Oncology Institute of the São Paulo Federal University from 1991 to 2011.
Brainstem tumors corresponded to 9.1 % of all pediatric tumors operated in that same period. Eleven previously described “safe entry zones” were used. We describe a new safe zone located in the superior ventral pons, which we named supratrigeminal approach. The operative mortality seen in the first 2 months after surgery was 1.9 % (four patients), and the morbidity rate was 21.2 %.
Anatomic knowledge of intrinsic and extrinsic brainstem structures, in association with a refined neurosurgical technique assisted by intraoperative monitoring, and surgical planning based on magnetic resonance imaging (MRI) and tractography have allowed for wide resection of brainstem lesions with low mortality and acceptable morbidity rates.
KeywordsPediatric brainstem gliomas Brainstem surgery Safe entry zone White fiber anatomy Supratrigeminal approach Low-grade astrocytoma
The brainstem is one of the most complex structures in the human body and contains the most complex intracranial anatomy . This compact, midline organ is protected anteriorly by the clivus, laterally by the petrous part of temporal bone, superiorly by the diencephalon, and posteriorly by the cerebellum. All motor, sensory, sympathetic, and parasympathetic brain functions are integrated and travel through the brainstem. The structural complexity of the brainstem makes surgical procedures there in extremely difficult and require a perfect technique. Brainstem tumors are more common in children and represent up to 18 % of childhood brain tumors and 25 % of posterior cranial fossa tumors. There is no gender predilection. The mean age incidence for these tumors occurs around age 5 to 10 years . A second peak of incidence is seen in adults between 30 to 40 years of age. In recent years, several articles have been published on brainstem anatomy and “safe entry zones.” Most of these are related to cavernoma surgery and few are related to brainstem tumor surgical approaches in children [9, 19, 22, 26, 53]. The aim of this study was to review the described surgical approaches and those conducted by the first author (Cavalheiro, S.) of this article on the basis of 207 patients aged less than 18 years who underwent brainstem tumor surgery.
The various arrangements of fibers, Virchow-Robin spaces, and structures comprising the brainstem occasionally allow tumors to grow considerably with few symptoms. This may permit diffuse pontine tumors to grow within the pons without infiltrating the mesencephalon or medulla. When midbrain tumors grow, they spread towards the thalamus and do not infiltrate the pons. Tumors of the medulla tend to grow into the fourth ventricle without invading the pons, or grow caudally towards the spinal cord.
Many classifications have been proposed for brainstem tumors. We used that proposed by Choux et al.: type I, diffuse brainstem gliomas; type II, focal intrinsic tumors (solid or cystic); type III, exophytic; and type IV, cervicomedullary [14, 15, 17].
Diffuse tumors (type I)
Diffuse tumors are the most common, representing up to 80 % of brainstem tumors. They simultaneously affect multiple nuclei and pathways, and characteristically cause bilateral paralysis of cranial nerves VI and VII, progressing to hemiparesis and tetraparesis. They present with rapid clinical evolution, and as far as histopathology is concerned, most are malignant astrocytomas (WHO) grade III or IV. Radiologically, they are characterized by pontine enlargement with an entrapped basilar artery. They are hypointense on T1 magnetic resonance imaging (MRI), hyperintense on T2, hyperintense on FLAIR, and exhibit minimal contrast enhancement [6, 44].
Survival of these patients is short, and most die within the first 2 years after diagnosis. However, a few cases may respond to chemotherapy and radiation. There is no difference in prognosis using conventional or multi-fractionated radiotherapy. Metastases of the neuraxis may occur in 5 to 30 % of cases [10, 18, 25].
Stereotactic biopsy of diffuse brainstem tumors has been performed in a few centers. Its use is important mainly for molecular biology studies [52, 57, 62]. However, biopsies are associated with some complications. Pincus et al. (2006)  conducted a retrospective study of 182 stereotactic biopsy cases from 13 published reports of diffuse pontine lesions in children. They noted that tumor diagnosis was verified in 75 to 100 % of cases. In 87 % of cases, the lesions were gliomas, while the remaining 13 % were primitive neuroectodermal tumors, neurocytomas, ependymomas, and demyelinating lesions. 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 [32, 59]. Stereotactic biopsies can be performed through entry points in the frontal region or through the posterior fossa.
Focal tumors (type II)
Focal tumors behave differently from diffuse tumors. They are slow-growing lesions, and the symptomatology is indolent. They may be solid or cystic and, contrary to diffuse tumors, local lesions have well-delimited borders. Less edema is associated with focal tumors, which are mainly low-grade gliomas. They are usually hypointense on T1, with diffuse tumoral enhancement. Impregnation with gadolinium varies in focal tumors; however, homogeneous enhancement is highly suggestive of pilocytic astrocytoma .
If the tumor is superficial, surgery is advised; however, if it is deep, the treatment should be conservative, in the expectation that the tumor itself may provide an “opening door” for its resection. The use of tractography has allowed for better choices regarding surgical approaches to these tumors. Tumors in the quadrigeminal plate are usually focal and mostly pilocytic astrocytomas .
Exophytic tumors (type III)
Exophytic tumors are more accessible surgically. They tend to be large tumors with a large component out of the brainstem, facilitating surgery. They may have a cystic component, another factor that facilitates its resection. They are mostly low-grade astrocytomas .
Cervicomedullary junction tumors (type IV)
Cervicomedullary junction tumors often present as an exophytic growth, allowing surgeons direct access without incising the brainstem. These lesions usually do not infiltrate the pons and grow cranially into the fourth ventricle. They may extend caudally into the spinal cord. When growing toward the fourth ventricle, hydrocephalus may occur early on. When growing towards the spinal cord, they may produce syringomyelia, due to changes in cerebrospinal fluid dynamics. Although surgical approaches are facilitated by topography, these are cases that most often progress with serious morbidity. Postoperatively, these patients may have difficulty breathing, resulting in long periods of assisted mechanical ventilation, and swallowing difficulties, which in turn may cause severe aspiration pneumonia. Patients may require tracheostomy and gastrostomy, necessitating speech therapy. The use of electrophysiological monitoring during surgery has helped to prevent those complications .
Patients and methods
From 1991 to 2011, 303 patients younger than 18 years with brainstem tumors were treated by the Neurosurgical Service and Pediatric Oncology Institute of the Federal University of Sao Paulo. Of these, the first author of this article surgically treated 207. The remaining 96 cases were diffuse tumors. Here, we describe the surgical approaches and relevant extrinsic/intrinsic anatomical points used.
The midbrain was divided into three parts: anterior, central, and posterior. The anterior segment is delimited posteriorly by the substantia nigra. The central midbrain extends from the substantia nigra to the aqueduct. The posterior part is restricted to the quadrigeminal plate. The pons was divided into two segments: anterior and posterior, or ventral and dorsal. Similarly, the medulla was divided into anterior and posterior, or ventral and dorsal, partitions. Detailed knowledge of the brainstem extrinsic and intrinsic anatomy is essential to avoid morbidity during the surgical approaches.
From the pericollicular access point, two “safe zones” can be accessed: an incision made in the midbrain below the inferior colliculus, or infracollicular access, and above the trochlear nerve, or supracollicular access. In the supracollicular approach, a transverse incision is made just above the superior colliculus and should be limited by the aqueduct. Further extension in this approach can damage the nuclei of cranial nerves III and IV, as well as the medial longitudinal fasciculus. With infracollicular access, a transverse incision between the trochlear nerve and the lower edge of the inferior colliculus is performed. As for the supracollicular route, an incision deeper than the cerebral aqueduct will damage the nuclei of the third and fourth cranial nerves and the medial longitudinal fasciculus. More lateral extensions of this incision will damage the superior cerebellar peduncle, the trigeminal mesencephalic tract, and the decussation of the superior cerebellar peduncle.
For lesions extending towards the fourth ventricle, we can incise the quadrangular lobe of the cerebellum for greater access to the cerebellar mesencephalic fissure. In this approach, it is essential to have a spatial imagination of the third and fourth nerves nuclei, as well as of their course inside the midbrain.
The ultrasonic aspirator is extremely important in that situation, and the color of the tumor is also most helpful in achieving total resections. Some tumors, however, are the same color as the brainstem, and then the surgeon has to rely on the position of the fibers, as well as on the tumor texture and circulation. Tumors are usually softer than the normal brain stem and also more vascularized, which makes it easier to remove them.
Posterior (dorsal) midbrain
Posterior midbrain or quadrigeminal plate is the name given to the portion of the midbrain that is posterior to the cerebral aqueduct. The tumors of the quadrigeminal plate are the smallest brain tumors liable to kill the patient from hydrocephalus. They account for approximately 5 % of pediatric tumors of the brain stem . They are usually indolent lesions and the treatment is limited to the treatment of hydrocephalus. Most of the time, these tumors are isointense on T1-weighted and hyperintense on T2-weighted images. Up to 19 % of cases may have gadolinium-enhanced MRI .
This approach is mainly recommended for tumors having a large superior and lateral extension, with the displaced venous complex impairing the view of the tumor through a posterior medial pathway.
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.
Most pontine tumors are diffuse; therefore, resective surgery is not beneficial and chemotherapy/radiotherapy is indicated. Neurosurgeons must differentiate between focal, low-grade exophytic, and diffuse tumors for patients to benefit from surgery.
This is a much smaller triangle and the safe distances are not always the same, so that intraoperative monitoring is mandatory. The safe area to access the infracollicular triangle as described by Kyoshima et al.  would begin on average 6.5 mm above the obex and would extend for 9.2 mm in the cranial-caudal direction; the supracollicular triangle would be on average 22.5 mm above the obex, with an extension of 13.6 mm.
We have used a third approach, when no space is found in the rhomboid fossa, namely the interfacial approach. Bricolo and Turazzi  have described the midline access in the rhomboid fossa as being possible at the level of the facial colliculi, next to the nucleus of the sixth nerve, since the fibers of the medial longitudinal fasciculi are not yet crossed at this level. In this approach, the medial longitudinal fasciculus is damaged, which may disturb the conjugate movement of the eyes. From the surgical point of view, we have used a bilateral telovelar approach, with coagulation of the choroid plexus of the fourth ventricle, which allows for ample access from the obex to the cerebral aqueduct without need to harm the cerebellar vermis.
More lateral lesions have been approached through the lateral sulcus limitans, also via a telovelar approach .
Lawton et al.  have proposed a supratonsillar approach to the inferior cerebellar peduncle, without the need to open the IV ventricle and perform an expanded telovelar approach. This route has been described for cavernomas, but it can be sufficient for tumoral lesions of the inferior cerebellar peduncle extending to the midline. This technique is best used with the aid of neuronavigation.
Therefore, for the pons, we have the following “safe zones”: supratrigeminal, peritrigeminal, suprafacial, infrafacial, interfacial, and through the lateral sulcus limitans.
Intrinsic lesions in the posterior part of the medulla are difficult to approach due to the huge quantity of nuclei in that region. On the other hand, most of lesions therein have an exophytic component, which facilitates the access. These tumors are called cervico-medullary. Medullary lesions inferior to the obex may be accessed via the midline through the posterior median sulcus, as are the intramedullary lesions.
In the intraoperative period, severe vegetative alterations may occur, such as hypertension and tachycardia in the case of medullary lesions on the right side and bradycardia for medullary lesions on the left side.
Distribution of the 207 operated cases according to topography, approach, safe zone entry point, and morbidity/mortality
Safe zone entry point
Transventricular transforaminal endoscopic approach (6)
Pterional or fronto-obito zygomatic transylvian approach (10)
Infratentorial supracerebellar (53)
Supracollicular and/or infracollicular
-Air embolism (2)
-Rubral tremor (2)
Lateral mesencephalic sulcus
Infratentorial supracerebellar combined with telovelar approach (6)
Supracollicular and/or infracollicular
Infratentorial supracerebellar combined with telovelar approach (1)
Fronto-obito zygomatic transylvian approach (3)
Suboccipital craniotomy with telovelar approach (61)
-Facial paresis (3)
Facial paresis (9)
Far-Lateral Approach (11)
Suboccipital craniotomy with Telovelar approach (40)
-Breathing and swallowing impairment (9)
-Vocal cord incoordination (2)
Eighty-four patients had midbrain tumors. Sixteen were located in the anterior portion of the midbrain, 59 in the central midbrain, and nine in the quadrigeminal plate. Six patients with tumors located in the anterior portion extending to the third ventricle were operated on by pure neuroendoscopy, coupled with an ultrasonic aspirator device (Sonoca 300 and 92–030 micro handpiece—Söring). All of the lesions were exophytic, and there was no need to incise the brainstem. The tumors did not bleed much and could be easily aspirated with the ultrasonic aspirator at low power. The main clinical manifestation in these patients was intracranial hypertension due to hydrocephalus. All tumors were pilocytic astrocytomas, and removal was completed with no case requiring a ventricular shunt. Ten patients with tumors in the anterior portion of the midbrain extending to the interpeduncular fossa were operated via the transsylvian approach. Six accesses were achieved via classic pterional for exophytic tumors and four via fronto-orbito-zygomatic, and access to the brainstem was lateral to the third nerve (perioculomotor access). Regarding the central midbrain (59 cases), 53 patients were approached using a supracerebellar infratentorial entry in the sitting position, with 41 cases median and 12 paramedian. In six patients, access was achieved through a combined median supracerebellar infratentorial route with sub-occipital telovelar access through the rhomboid fossa. For the medial supracerebellar infratentorial approaches, the pre-central cerebellar vein was coagulated in all the cases, and no complication ensued. In the paramedian access, coagulation of the pre-central cerebellar vein was not necessary, and the entry point to the brainstem was through the lateral mesencephalic sulcus. Two patients had air embolisms, and aspiration through a central venous catheter was needed to resolve the issue. The air entry point was in the transverse sinus adjacent to the sigmoid sinus, which is the highest and most lateral point of opening in the dura mater. Ten patients had hypertensive pneumoventricles, of which two underwent neuroendoscopy for treatment. Two patients had rubral tremors controlled with clonazepam. Nine patients had tumors in the quadrigeminal lamina, eight of whom were operated via three-quarters prone, and one via a combined infratentorial supracerebellar and sub-occipital telovelar approach. All tumors of the midbrain were low-grade astrocytomas, most of them pilocytic astrocytomas.
Of 168 patients presenting with pontine tumors, 96 were diffuse and not operated upon. Seventy-two tumors in this topography were operated. Four cases had tumors located in the anterior and superior pons, seven in the anterior and inferior pons, 48 in the superior and posterior pons, and thirteen in the inferior and posterior portion
Three tumors located in the anterior and superior pons were operated on using a fronto-orbital-zygomatic route with the brainstem entry point being supratrigeminal, between the third cranial nerve and trigeminal nerve, 4 mm below to the mesencephalon-pontine sulcus. One case was operated on using the pre-sigmoid approach. None of these patients with tumors in the anterior and superior portion of the pons had morbidity. In seven cases, the tumors were situated in the anterior and inferior portion of the pons and were accessed via a presigmoid route. Forty-eight tumors were located in the posterior and superior pons, while thirteen were located in the posterior and inferior pons. All tumors located in the dorsal part of the pons were operated on using a telovelar route through the rhomboid fossa with patients in the prone position. Forty-five tumors in the superior and posterior pons were approached by a suprafacial pathway, and three cases using an interfacial pathway above the facial colliculus. In six patients operated using a suprafacial route, there was injury of the medial longitudinal fasciculus and facial paresis in three cases. In all cases, the symptoms regressed 6 months after surgery. One patient developed acute hydrocephalus and died 3 days later. In the three cases operated on using the interfacial pathway, two developed symptoms of medial longitudinal fasciculus injury that disappeared within 6 months. No facial nerve involvement was observed. Thirteen patients had tumors in the posterior and inferior portion of the pons and were operated on via the infrafacial route. Eight of these patients had facial paralysis, with five cases resulting in permanent paralysis. Twenty-two cases were grade III and grade IV astrocytomas, while 50 cases were low-grade astrocytomas.
Fifty-one patients had medullary tumors, with 11 located in the anterior and 40 at the so-called cervicomedullary junction. Anterior tumors were accessed using a far-lateral approach with an entry point through the olivary medullary route, or where the exophytic tumor resided. Dentate ligament resection was performed in all cases using this route. Cervicomedullary junction tumors were operated on using a 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 patients required permanent tracheostomy due to vocal cord incoordination. Of the medullary tumors, eight were gangliogliomas, three were hemangioblastomas, 29 were astrocytomas, eight were grade III and IV astrocytomas, and 21 were low-grade astrocytomas.
For the entire series of 207 surgically treated tumors of the brainstem, operative mortality seen in the first 2 months after surgery was 1.9 % (four patients) and surgical morbidity occurred in 21.2 % (45 cases). All tumors of the midbrain in our series were low-grade astrocytomas. In the pons, 50 had low-grade astrocytomas, and 22 were high-grade tumors. Of 51 medullary tumors, only eight were high-grade astrocytomas. Thus, of 207 children with tumors of the brainstem, 30 (14.4 %) were high-grade tumors, while 177 were of low grade of malignancy. The follow-up ranged from 3 to 20 years with a mean of 13 years. The disease-free survival (5 years) for benign tumors was 92 %, while median survival for high-grade gliomas was 18 months. Table 1 summarizes the patients and the safe zone entrance used in the 207 patients.
Tumors of the brainstem are more common in children than in adults. Few publications address surgical approaches to brainstem tumors in children. Most of them are related to brainstem approaches for surgical treatment of cavernomas. Surgery for removal of a cavernoma in this location is far different from surgery to remove a brainstem tumor. A peculiar feature of cavernomas is that the cavity produced by widening Virchow-Robin spaces and the consolidation of clots causes a large space after the removal of the clot, facilitating cavernoma resection. Therefore, small incisions at the surface of the brainstem are sufficient to remove bulky cavernomas. In pediatric tumors of the brainstem, the first disadvantage is working on a very small structure compared to the brainstem of an adult, except with rare cystic lesions. On the other hand, many tumors are exophytic, allowing for complete removal without incising the brainstem.
Improvements in diagnosis, with high resolution MRI combined with tractography, are very helpful for surgical decisions as well as for the choice of the safest and more precise surgical approach. Advances of neuroanesthesiology, intraoperative electrophysiological monitoring, and intensive postoperative care, give more security, allowing for more aggressive surgical excisions and preventing damage .
Neurosurgical instruments have also evolved significantly. Today, we have microscopes with high brightness and such definition as to allow improved recognition of where the tumor ends and normal tissue begins. Lighter and more delicate instruments with diamond tip scalpels allow precise incisions of the brainstem. The routine use of ultrasonic surgical aspirators with 1-mm tips allows us to remove large lesions through small openings in the brainstem. Surgical planning of the most appropriate means of access, associated with intrinsic and extrinsic knowledge of brainstem anatomy, is also key to achieving success in surgery.
The brainstem is routinely divided into three parts: midbrain, pons, and medulla . We further divided the brainstem into seven parts: anterior, central, and posterior midbrain; anterior and posterior pons; and anterior and posterior medulla, which helped us to choose the best surgical approaches [11, 12].
Cantore et al.  divided the brain stem into two surgical planes—the anterior and the posterior. Thus, they classify six regions in the brain stem. Our reason for dividing the mesencephalon into three portions is because the quadrigeminal plate tumors characteristics are different from those of the anterior and central midbrain. Most tumors in the quadrigeminal plate are indolent and rarely have to be operated upon, restricting treatment to hydrocephalus control .
Four “safe entry zones” for the midbrain have been described. The most complex and anterior, called the perioculomotor zone, has been described by Bricolo et al.  There is a space between the oculomotor nerve and the pyramidal tract which can be accessed through an incision parallel and lateral to the oculomotor nerve. The presence of a tumor may increase this distance, facilitating surgery. When tumors have an exophytic component, the brainstem can be directly entered through the tumor. Clinically, these patients present preoperatively with third cranial nerve paralysis and contralateral pyramidal involvement (Weber syndrome) that usually disappears quickly after lesion removal. Small tumors only cause diplopia.
In our series, 16 tumors were located in the anterior portion of the mesencephalon. Six were growing towards the III ventricle and were operated on by pure neuroendoscopy, coupled with an ultrasonic aspirator device. We found few literature reports of brainstem tumor resection using purely neuroendoscopic methods. Miki et al. have used the neuroendoscopic trans-third ventricle approach in six cases for lesions of the ventral brainstem surface , but just in one case for brainstem tumor.
In ten patients of our series, tumors grew towards the interpeduncular cistern. Six of these tumors were exophytic, large, and were approached by a classic pterional route with opening of the Sylvian fissure and lesion removal. Wide opening of the Sylvian fissure in young children is sometimes difficult, and simple delicate manipulation can cause vasospasm, thus papaverine is often used. In four patients, the tumors were intrinsic, and the brainstem was approached through the perioculomotor route. In all the cases, a fronto-orbito-zygomatic approach was used. We may also use the temporopolar access described by Sano in 1980 , which provides an anterolateral view of the interpeduncular fossa. These are the access routes we use for the anterior portion of the midbrain, entering through the third ventricle, or through the perioculomotor space. Konovalov and Kadyrov  proposed a transchoroidal temporal access to these anterolateral lesions located in the midbrain, especially on the dominant side and when tumors extend to the ambient cistern. The fact is these lesions are quite rare in this topography. In our series, only 7 % of the tumors considered surgical were located in the anterior portion of the midbrain. Although Albright 1993  reported that only 7 to 8 % of brainstem tumors are located in the midbrain, in Yasargil’s  series of 167 brainstem tumors, 26 (15.5 %) were located in the midbrain, double that reported by Albright . Garzon et al.  found that 33.8 % of brainstem tumors were located in the midbrain. In our series of 207 cases considered surgical, 84 were located in the midbrain (40.5 %), but if we consider all cases of brainstem tumors treated by our service, this rate drops to 27.7 %. We believe this is because we are a neurosurgical center of reference, not being forwarded cases of diffuse pontine tumors.
Of 59 patients with central midbrain tumors operated through an infratentorial supracerebellar routes described by Krause in 1911 , 41 had a median and 12 a paramedian route. When approaching via the paramedian route, we used the same access as the median approach; the only difference being that the brainstem is accessed via the lateral mesencephalic sulcus. Six patients had tumors growing not only towards the third ventricle but also towards the fourth ventricle, and they were operated on, via a combined approach, namely an infratentorial-supracerebellar followed by a suboccipital telovelar approach across the fourth ventricle. All patients were operated on in the sitting position with the head bent. Wide craniotomy of the posterior fossa was performed and the dura opened to avoid the occipital sinus, which is usually patent in young children. The C1 arch was removed in all cases. Yasargil  advocates a different access to this region by not removing the arch of C1 and opening the dura mater 2 cm below and parallel to the transverse sinus, thus preventing further exposure of the cerebellum to avoid possible herniation. In our series, we had no cerebellar herniation. The vermian veins, which are bridging veins between the tentorial face of the cerebellum and the tentorial and transverse sinus, were coagulated without any complication . When necessary, we also coagulated the precentral cerebellar vein without any clinical repercussions. In two cases, the patients had a symptomatic air embolism which was resolved with blood aspiration though the central line and identification of the venous opening in the apex of the dura mater incision close to the transverse sinus.
Nine patients with quadrigeminal plate tumors underwent surgery, eight via the occipital transtentorial route and one through combined infratentorial supracerebellar and suboccipital telovelar routes. In four cases, entries were supracollicular, and five were infracollicular, above the fourth cranial nerve. For tumors of the central or posterior portion of the midbrain growing in the direction to the third ventricle, we used the supracerebellar infratentorial approach. For tumors growing into the fourth ventricle, we use a transtentorial occipital access in the three-quarter position. When the lesions grew into the third and fourth ventricles, we used the combined access route.
Ogata and Yonekawa  proposed a paramedian infratentorial supracerebellar access route for lesions of the superior, intermediate, and lower cerebellar peduncle. They demonstrated that it is possible to open the surface of the intermediate cerebellar peduncle lateral to the cerebellar mesencephalic fissure.
The approaches to the anterior portion of the pons are the most difficult. Bagahai et al.  have described a safe entry zone to the ventrolateral portion of the pons between the output points of the fifth and seventh cranial nerves. This corridor, however, is very narrow and is good only for biopsy or removal of cavernomas in that region. This access can be reached via an occipital paramedian approach or through a petrous access. In other access routes to the anterior pons, the region around the emergence of the fifth cranial nerve is a “safe” area that may be opened 1 cm wide and 1 cm from the midline. However, one should be careful not to go further anterior to avoid the corticospinal tract.
Eleven of our patients had tumors in the anterior pons. Four were anterior and superior, and seven were anterior and inferior. Three anterior and superior tumors were accessed via a fronto-orbito-zygomatic approach, and the point of entry into the lesion was a vertical incision, 4 mm inferior to the mesencephalopontine sulcus in the same direction as the third nerve. In three patients operated using this route, there was no increased morbidity. This approach does not have a similar description in the literature, and we prefer to call it “supratrigeminal access” to differentiate it from peritrigeminal access between the fifth and seventh cranial nerves. In fact, this new entry point is between the third and fifth cranial nerves medial to the pyramidal tract. Other tumors of the ventral pons were approached using a pre-sigmoid route, with ligature of the superior petrosal sinus.
Sixty-one tumors were located in the posterior pons, 48 of them being superior and 13 inferior. The superior tumors were approached either via the suprafacial triangle as proposed by Kyoshima et al. , or, in lateral cases, through the lateral sulcus limitans. In three patients, because of distortion caused by the tumor in the rhomboid fossa, it was extremely difficult to locate an entry point by stimulating the facial nerve. Therefore, the entry point was an interfacial access superior to the facial colliculus, as described by Bricollo and Taruzzi . However, the medial longitudinal fasciculus was injured in two patients. Thirteen patients with inferior pons tumors were operated on through the infrafacial triangle. Eight patients operated by this route developed facial paralysis, which was permanent in five of them. We believe that this route should be reserved only for small exophytic tumors or cavernomas. Access through the rhomboid fossa, below the medullary striae, should also be avoided as this region has a high density of cranial nerve nuclei. All access to the rhomboid fossa was performed using a suboccipital route with the removal of the C1 arch and telovelar approach, sometimes bilaterally, to avoid opening the cerebellar vermis. The patient’s position was ventral decubitus.
Medullary tumors present the same technical difficulty as the tumors of the pons. The anterior ones were approached via suboccipital far lateral craniotomy with removal of the C1 arch and section of the dentate ligamentum which is close to the vertebral artery entry into the skull. That section of the ligament has permitted further mobility of the medulla, facilitating identification of the olivary body and entry into the brain stem through the posterior olivary sulcus (or transolivary entry). Right-sided medullary access usually produced intraoperative hypertension and tachycardia, whereas access from the left side produced bradycardia. These natural alarms must not be suppressed with drugs, such as atropine or hypotensive drugs, because they reveal that we are manipulating the brainstem too aggressively. These are indirect physiological alarm that requires attention. Usually, these vegetative storms occur when the lesion is under traction, which should be avoided. Instead, we should remove the tumor using an ultrasonic aspirator, avoiding traction. These small vegetative storms are not reasons to interrupt procedures, because they cease immediately upon stopping the traction and irrigation with warm saline.
Lesions situated in the posterior portion of the medulla were also operated via occipital telovelar approach, the medulla being reached opening the midline below the obex, through the posterior medial sulcus.
There are eleven previously described “safe” entry zone areas in the brainstem. In this article, we describe another zone, the “supratrigeminal,” for anterior and superior pons lesions. This route was used in three patients and showed no morbidity. It is therefore a reasonable access route. However, a fronto-orbito-zygomatic access is needed for wide visualization of the mesencephalopontine sulcus and the third cranial nerve.
It is up to neurosurgeons to choose correctly pathways for complete lesion resection with a minimum morbidity. However, morbidity is still high (22 % in our series). Hydrocephalus is always a catastrophic complication in the postoperative period of brainstem tumors, and the neurosurgeon should always be aware of this possibility. One of our patients died of hydrocephalus. Thus, whenever possible, we place an external ventricular drain that is removed in the first 48 h postoperatively.
The brainstem does not permit either traction or coagulation; thus, we routinely use ultrasonic aspirators with little aspiration and delicate tips, only performing bipolar coagulation as a last resort with abundant irrigation since the heat may damage the brainstem delicate structures.
The authors wish to thank Mrs Blanche Torres for helping us to write this manuscript and Mr. StharMar de Vasconcelos Silva for the artistics drawings.
Conflict of interest
The authors declare that they have no competing interest.
Financial and material support
- 11.Cavalheiro S, Madeira M, Braga FM (1998) Pediatric brain stem tumors; surgical trial 8th Internationational Symposium on Pediatric Neuro-Oncology Roma, Italia, p 216Google Scholar
- 12.Cavalheiro S, Madeira M, Braga FM (1997) Experiencia cirúrgica em tumores do tronco cerebral na infância. J Brasileiro de Neurocirurgia 8:51–59Google Scholar
- 13.Cavalheiro S, Zymberg S, Coletta DD Jr, Amancio EJ, Ramin SL, Silveira RL, Araujo RJP, Braga FM (1995) Tumores da lamina quadrigemia na infância. Arquivos Brasileiros de Neurocirurgia 14:192–195Google Scholar
- 14.Choux MLG (2000) Brainstem tumors. In: Choux MDRC, Hockley A (eds) Pediatric neurosurgery. Churchill Livingstone, New York, pp 471–491Google Scholar
- 17.Fisher PG, Breiter SN, Carson BS, Wharam MD, Williams JA, Weingart JD, Foer DR, Goldthwaite PT, Tihan T, Burger PC (2000) A clinicopathologic reappraisal of brain stem tumor classification. identification of pilocystic astrocytoma and fibrillary astrocytoma as distinct entities. Cancer 89:1569–1576CrossRefPubMedGoogle Scholar
- 19.Garrett M, Spetzler RF (2009) Surgical treatment of brainstem cavernous malformations. Surgical neurology 72 Suppl 2:S3-9; discussion S9-10Google Scholar
- 33.Klimo P Jr, Pai Panandiker AS, Thompson CJ, Boop FA, Qaddoumi I, Gajjar A, Armstrong GT, Ellison DW, Kun LE, Ogg RJ, Sanford RA (2013) Management and outcome of focal low-grade brainstem tumors in pediatric patients: the St. Jude experience. J Neurosurg Pediatr 11:274–281PubMedCentralCrossRefPubMedGoogle Scholar
- 34.Klinger J (1935) Erleichterung der makroskopischen praeparation des Gehirns durch den Gefrierprozess. Schweiz Arch Neurol Psychiatr 36:247–256Google Scholar
- 35.Konovalov AN, Kadyrov Sh U (2013) [Temporal transchoroidal approach for tumors of the midbrain and thalamus]. Zhurnal voprosy neirokhirurgii imeni N. N Burdenko 77:16–24, discussion 24-15Google Scholar
- 36.Krause F (1911) Die Chirurgie des Ruckenmarks. Chirurgie des Gehirns und Ruckenmarks. vol II. Urban & Schwarzenberg Berlin-Wien, pp 649-820Google Scholar
- 37.Krause F (1926) Operative freilegung der Vierhugel nebst Beobachtungen uber Hirnbrisk and Dekonpression. Zentralb Chirurgie 53:7Google Scholar
- 38.Kulkarni AV, Drake JM, Mallucci CL, Sgouros S, Roth J, Constantini S, Canadian Pediatric Neurosurgery Study G (2009) Endoscopic third ventriculostomy in the treatment of childhood hydrocephalus. J Pediatr 155(254-259):e251Google Scholar
- 40.Lawton MT, Quinones-Hinojosa A, Jun P (2006) The supratonsillar approach to the inferior cerebellar peduncle: anatomy, surgical technique, and clinical application to cavernous malformations. Neurosurgery 59:ONS244-251; discussion ONS251-242Google Scholar
- 41.Ludwig E KJ (1956) The inner structure of the brain demonstrated on the basis of macroscopical preparations. Atlas Cerebri Humani. Brown Boston: LittleGoogle Scholar
- 52.Puget S, Blauwblomme T, Grill J (2012) Is biopsy safe in children with newly diagnosed diffuse intrinsic pontine glioma? American Society of Clinical Oncology educational book / ASCO. American Society of Clinical Oncology. Meeting:629-633Google Scholar
- 62.Taylor KR, Mackay A, Truffaux N, Butterfield YS, Morozova O, Philippe C, Castel D, Grasso CS, Vinci M, Carvalho D, Carcaboso AM, de Torres C, Cruz O, Mora J, Entz-Werle N, Ingram WJ, Monje M, Hargrave D, Bullock AN, Puget S, Yip S, Jones C, Grill J (2014) Recurrent activating ACVR1 mutations in diffuse intrinsic pontine glioma. Nat Genet 46:457–461PubMedCentralCrossRefPubMedGoogle Scholar
- 64.Yasargil M (1996): Midline tumors (corpus callosum, septum pellucidum, basal ganglia, diencephalon, and brainstem. Microneurosurgery vol IV. Thieme New York, pp 291-312Google Scholar
Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.