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Report 2013: Tumors of the pineal region
Tectal plate tumours. Our experience with a paediatric surgical series Tumeurs de la lame tectale. Notre expérience chirurgicale avec une série pédiatrique de 27 patients C. Mottolese a,∗ , A. Szathmari a , P.A. Beuriat a , D. Frappaz b , A. Jouvet c , M. Hermier d a
Pediatric Service of Neurosurgery Service E, “Pierre Wertheimer” Hospital, 59, boulevard Pinel, 69677 Lyon, France Pediatric Neuro-oncological Service, Leon-Berard Hospital, Lyon, France Anatomo-Pathological Service, “P. Wertheimer” Hospital, 59, boulevard Pinel, 69677 Lyon, France d Neuroradiological Service “P. Wertheimer” Hospital, 59, boulevard Pinel, 69677 Lyon, France b c
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Article history: Received 29 March 2013 Received in revised form 23 November 2013 Accepted 23 December 2013 Available online xxx Keywords: Tectal plate Exophytic gliomas Sub-occipital transtentorial approach Brain stem Obstructive hydrocephalus
a b s t r a c t Introduction. – Exophytic tectal plate tumours are a particular kind of brain stem tumour that can be treated with microsurgical resection. This paper reports our surgical experience with a paediatric series stressing and underlines the fact that this surgery can be possible because the rate of surgical mortality is low in experienced hands with acceptable morbidity. Material and methods. – From 1997 to 2010, 27 patients were treated for exophytic tectal plate tumours. The clinical symptomatology was characterized by an intracranial hypertensive syndrome in 77% of cases, visual disorders in 36% of cases and a Parinaud’s syndrome in 12% of cases. All patients were studied using a pre-operative cranio-spinal MRI with and without gadolinium. Hydrocephalus was present in 20 cases treated with a VP shunt in 6 cases and an ETV in the other cases. The surgical removal was total in 60% of cases, partial in 28% of cases and only a large biopsy in 12% of cases. From an histological point of view benign gliomas were diagnosed in 84% of cases and in 16% of cases were classified as WHO grade II and III. Eight patients needed complementary treatment, four with chemotherapy and four with chemotherapy associated to radiotherapy. As a surgical complication two patients had hydrocephalus, one patient had a sub-dural acute haematoma, two patients had an infectious complication requiring surgical treatment and antibiotic therapy, and 5 patients a mechanical shunt dysfunction. No post-surgical mortality was observed. Results. – The most recent results after a median survival of 4.3 years show that 22 patients are still alive while 5 patients died of a progressive disease. Twenty patients in school age continue to follow a normal school programme but 10 patients need assistance. Conclusion. – Exophytic tectal plate tumours can be treated based on a microsurgical approach in paediatric patients. In experienced hands surgery can be performed with an acceptable morbidity and with zero percent mortality. In our experience, the sub-occipital transtentorial approach permits a wide view of the region and safe surgical removal. © 2014 Published by Elsevier Masson SAS.
r é s u m é Mots clés : Tumeur de la lame quadrijumelle Gliome exophytique Abord sous-occipital trans-tentoriel Hydrocéphalie triventriculaire
Introduction. – Les tumeurs exophytiques de la lame quadrijumelle peuvent être traitées chirurgicalement. Nous présentons notre expérience chirurgicale à propos d’une série pédiatrique en soulignant le fait que cette chirurgie peut être réalisée avec une faible morbi-mortalité dans les mains de chirurgiens expérimentés. Patients et méthode. – Sur la période 1997–2000, 27 patients ont été traités pour une tumeur exophytique de la lame quadrijumelle. La symptomatologie clinique a été représentée par un syndrome d’hypertension intracrânienne dans 77 % des cas, des troubles visuels dans 36 % des cas et un syndrome de Parinaud dans 12 % des cas. Tous les patients ont bénéficié d’une IRM cranio-spinale sans et
∗ Corresponding author. E-mail address: [email protected] (C. Mottolese). http://dx.doi.org/10.1016/j.neuchi.2013.12.007 0028-3770/© 2014 Published by Elsevier Masson SAS.
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avec gadolinium. Une hydrocéphalie était présente dans 20 cas, traitée par une dérivation ventriculopéritonéale chez 6 patients et par une ventriculocisternostomie endoscopique dans les autres 14 cas. Du point de vue histologique, 84 % des cas présentaient des gliomes bénins, et dans 16 % des cas des gliomes de grades II–III. Huit patients ont eu un traitement complémentaire : quatre avec chimiothérapie et 4 avec chimiothérapie associée à une radiothérapie. Dans les suites postopératoires, 2 malades ont présenté une hydrocéphalie, un patient a présenté un hématome sous-dural aiguë, deux patients une complication infectieuse traitée par antibiothérapie, cinq patients un dysfonctionnement de la dérivation. Aucune mortalité post-opératoire n’a été observée. Résultats. – Les résultats tardifs après un suivi moyen de 4,3 ans ont montré que vingt-deux patients sont vivants et cinq sont décédés pour une maladie évolutive. Vingt patients sont en âge scolaire, douze sont capable de suivre une scolarité normale et dix une scolarité normale avec un programme adapté. Conclusion. – Les tumeurs exophytiques de la lame quadrijumelle de l’enfant peuvent être traitées chirurgicalement dans des mains expérimentées. Cette chirurgie peut être réalisée avec une morbidité acceptable et une mortalité de 0 %. Dans notre expérience, l’abord sous-occipital trans-tentoriel permet une large vue de la région et une exérèse chirurgicale aisée. © 2014 Publie´ par Elsevier Masson SAS.
1. Introduction Tectal plate tumours are brain stem lesions and their incidence represents 10 to 25% of all paediatric tumours of the CNS. MRI has permitted greater diagnosis but it is difficult, in some cases, to distinguish them from true pineal tumours. MRI has also permitted to show the increasing potential capacity of reaching a surgical decision, in these cases, possible (Figs. 1 and 2). Lapras in 1994 reported his surgical experience with exophytic tectal plate tumours and can be considered one of the pioneers of this surgery [1]. In fact, by removing a pineal region tumour at the end of the surgical procedure he could observe that the pineal gland was in place while the tectal plate was completely removed and the plane of the aqueduct of Sylvius exposed (Figs. 3 and 4). In this way, the route for the surgical removal of exophytic tectal plate tumours was opened and in Lyon, as in other neurosurgical centers, this surgery was performed either in children or in adult patients because these tumours generally have a benign course [2]. Tectal gliomas are generally low-grade astrocytomas and are considered as a benign subgroup of brain stem gliomas. Their treatment is not completely defined but well differentiated gliomas can be cured with only a microsurgical removal [3]. Their incidence is mainly in the third and fourth decades in adult patients while in children the peak of incidence is at ten years [4]. We report our experience with tectal plate tumours that represent nothing else than a glioma of the pineal region and we consider that generally pineal gland gliomas are tectal plate tumours. This experience concerns a retrospective review of exophytic tectal plate gliomas, a special subgroup of brain stem tumours, that differ from other intrinsic gliomas of the tectal plate with an indolent clinically stable nature [5,6]. 2. Clinical material and methods From 1997 to 2010, we treated 27 paediatric age patients for a tectal plate tumour. The age ranged from between two years to 16 years for the oldest patient. The mean age at diagnosis was 7 years and 4 months. We observed two incidence peaks at eight and at eleven years. We did not observe a great difference in gender distribution with 12 boys and 15 girls. From a clinical point of view, 77% of patients presented with clinical signs of intracranial hypertension. In 36% of cases, patients had visual disorders and in 42% of cases a papillary oedema and in 12% of cases Parinaud syndrome.
Figs. 1 and 2. Radiological images of an exophytic tectal plate tumour. Images radiologiques d’une tumeur tectale.
In 11 cases (42%), signs of a cerebellar syndrome were present, an associated hearing loss in 8% of patients and a nystagmus in 19% of cases. Twenty-two patients were studied at the beginning with a CTscan but all had a cerebral MRI associated with a spinal MRI based
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Histological examination showed a pilocytic astrocytoma in 56% of cases, an astrocytoma of WHO grade II in 16% of cases, WHO grade III in 8% of cases, a WHO grades II–III in 8% of cases and gangliogliomas in 12% of cases. Neither glioblastomas nor hamartomas were observed. Different complications were observed: • two patients had an acute hydrocephalus after the direct approach of the tectal plate tumour and were treated with a VP shunt; one patient had an acute sub-dural haematoma; • one case was complicated by an empyema and an abscess in the occipital region that required surgical treatment and antibiotic treatment for three weeks; • five patients had a mechanical dysfunction of the shunt. 3. Results
Figs. 3 and 4. The limits of tectal plate surgery: on the same surgical plane the aqueduct and the third ventricle. Limites de la chirurgie de la lame tectale : dans le même plan, l’aqueduc et le troisième ventricule.
on our protocol for radiological examination in children with a cerebral tumour. In 78% of cases, the MRI showed an enhancement with gadolinium. In one case an arachnoid cyst was associated while in another case a cavernoma was at the origin of an intracerebral haemorrhage. One case was a giant tumour of the tectal plate that was diagnosed at the end of the surgical procedure when the origin of the tectal plate was completely recognized. In two cases, the spinal MRI showed a metastatic location in the dorsal and lumbar region and in only one patient spinal metastasis was associated with a location in the hypothalamic region. In both cases the tectal tumour was a pilocytic astrocytoma. In 20 patients, an active hydrocephalus occurred that was treated with a ventriculo-peritoneal shunt in 6 cases while in three patients a ventriculo-atrial shunt was necessary while in the other 11 patients cases an endoscopic third ventriculostomy was performed. All patients were operated on using a sub-occipital transtentorial approach as well as when there was an extension in the posterior fossa. However, only two cases were operated on through a posterior fossa approach. All surgical removal was evaluated with an MRI carried-out in the first 48 hours post-operatively. All patients were operated in a sitting position except one case that was operated in the prone position. The removal was considered total in 60% of cases (no tumours observed), partial in 28% of cases and in the remaining 12% only a biopsy was possible (Figs. 5–8).
Early post-operative immediate results and most recent results, based on the follow-up and evolution during the time, are reported. Early results refer primarily to the post-operative period and the first six months. In this period, 7 patients were in a comatose state after the surgical procedure in the immediate post-operative period and in a state that was described as the beauty sleeping syndrome and all patients recovered without neuropsychological sequelae. Eleven patients had visual disorders associated with a Parinaud’s syndrome in 5 cases. Five patients complained of hypoacusia after the surgery and one patient had a cerebellar syndrome. One patient had a motor deficit, one patient a seizure, and one a language disorder. Eight patients received complementary treatment with either chemo and radiotherapy or with chemotherapy alone: four patients received chemotherapy associated with radiotherapy and four chemotherapy alone. The follow-up period was between one to 5 years for 11 patients; between 5 and 1 years for 9 patients and beyond 10 years for 5 patients. The median survival was 4.3 years. The latest results have shown that 22 patients are still alive (81%) while 5 patients (19%) died. Nine patients that had Parinaud’s syndrome, observed in the post-operative period, later recovered completely. Six patients had a hearing loss. Twenty-two patients were of school age: 12 were able to attend a normal school but for 10 patients it was a special needs programme was necessary with planning of their study time. 4. Discussion Exophytic brain stem tumours have a growth that extends into the arachnoidal space or the ventricular cavities as reported by Barkovich et al. [7]. Tectal plate tumours represent a particular subgroup of brain stem tumours and when they present an exophytic development they can require surgical treatment as previously reported by Lapras [1]. The incidence of tectal plate tumours until now has been difficult to establish but based on MR imaging and solid squares it varies from 1.3% to 6.5% as reported by Stark [8] while for Oka their incidence is 10% [9]. Jallo reported an incidence of 5% of brainstem tumours in children [10]. As reported in literature the discussion about nosological treatment is still opened to debate and controversial depending on the
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Figs. 5–8. Pre-operative and post-operative images of a tectal plate tumour. Image pré- et postopératoire d’une tumeur de la lame tectale.
surgical experience of the surgeons, symptomatology, the age and their clinical or radiological evolution. Many cases reported in literature with a triventricular obstructive hydrocephalus have shown their potential capacity of growing that have been recorded by a serial MRI with and without a contrast agent. Generally from histological point of view they are benign lesions that have an indolent behaviour, also, if in the follow-up, the evolution and the valuation of radiological pictures help to show their potential growing capacity. For this reason their incidence is very low in very young patients while they are more frequent in older children or young adults [11,12]. We have found a double incidence peak one at eight years and the other at eleven years. Their development in the pineal region may explain why sometimes it can be difficult to distinguish tectal plate tumours from true pineal tumours also for experienced eyes. As previously reported by Bognar in 1994 MRI is now the examination of choice but also has the possibility of using a sequence of diffusion and spectrometry and therefore currently very difficult to obtain a precise diagnosis of their histological type [13].
It is also evident that a limited size and the presence of calcifications can be element of benignity. The use of brainstem auditory evoked potential (BAEPs) monitoring has facilitated surgery in this area permitting, in the operating room, to establish the limits of the removal of lesions according to the alterations of electrical signals and guiding the surgeon in the removal of tumours and the use of this recording becomes a part of daily routine practice for all modern operating rooms (Figs. 9 and 10). According to the experience of Lapras the extension of the surgical removal does not have to pass through the plane of the aqueduct in depth and inferiorly does not touch the plane of the fourth cranial nerve encroachment. Superiorly the removal has to respect the posterior commissure to avoid a definitive Parinaud’s syndrome (Figs. 11 and 12) These resection limits are reserved for an extensive lesion of the tectal plate while for focal lesions it is more useful to remain in the plane that is between the tumour and the non-pathological tissue. The use of the CUSA cavitron with a low aspiration power is very useful when the limits of resection are not very clear.
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Figs. 9 and 10. Per-operative recording of the BEAPs during surgery of tectal plate tumor. Monitoring peropératoire des potentiels évoqués auditifs.
Figs. 11 and 12. Respecting the posterior commissure permits to avoid a Parinaud’s syndrome. Le respect de la commissure postérieure permet d’éviter un syndrome de Parinaud.
Generally the consistency of tectal plate tumours is not very hard. Surgery of the tectal plate tumours has permitted to establish that if a tectal colliculus has to be removed the other has to be
respected and in this way it is possible to avoid severe sequelae for auditory and for conjugate ocular movements. Concerning the surgical approach we prefer the sub-occipital transtentorial approach because it permits a wide exposure of the entire region, with a more comfortable access to the lateral extension in comparison with the infratentorial supracerebellar that can be useful in cases of an extension into the posterior fossa (Figs. 13–16). In our experience, the sitting position is preferable to the ventral position because the gravitational effect coupled with the aspiration of the CSF permits a larger exposure that remains more anatomical and does not oblige the surgeon to constantly move in order to return to the anatomy of the patient in his own mind. In the sitting position, the gravitation permits to operate in a field without blood and in cases of hemorrhage it seems easier to control hemostasis because it is more evident to locate the source of the hemorrhage [21]. To improve clinical results and to diminish the rate of definitive sequelae, care should be used to spare the venous structures and the arterial system to avoid extensive vascular lesions that could compromise surgical results. The clinical results appear to show that surgery for exophytic tectal plate tumours is possible and our experience seems to confirm the experience of Lapras. Lapras showed that the rate of morbidity was 50% and the rate of mortality 10% [1]. Our series shows that the rate of mortality is zero per cent associated an overall morbidity of only 30.3%.
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Figs. 13–16. A giant tectal plate tumour treated by an infratentorial posterior fossa approach. Tumeur géante traitée avec un abord par la fosse cérébrale postérieure.
Based on our experience we observed no correlation between the size of the lesion and the surgical indication, or between the size of the lesion and the rate of post-operative complications as reported by Ternier et al. [3]. In other terms, the surgical indication for exophytic tumours is not only related to the volume of the lesion but it is also important to consider the evolution and the progression of tumour growth as well as the clinical picture with neurological deficits that can translate into an aggressive evolution [22]. We have seen that the lower volume of the tumour considered for the surgical indication and for the direct approach was approximately between 2.5 cm3 and 3 cm3 . Some smaller tumours can become symptomatic because they can be at origin of a hydrocephalus but at the same time may never been operated on. This fact explains why these tumours have been described as “the smallest tumour in the body that can lead to the death of patient” [14].
These are the tumours that have an indolent evolution and a limited growth potential. Therefore, they can only be treated using a conservative programme, including a ventriculostomy (ETV) as well as a radiological follow-up with MRI as reported by Daglioglu et al. [15]. In our experience, a direct surgical approach is justified if the increasing volume of an exophytic lesion becomes symptomatic. The appearance of an increase in contrast enhancement is correlated with a more aggressive biological behavior of the tumours as shown by the incidence of 16% of WHO grades II–III astrocytomas. The incidence of oligodendrogliomas, oligoastrocytomas and ependymomas is less common. We have never found any tectal plate hamartomas, as reported by some authors [3], or any tectal plate glioblastomas as reported by Neto and Stark, and Nemer in young adult patients. Also in a
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paediatric series tectal plate glioblastomas represent quite a rare lesion [8,11,16]. What seems important to mention is that in cases of infiltrative and more aggressive tectal tumours surgery can be more difficult because it is much harder to respect the limits of the resection. We must also stress, as reported by Lapras and Bognar, that the removal of a limited part of the tectal plate, i.e. the inferior or superior colliculi would have no evident clinical consequences [1]. The inferior colliculi is a part of the brain stem with a high number of connections, including the dorsal and ventral cochlear nuclei, the projection for lateral and medial superior olive, and the lateral and dorsal lemniscus. These fibers project into the thalamus and the auditory cortex and each region is connected to the contralateral part as reported by Hacknei [17]. As regards the superior colliculi, Pasik showed that in monkey lesions this did not induce the expected clinical effect. In this case, in a limited lesion of the superior colliculi its function can be assured by the contralateral structure [18]. In cases of hydrocephalus the third ventriculostomy (ETV) permits to avoid shunts. However, we think, as opposed to true pineal tumours, that a biopsy is not indicated because to obtain samples of tumours it is necessary to pass through normal nervous tissue to join the tumour, which presents the risk of increasing post-operative sequelae and the rate of white samples. The importance of BAEPs for surgical removal was previously reported in Lyon by Bognar and Fisher who proposed the monitoring of latencies of Wave I, II, and V as well the I–V conduction time and I–V amplitude ratio for BAEPs and Na and PA latencies. Also Pa–Na amplitude ratio for middle latency auditory evoked potentials (MLAEPs) [13]. Neurophysiologist can alert surgeons as to the modifications of signals to stop surgery, and to wait and change the axis of resection. Bognar and Fisher also reported the first case in the neurosurgical literature where surgery was limited to the inferior colliculi without any hearing loss but with only a limited decrease in the dichotic listening test. This slight dysfunction reordered during the surgical procedure permitted to demonstrate that the afferent input can be send by both cochlear nuclei to both cortices through one functional colliculi rendering evident the role of the extralemniscal auditory pathways [13]. For this reason, the transcollicular approach to the quadrigeminal plate lesion has been proposed and can represent a relatively certain and safe avenue for the removal of limited tectal plate lesions. In cases of partial removal of benign lesions it is sufficient, in our experience, to monitor the patients with a MRI follow-up every six months for two years and after once a year because it sometimes possible to observe the stabilization of the lesion as well as its regression during the follow-up period as we observed in two cases. Pollack recommended a follow-up every six months for a year, after a yearly check-up for four years and after an MRI every two or three years for patients with a stabilized disease [19]. In cases of more aggressive tumours chemotherapy alone or associated with radiotherapy can be useful to control the evolution of the disease. A long term follow-up, in our experience, permits to observe that from a educational point of view 22 of 27 patients were able to follow a school programme with a completely normal programme for 12 patients whereas for 10 patients a normal programme was only possible with an adapted time of study. Concerning the possibility of stereotactic radiosurgery for tectal gliomas as proposed by some authors we think that this is possible but the possibility of radio-induced oedema with severe complications are not rare and therefore we prefer the direct approach.
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The use of gamma knife in focal tectal tumours is still under investigation [20] while in cases of a small increase in dose with stereotactic radiosurgery severe risks have been reported [12]. Our philosophy for exophytic tectal plate tumours is based on the fact that surgical treatment with a low rate of complications can delay chemotherapy and radiotherapy as well as their complications. 5. Conclusion In our experience, surgery of tectal plate tumours in their exophytic form can be possible with a low morbidity and a mortality that over the years has reached zero percent. In experienced hands mortality and morbidity are very low and this fact prompted us to consider surgery for treatment. The absence of hamartomas in our series confirms the potential evolution and growth of tectal plate tumours and consequently their possible surgical removal without the need of complementary treatment in cases of a benign histology. In cases of aggressive lesions, chemotherapy associated with radiotherapy can facilitate a longer survival in patients over three years of age. From a surgical point of view we prefer the suboccipital transtentorial approach performed in the sitting position because of the possibility to effectively control the lateral extension of tumours. The supracerebellar infratentorial approach or a transvermian posterior fossa route can be used only in cases of inferior extension of the tumour inside the fourth ventricle. As regards the paediatric population we stress the importance of staging the disease at beginning because spinal metastasis can be present and consequently complementary treatment, also in cases of pilocytic astrocytoma, is obligatory. Disclosure of interest The authors declare that they have no conflicts of interest concerning this article. References [1] Lapras Cl, Bognar L, Turjman F, Villanyi E, Mottolese C, Fischer C, et al. Tectal plate gliomas. Part I: microsurgery of the tectal plate gliomas. Acta Neurochir (Wien) 1994;126:76–83. [2] Daniel CB, Christos G, Leslie JA, et al. Tectal gliomas: natural history of an indolent lesion in pediatric patients. Pediatr Neurosurg 2000;32:24–9. [3] Ternier J, Wray A, Puget S, Bodaert N, Zerah M, Sainte-Rose C. Tectal lesions in children. J Neurosurg 2006;104:369–76 [6 Suppl. Pediatrics]. [4] Selvapandian S, Rajshekhar V, Chandy MJ. Brain stem glioma: comparative study of clinic-radiological presentation, pathology and outcome in children and adults. Acta Neurochir 1999;141:721–7. [5] Alpers BJ, Watts JW. Mesencephalic gliomas. A clinical and pathological analysis of ten cases. Arch Neurol Psychiatry 1935;34:1250–73. [6] Poussaint TY, Kowal JR, Barnes PD, Zurkowski D, Antony DC, Goumnerova L, et al. Tectal tumors of childhood: clinical and imaging follow-up. AJNR Am J Neuroradiol 1998;19:977–83. [7] Barkovich AJ, Krisher J, Kun LE, Pacer R, Zimmerman RA, Freeman CR, et al. Brain stem gliomas: a classification system based on magnetic resonance imaging. Pediatr Neurosurg 1991;16:73–83. [8] Stark AM, Fritsch MJ, Clavier A, Dorner L, Mehdorn M. Management of tectal glioma in children. Pediatr Neurol 2004;33(1):33–8. [9] Oka K, Kin Y, Go Y, et al. Neuroendoscopic approach to tectal tumors: a consecutive series. J Neurosurg 1999;91:964–70. [10] Jallo GI, Biser-Rohrbaugh A, Freed D. Brainstem gliomas. Child Nerv Syst 2004;20:143–53. [11] Neto FC, Lopes A, Filho MA, Catanoce A, Joaquim AF, de Oliveira E. Tectal Glioblastoma. Arq Neuropsiquiatr 2007;65(4-A):996–9. [12] Lazaro B, Landeiro JA. Tectal plate tumors. Arq Neuropsichiatr 2006;64(2B):432–6. [13] Bognar L, Fischer C, Turjman F, Michel F, Villanyi E, Mottolese C, et al. Tectal plate gliomas part III: apparent lack of consequences of unilateral inferior collicular lesion due to localized glioma surgery. Acta Neurochir (Wien) 1994;127:161–5. [14] Kernhoan WJ. Tumors of the central nervous system. In: Atlas of tumor pathology. Washington, DC: Armed Forces Institute of Pathology; 1952. p. 19–42.
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[19] Pollack IF, Pang D, Albright AL. The long-term outcome in children with lateonset aqueductal stenosis resulting from benign intrinsic tectal tumors. J Neurosurg 1994;80:681–8. [20] Grant GA, Avellino AM, Loeser JD, Ellenboegen RG, Berger MS, Robert TS. Management of intrinsic gliomas of the tectal plate in children. A ten-year review. Pediatr Neurosurg 1999;31:170–6. [21] Bruce JN. Sitting position for removal of pineal region lesions. World Neurosurg 2012;77(5/6):657–8. [22] Heffez DS, Zinreich SI, Long DM. Surgical resection of intrinsic brain stem lesions: an overview. Neurosurgery 1990;27:789–98.
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Report 2013: Tumors of the pineal region
Tectal plate tumours. Our experience with a paediatric surgical series Tumeurs de la lame tectale. Notre expérience chirurgicale avec une série pédiatrique de 27 patients C. Mottolese a,∗ , A. Szathmari a , P.A. Beuriat a , D. Frappaz b , A. Jouvet c , M. Hermier d a
Pediatric Service of Neurosurgery Service E, “Pierre Wertheimer” Hospital, 59, boulevard Pinel, 69677 Lyon, France Pediatric Neuro-oncological Service, Leon-Berard Hospital, Lyon, France Anatomo-Pathological Service, “P. Wertheimer” Hospital, 59, boulevard Pinel, 69677 Lyon, France d Neuroradiological Service “P. Wertheimer” Hospital, 59, boulevard Pinel, 69677 Lyon, France b c
a r t i c l e
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Article history: Received 29 March 2013 Received in revised form 23 November 2013 Accepted 23 December 2013 Available online xxx Keywords: Tectal plate Exophytic gliomas Sub-occipital transtentorial approach Brain stem Obstructive hydrocephalus
a b s t r a c t Introduction. – Exophytic tectal plate tumours are a particular kind of brain stem tumour that can be treated with microsurgical resection. This paper reports our surgical experience with a paediatric series stressing and underlines the fact that this surgery can be possible because the rate of surgical mortality is low in experienced hands with acceptable morbidity. Material and methods. – From 1997 to 2010, 27 patients were treated for exophytic tectal plate tumours. The clinical symptomatology was characterized by an intracranial hypertensive syndrome in 77% of cases, visual disorders in 36% of cases and a Parinaud’s syndrome in 12% of cases. All patients were studied using a pre-operative cranio-spinal MRI with and without gadolinium. Hydrocephalus was present in 20 cases treated with a VP shunt in 6 cases and an ETV in the other cases. The surgical removal was total in 60% of cases, partial in 28% of cases and only a large biopsy in 12% of cases. From an histological point of view benign gliomas were diagnosed in 84% of cases and in 16% of cases were classified as WHO grade II and III. Eight patients needed complementary treatment, four with chemotherapy and four with chemotherapy associated to radiotherapy. As a surgical complication two patients had hydrocephalus, one patient had a sub-dural acute haematoma, two patients had an infectious complication requiring surgical treatment and antibiotic therapy, and 5 patients a mechanical shunt dysfunction. No post-surgical mortality was observed. Results. – The most recent results after a median survival of 4.3 years show that 22 patients are still alive while 5 patients died of a progressive disease. Twenty patients in school age continue to follow a normal school programme but 10 patients need assistance. Conclusion. – Exophytic tectal plate tumours can be treated based on a microsurgical approach in paediatric patients. In experienced hands surgery can be performed with an acceptable morbidity and with zero percent mortality. In our experience, the sub-occipital transtentorial approach permits a wide view of the region and safe surgical removal. © 2014 Published by Elsevier Masson SAS.
r é s u m é Mots clés : Tumeur de la lame quadrijumelle Gliome exophytique Abord sous-occipital trans-tentoriel Hydrocéphalie triventriculaire
Introduction. – Les tumeurs exophytiques de la lame quadrijumelle peuvent être traitées chirurgicalement. Nous présentons notre expérience chirurgicale à propos d’une série pédiatrique en soulignant le fait que cette chirurgie peut être réalisée avec une faible morbi-mortalité dans les mains de chirurgiens expérimentés. Patients et méthode. – Sur la période 1997–2000, 27 patients ont été traités pour une tumeur exophytique de la lame quadrijumelle. La symptomatologie clinique a été représentée par un syndrome d’hypertension intracrânienne dans 77 % des cas, des troubles visuels dans 36 % des cas et un syndrome de Parinaud dans 12 % des cas. Tous les patients ont bénéficié d’une IRM cranio-spinale sans et
∗ Corresponding author. E-mail address: [email protected] (C. Mottolese). http://dx.doi.org/10.1016/j.neuchi.2013.12.007 0028-3770/© 2014 Published by Elsevier Masson SAS.
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avec gadolinium. Une hydrocéphalie était présente dans 20 cas, traitée par une dérivation ventriculopéritonéale chez 6 patients et par une ventriculocisternostomie endoscopique dans les autres 14 cas. Du point de vue histologique, 84 % des cas présentaient des gliomes bénins, et dans 16 % des cas des gliomes de grades II–III. Huit patients ont eu un traitement complémentaire : quatre avec chimiothérapie et 4 avec chimiothérapie associée à une radiothérapie. Dans les suites postopératoires, 2 malades ont présenté une hydrocéphalie, un patient a présenté un hématome sous-dural aiguë, deux patients une complication infectieuse traitée par antibiothérapie, cinq patients un dysfonctionnement de la dérivation. Aucune mortalité post-opératoire n’a été observée. Résultats. – Les résultats tardifs après un suivi moyen de 4,3 ans ont montré que vingt-deux patients sont vivants et cinq sont décédés pour une maladie évolutive. Vingt patients sont en âge scolaire, douze sont capable de suivre une scolarité normale et dix une scolarité normale avec un programme adapté. Conclusion. – Les tumeurs exophytiques de la lame quadrijumelle de l’enfant peuvent être traitées chirurgicalement dans des mains expérimentées. Cette chirurgie peut être réalisée avec une morbidité acceptable et une mortalité de 0 %. Dans notre expérience, l’abord sous-occipital trans-tentoriel permet une large vue de la région et une exérèse chirurgicale aisée. © 2014 Publie´ par Elsevier Masson SAS.
1. Introduction Tectal plate tumours are brain stem lesions and their incidence represents 10 to 25% of all paediatric tumours of the CNS. MRI has permitted greater diagnosis but it is difficult, in some cases, to distinguish them from true pineal tumours. MRI has also permitted to show the increasing potential capacity of reaching a surgical decision, in these cases, possible (Figs. 1 and 2). Lapras in 1994 reported his surgical experience with exophytic tectal plate tumours and can be considered one of the pioneers of this surgery [1]. In fact, by removing a pineal region tumour at the end of the surgical procedure he could observe that the pineal gland was in place while the tectal plate was completely removed and the plane of the aqueduct of Sylvius exposed (Figs. 3 and 4). In this way, the route for the surgical removal of exophytic tectal plate tumours was opened and in Lyon, as in other neurosurgical centers, this surgery was performed either in children or in adult patients because these tumours generally have a benign course [2]. Tectal gliomas are generally low-grade astrocytomas and are considered as a benign subgroup of brain stem gliomas. Their treatment is not completely defined but well differentiated gliomas can be cured with only a microsurgical removal [3]. Their incidence is mainly in the third and fourth decades in adult patients while in children the peak of incidence is at ten years [4]. We report our experience with tectal plate tumours that represent nothing else than a glioma of the pineal region and we consider that generally pineal gland gliomas are tectal plate tumours. This experience concerns a retrospective review of exophytic tectal plate gliomas, a special subgroup of brain stem tumours, that differ from other intrinsic gliomas of the tectal plate with an indolent clinically stable nature [5,6]. 2. Clinical material and methods From 1997 to 2010, we treated 27 paediatric age patients for a tectal plate tumour. The age ranged from between two years to 16 years for the oldest patient. The mean age at diagnosis was 7 years and 4 months. We observed two incidence peaks at eight and at eleven years. We did not observe a great difference in gender distribution with 12 boys and 15 girls. From a clinical point of view, 77% of patients presented with clinical signs of intracranial hypertension. In 36% of cases, patients had visual disorders and in 42% of cases a papillary oedema and in 12% of cases Parinaud syndrome.
Figs. 1 and 2. Radiological images of an exophytic tectal plate tumour. Images radiologiques d’une tumeur tectale.
In 11 cases (42%), signs of a cerebellar syndrome were present, an associated hearing loss in 8% of patients and a nystagmus in 19% of cases. Twenty-two patients were studied at the beginning with a CTscan but all had a cerebral MRI associated with a spinal MRI based
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Histological examination showed a pilocytic astrocytoma in 56% of cases, an astrocytoma of WHO grade II in 16% of cases, WHO grade III in 8% of cases, a WHO grades II–III in 8% of cases and gangliogliomas in 12% of cases. Neither glioblastomas nor hamartomas were observed. Different complications were observed: • two patients had an acute hydrocephalus after the direct approach of the tectal plate tumour and were treated with a VP shunt; one patient had an acute sub-dural haematoma; • one case was complicated by an empyema and an abscess in the occipital region that required surgical treatment and antibiotic treatment for three weeks; • five patients had a mechanical dysfunction of the shunt. 3. Results
Figs. 3 and 4. The limits of tectal plate surgery: on the same surgical plane the aqueduct and the third ventricle. Limites de la chirurgie de la lame tectale : dans le même plan, l’aqueduc et le troisième ventricule.
on our protocol for radiological examination in children with a cerebral tumour. In 78% of cases, the MRI showed an enhancement with gadolinium. In one case an arachnoid cyst was associated while in another case a cavernoma was at the origin of an intracerebral haemorrhage. One case was a giant tumour of the tectal plate that was diagnosed at the end of the surgical procedure when the origin of the tectal plate was completely recognized. In two cases, the spinal MRI showed a metastatic location in the dorsal and lumbar region and in only one patient spinal metastasis was associated with a location in the hypothalamic region. In both cases the tectal tumour was a pilocytic astrocytoma. In 20 patients, an active hydrocephalus occurred that was treated with a ventriculo-peritoneal shunt in 6 cases while in three patients a ventriculo-atrial shunt was necessary while in the other 11 patients cases an endoscopic third ventriculostomy was performed. All patients were operated on using a sub-occipital transtentorial approach as well as when there was an extension in the posterior fossa. However, only two cases were operated on through a posterior fossa approach. All surgical removal was evaluated with an MRI carried-out in the first 48 hours post-operatively. All patients were operated in a sitting position except one case that was operated in the prone position. The removal was considered total in 60% of cases (no tumours observed), partial in 28% of cases and in the remaining 12% only a biopsy was possible (Figs. 5–8).
Early post-operative immediate results and most recent results, based on the follow-up and evolution during the time, are reported. Early results refer primarily to the post-operative period and the first six months. In this period, 7 patients were in a comatose state after the surgical procedure in the immediate post-operative period and in a state that was described as the beauty sleeping syndrome and all patients recovered without neuropsychological sequelae. Eleven patients had visual disorders associated with a Parinaud’s syndrome in 5 cases. Five patients complained of hypoacusia after the surgery and one patient had a cerebellar syndrome. One patient had a motor deficit, one patient a seizure, and one a language disorder. Eight patients received complementary treatment with either chemo and radiotherapy or with chemotherapy alone: four patients received chemotherapy associated with radiotherapy and four chemotherapy alone. The follow-up period was between one to 5 years for 11 patients; between 5 and 1 years for 9 patients and beyond 10 years for 5 patients. The median survival was 4.3 years. The latest results have shown that 22 patients are still alive (81%) while 5 patients (19%) died. Nine patients that had Parinaud’s syndrome, observed in the post-operative period, later recovered completely. Six patients had a hearing loss. Twenty-two patients were of school age: 12 were able to attend a normal school but for 10 patients it was a special needs programme was necessary with planning of their study time. 4. Discussion Exophytic brain stem tumours have a growth that extends into the arachnoidal space or the ventricular cavities as reported by Barkovich et al. [7]. Tectal plate tumours represent a particular subgroup of brain stem tumours and when they present an exophytic development they can require surgical treatment as previously reported by Lapras [1]. The incidence of tectal plate tumours until now has been difficult to establish but based on MR imaging and solid squares it varies from 1.3% to 6.5% as reported by Stark [8] while for Oka their incidence is 10% [9]. Jallo reported an incidence of 5% of brainstem tumours in children [10]. As reported in literature the discussion about nosological treatment is still opened to debate and controversial depending on the
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Figs. 5–8. Pre-operative and post-operative images of a tectal plate tumour. Image pré- et postopératoire d’une tumeur de la lame tectale.
surgical experience of the surgeons, symptomatology, the age and their clinical or radiological evolution. Many cases reported in literature with a triventricular obstructive hydrocephalus have shown their potential capacity of growing that have been recorded by a serial MRI with and without a contrast agent. Generally from histological point of view they are benign lesions that have an indolent behaviour, also, if in the follow-up, the evolution and the valuation of radiological pictures help to show their potential growing capacity. For this reason their incidence is very low in very young patients while they are more frequent in older children or young adults [11,12]. We have found a double incidence peak one at eight years and the other at eleven years. Their development in the pineal region may explain why sometimes it can be difficult to distinguish tectal plate tumours from true pineal tumours also for experienced eyes. As previously reported by Bognar in 1994 MRI is now the examination of choice but also has the possibility of using a sequence of diffusion and spectrometry and therefore currently very difficult to obtain a precise diagnosis of their histological type [13].
It is also evident that a limited size and the presence of calcifications can be element of benignity. The use of brainstem auditory evoked potential (BAEPs) monitoring has facilitated surgery in this area permitting, in the operating room, to establish the limits of the removal of lesions according to the alterations of electrical signals and guiding the surgeon in the removal of tumours and the use of this recording becomes a part of daily routine practice for all modern operating rooms (Figs. 9 and 10). According to the experience of Lapras the extension of the surgical removal does not have to pass through the plane of the aqueduct in depth and inferiorly does not touch the plane of the fourth cranial nerve encroachment. Superiorly the removal has to respect the posterior commissure to avoid a definitive Parinaud’s syndrome (Figs. 11 and 12) These resection limits are reserved for an extensive lesion of the tectal plate while for focal lesions it is more useful to remain in the plane that is between the tumour and the non-pathological tissue. The use of the CUSA cavitron with a low aspiration power is very useful when the limits of resection are not very clear.
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Figs. 9 and 10. Per-operative recording of the BEAPs during surgery of tectal plate tumor. Monitoring peropératoire des potentiels évoqués auditifs.
Figs. 11 and 12. Respecting the posterior commissure permits to avoid a Parinaud’s syndrome. Le respect de la commissure postérieure permet d’éviter un syndrome de Parinaud.
Generally the consistency of tectal plate tumours is not very hard. Surgery of the tectal plate tumours has permitted to establish that if a tectal colliculus has to be removed the other has to be
respected and in this way it is possible to avoid severe sequelae for auditory and for conjugate ocular movements. Concerning the surgical approach we prefer the sub-occipital transtentorial approach because it permits a wide exposure of the entire region, with a more comfortable access to the lateral extension in comparison with the infratentorial supracerebellar that can be useful in cases of an extension into the posterior fossa (Figs. 13–16). In our experience, the sitting position is preferable to the ventral position because the gravitational effect coupled with the aspiration of the CSF permits a larger exposure that remains more anatomical and does not oblige the surgeon to constantly move in order to return to the anatomy of the patient in his own mind. In the sitting position, the gravitation permits to operate in a field without blood and in cases of hemorrhage it seems easier to control hemostasis because it is more evident to locate the source of the hemorrhage [21]. To improve clinical results and to diminish the rate of definitive sequelae, care should be used to spare the venous structures and the arterial system to avoid extensive vascular lesions that could compromise surgical results. The clinical results appear to show that surgery for exophytic tectal plate tumours is possible and our experience seems to confirm the experience of Lapras. Lapras showed that the rate of morbidity was 50% and the rate of mortality 10% [1]. Our series shows that the rate of mortality is zero per cent associated an overall morbidity of only 30.3%.
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Figs. 13–16. A giant tectal plate tumour treated by an infratentorial posterior fossa approach. Tumeur géante traitée avec un abord par la fosse cérébrale postérieure.
Based on our experience we observed no correlation between the size of the lesion and the surgical indication, or between the size of the lesion and the rate of post-operative complications as reported by Ternier et al. [3]. In other terms, the surgical indication for exophytic tumours is not only related to the volume of the lesion but it is also important to consider the evolution and the progression of tumour growth as well as the clinical picture with neurological deficits that can translate into an aggressive evolution [22]. We have seen that the lower volume of the tumour considered for the surgical indication and for the direct approach was approximately between 2.5 cm3 and 3 cm3 . Some smaller tumours can become symptomatic because they can be at origin of a hydrocephalus but at the same time may never been operated on. This fact explains why these tumours have been described as “the smallest tumour in the body that can lead to the death of patient” [14].
These are the tumours that have an indolent evolution and a limited growth potential. Therefore, they can only be treated using a conservative programme, including a ventriculostomy (ETV) as well as a radiological follow-up with MRI as reported by Daglioglu et al. [15]. In our experience, a direct surgical approach is justified if the increasing volume of an exophytic lesion becomes symptomatic. The appearance of an increase in contrast enhancement is correlated with a more aggressive biological behavior of the tumours as shown by the incidence of 16% of WHO grades II–III astrocytomas. The incidence of oligodendrogliomas, oligoastrocytomas and ependymomas is less common. We have never found any tectal plate hamartomas, as reported by some authors [3], or any tectal plate glioblastomas as reported by Neto and Stark, and Nemer in young adult patients. Also in a
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paediatric series tectal plate glioblastomas represent quite a rare lesion [8,11,16]. What seems important to mention is that in cases of infiltrative and more aggressive tectal tumours surgery can be more difficult because it is much harder to respect the limits of the resection. We must also stress, as reported by Lapras and Bognar, that the removal of a limited part of the tectal plate, i.e. the inferior or superior colliculi would have no evident clinical consequences [1]. The inferior colliculi is a part of the brain stem with a high number of connections, including the dorsal and ventral cochlear nuclei, the projection for lateral and medial superior olive, and the lateral and dorsal lemniscus. These fibers project into the thalamus and the auditory cortex and each region is connected to the contralateral part as reported by Hacknei [17]. As regards the superior colliculi, Pasik showed that in monkey lesions this did not induce the expected clinical effect. In this case, in a limited lesion of the superior colliculi its function can be assured by the contralateral structure [18]. In cases of hydrocephalus the third ventriculostomy (ETV) permits to avoid shunts. However, we think, as opposed to true pineal tumours, that a biopsy is not indicated because to obtain samples of tumours it is necessary to pass through normal nervous tissue to join the tumour, which presents the risk of increasing post-operative sequelae and the rate of white samples. The importance of BAEPs for surgical removal was previously reported in Lyon by Bognar and Fisher who proposed the monitoring of latencies of Wave I, II, and V as well the I–V conduction time and I–V amplitude ratio for BAEPs and Na and PA latencies. Also Pa–Na amplitude ratio for middle latency auditory evoked potentials (MLAEPs) [13]. Neurophysiologist can alert surgeons as to the modifications of signals to stop surgery, and to wait and change the axis of resection. Bognar and Fisher also reported the first case in the neurosurgical literature where surgery was limited to the inferior colliculi without any hearing loss but with only a limited decrease in the dichotic listening test. This slight dysfunction reordered during the surgical procedure permitted to demonstrate that the afferent input can be send by both cochlear nuclei to both cortices through one functional colliculi rendering evident the role of the extralemniscal auditory pathways [13]. For this reason, the transcollicular approach to the quadrigeminal plate lesion has been proposed and can represent a relatively certain and safe avenue for the removal of limited tectal plate lesions. In cases of partial removal of benign lesions it is sufficient, in our experience, to monitor the patients with a MRI follow-up every six months for two years and after once a year because it sometimes possible to observe the stabilization of the lesion as well as its regression during the follow-up period as we observed in two cases. Pollack recommended a follow-up every six months for a year, after a yearly check-up for four years and after an MRI every two or three years for patients with a stabilized disease [19]. In cases of more aggressive tumours chemotherapy alone or associated with radiotherapy can be useful to control the evolution of the disease. A long term follow-up, in our experience, permits to observe that from a educational point of view 22 of 27 patients were able to follow a school programme with a completely normal programme for 12 patients whereas for 10 patients a normal programme was only possible with an adapted time of study. Concerning the possibility of stereotactic radiosurgery for tectal gliomas as proposed by some authors we think that this is possible but the possibility of radio-induced oedema with severe complications are not rare and therefore we prefer the direct approach.
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The use of gamma knife in focal tectal tumours is still under investigation [20] while in cases of a small increase in dose with stereotactic radiosurgery severe risks have been reported [12]. Our philosophy for exophytic tectal plate tumours is based on the fact that surgical treatment with a low rate of complications can delay chemotherapy and radiotherapy as well as their complications. 5. Conclusion In our experience, surgery of tectal plate tumours in their exophytic form can be possible with a low morbidity and a mortality that over the years has reached zero percent. In experienced hands mortality and morbidity are very low and this fact prompted us to consider surgery for treatment. The absence of hamartomas in our series confirms the potential evolution and growth of tectal plate tumours and consequently their possible surgical removal without the need of complementary treatment in cases of a benign histology. In cases of aggressive lesions, chemotherapy associated with radiotherapy can facilitate a longer survival in patients over three years of age. From a surgical point of view we prefer the suboccipital transtentorial approach performed in the sitting position because of the possibility to effectively control the lateral extension of tumours. The supracerebellar infratentorial approach or a transvermian posterior fossa route can be used only in cases of inferior extension of the tumour inside the fourth ventricle. As regards the paediatric population we stress the importance of staging the disease at beginning because spinal metastasis can be present and consequently complementary treatment, also in cases of pilocytic astrocytoma, is obligatory. Disclosure of interest The authors declare that they have no conflicts of interest concerning this article. References [1] Lapras Cl, Bognar L, Turjman F, Villanyi E, Mottolese C, Fischer C, et al. Tectal plate gliomas. Part I: microsurgery of the tectal plate gliomas. Acta Neurochir (Wien) 1994;126:76–83. [2] Daniel CB, Christos G, Leslie JA, et al. Tectal gliomas: natural history of an indolent lesion in pediatric patients. Pediatr Neurosurg 2000;32:24–9. [3] Ternier J, Wray A, Puget S, Bodaert N, Zerah M, Sainte-Rose C. Tectal lesions in children. J Neurosurg 2006;104:369–76 [6 Suppl. Pediatrics]. [4] Selvapandian S, Rajshekhar V, Chandy MJ. Brain stem glioma: comparative study of clinic-radiological presentation, pathology and outcome in children and adults. Acta Neurochir 1999;141:721–7. [5] Alpers BJ, Watts JW. Mesencephalic gliomas. A clinical and pathological analysis of ten cases. Arch Neurol Psychiatry 1935;34:1250–73. [6] Poussaint TY, Kowal JR, Barnes PD, Zurkowski D, Antony DC, Goumnerova L, et al. Tectal tumors of childhood: clinical and imaging follow-up. AJNR Am J Neuroradiol 1998;19:977–83. [7] Barkovich AJ, Krisher J, Kun LE, Pacer R, Zimmerman RA, Freeman CR, et al. Brain stem gliomas: a classification system based on magnetic resonance imaging. Pediatr Neurosurg 1991;16:73–83. [8] Stark AM, Fritsch MJ, Clavier A, Dorner L, Mehdorn M. Management of tectal glioma in children. Pediatr Neurol 2004;33(1):33–8. [9] Oka K, Kin Y, Go Y, et al. Neuroendoscopic approach to tectal tumors: a consecutive series. J Neurosurg 1999;91:964–70. [10] Jallo GI, Biser-Rohrbaugh A, Freed D. Brainstem gliomas. Child Nerv Syst 2004;20:143–53. [11] Neto FC, Lopes A, Filho MA, Catanoce A, Joaquim AF, de Oliveira E. Tectal Glioblastoma. Arq Neuropsiquiatr 2007;65(4-A):996–9. [12] Lazaro B, Landeiro JA. Tectal plate tumors. Arq Neuropsichiatr 2006;64(2B):432–6. [13] Bognar L, Fischer C, Turjman F, Michel F, Villanyi E, Mottolese C, et al. Tectal plate gliomas part III: apparent lack of consequences of unilateral inferior collicular lesion due to localized glioma surgery. Acta Neurochir (Wien) 1994;127:161–5. [14] Kernhoan WJ. Tumors of the central nervous system. In: Atlas of tumor pathology. Washington, DC: Armed Forces Institute of Pathology; 1952. p. 19–42.
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