Clinical Neurology and Neurosurgery 115 (2013) 1745–1752
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Trans-lamina terminalis approach for third ventricle and suprasellar tumours Pedro Santos Silva ∗ , António Cerejo, Patrícia Polónia, Josué Pereira, Rui Vaz Neurosurgery Department, Hospital de São João, Porto, Portugal
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Article history: Received 27 November 2012 Received in revised form 4 April 2013 Accepted 7 April 2013 Available online 7 May 2013 Keywords: Lamina terminalis Third ventricle tumour Suprasellar tumour Trans-lamina terminalis
a b s t r a c t Background: The trans-lamina terminalis (TLT) approach to the suprasellar region and third ventricle is complex, with risks of visual and hormonal deficits. However, the postoperative deficits might not be directly related to opening of the lamina terminalis but to the close relationship of tumours with vital neural and vascular structures. The analysis of results using this approach was the objective of this study. Material and methods: The TLT approach was used in 29 patients (18 craniopharyngiomas, 5 astrocytomas, 5 germinomas and 1 ganglioglioma). The extent of tumour removal, mortality and morbidity (especially visual or hormonal deficits) were studied. Results: Complete tumour removal was achieved in 15 patients, subtotal extensive removal (more than 90%) in 9 cases and partial removal in 5 cases. Panhypopituitarism developed in 22 patients. Total tumour removal was associated with the development of endocrinological disturbances. There was worsening or the onset of new visual field defects in 4 cases. Postoperative endocrine and visual deficits were in the range generally described regarding surgery for tumours in this region. Conclusion: The TLT approach allows for extensive removal of third ventricle and suprasellar tumours, without increased risks of visual and hormonal deficits, compared to those described regarding surgery for lesions in this region. © 2013 Elsevier B.V. All rights reserved.
1. Introduction The trans-lamina terminalis approach to tumours located in the suprasellar region and involving the third ventricle has been described in several publications, most of them devoted to specific pathologies [1–8], and this approach is considered to be complex, with the risk of producing visual and hormonal deficits due to damage to the optic pathways and the hypothalamus. Moreover, dissection and removal of lesions inside the third ventricle run the potential risk of injury to vascular and neuronal structures in the ventricular walls [1–4,6,8–11]. Lesions involving the third ventricle have been operated on by a subfrontal, combined with trans-lamina terminalis approach. Although other options have been considered [1,3,6,8,9,11], this approach has proved to be safe in terms of frontal lobe lesions, thus indicating that with appropriate care, brain retraction can be reduced to minimum levels. Importantly, the need for opening of the lamina terminalis might be not predictable in many cases (Fig. 1). Thus, surgeons operating on lesions in this region must be prepared to proceed with opening of the lamina terminalis if their
∗ Corresponding author at: Hospital São João, Neurosurgery Department, Alameda Prof. Hernâni Monteiro, 4200 319, Porto, Portugal. Tel.: +351 925878701. E-mail address:
[email protected] (P.S. Silva). 0303-8467/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.clineuro.2013.04.010
goal is total (or subtotal but extensive) removal of the tumour and to address the problems of this approach. In this work, a series of patients submitted to surgery with the use of the trans-lamina terminalis approach was studied, with several different pathologies. The extent of tumour removal and the results concerning postoperative visual and hormonal deficits are presented. 2. Material and methods 2.1. Cases included The trans-lamina terminalis approach was applied by the same team in 29 cases of suprasellar/third ventricle tumours, from 2000 to 2011. 2.2. Surgical procedure A bifrontal craniotomy was performed in all cases, with bilateral opening of the dura mater. The superior sagittal sinus was ligated, and the falx cerebri was cut in its frontal section. Surgery proceeded with very slow dissection under the right frontal lobe, allowing for the exit of cerebrospinal fluid. Both olfactory nerves were identified and dissected from the right side. The importance
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Fig. 1. Female, 57 years old, pre- (a) and postoperative (b) MRIs of craniopharyngioma. Although the lesion was not intraventricular, opening of the lamina terminalis was necessary for complete removal.
of keeping the olfactory nerves intact should be emphasised; in addition to the loss of olfactory function, avulsion of the olfactory nerves should be regarded as a sign of overpressure in the frontal lobe. The brain becomes progressively more relaxed due to the exit of cerebrospinal fluid, and the optic nerves come into view. Once the optic nerves were reached, adhesions and bridging veins from the left frontal pole were interrupted, thus liberating the frontal lobe without any retraction. Brain retractors were avoided until the optic nerves and the optic chiasm were reached, and then the retractors were placed in the midline, between the olfactory nerves. Surgery proceeded in the prechiasmatic space with identification of the tumour, followed by debulking as extensively as possible and bilateral dissection of the lesion from the optic nerves, carotid arteries and posterior communicating arteries. When the tumour was primarily situated in the retrochiasmatic region or into the third ventricle, opening of the lamina terminalis was planned preoperatively; however, in some cases, if the dissection from the prechiasmatic space to the hypothalamus was remarkably difficult, opening of the lamina terminalis was decided on intraoperatively (Fig. 2). With gentle replacement of the retractor, the chiasm and the lamina terminalis were exposed, with visualisation of anterior communicating artery. With dissectors, the lamina terminalis was opened proximal to anterior communicating artery, strictly in the midline. Extensive debulking of the tumour was then performed, followed by careful dissection of the lesion from the ventricular walls. With tumour manipulation, the opening in the lamina terminalis gradually enlarged, providing enough space for tumour debulking and dissection (Fig. 3). After debulking, the tumour capsule was dissected from the ventricular wall, keeping the capsule intact (special care is needed in the superior portion of the tumour,
Fig. 2. Opening of lamina terminalis. 1 - right optic nerve; 2 - left optic nerve; 3 - prefixed optic chiasm; 4 - olfactory nerves; 5 - opening in lamina terminalis; 6 tuberculum sellae.
Fig. 3. Tumour debulking through the lamina terminalis. 1 - tumour into view through enlarged lamina terminalis opening; 2 - left optic tract; 3 - optic chiasm.
in the vicinity of the Monro foramina (Fig. 4), which is a “blind zone” for the surgeon using this approach). If the capsule is not intact, remnants will retract superiorly and will be not visible through the lamina terminalis). Although the floor of the third ventricle was disrupted by the tumour in many cases, it was sometimes possible to preserve, at least partially, the pituitary stalk. In most cases, the tumour was very adherent to the optic chiasm, and very careful dissection was necessary. In some cases, the tumour could be removed either from the lamina terminalis or from the prechiasmatic space. As the tumour was gradually removed, the prepontine cistern was reached. The basilar artery apex complex was identified and separated from the lesion (Fig. 5), constituting the final step of tumour removal (Fig. 6). 2.3. Postoperative evaluation The patients were transferred anaesthetised to the Neurocritical Care Unit (NCU), with slow removal of drugs over the subsequent 6–12 h A CT scan was performed in all cases, 6–8 h after surgery, for the detection of complications, such as postoperative haematomas or hydrocephalus. The patients were kept in the NCU until they were fully awake with balanced diuresis and electrolytes, with or without
Fig. 4. Tumour dissection from the ventricular wall. 1 - tumour gently pulled from the “blind zone” (roof of the third ventricle and vicinity of the Monro foramina); 2 - olfactory nerves; 3 - right optic tract; 4 - optic chiasm.
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Table 1 Clinical presentation (number of patients). Signs of increased ICP Hydrocephalus Visual field defects Visual acuity loss Psychiatric symptoms Intraventricular haemorrhage
14 6 8 8 3 1
3.1. Clinical presentation (Table 1) Signs of increased ICP were frequent in this group of patients (14 cases), with hydrocephalus in 6 cases. Visual field defects or visual acuity loss was present in 16 patients. One case of germinoma presented with sudden onset of intraventricular haemorrhage, and 3 patients showed psychiatric symptoms at admission. Fig. 5. Removal of tumour from the basilar apex. 1 - last portion of tumour; 2 basilar artery; 3 - left superior cerebellar artery; 4 - right superior cerebellar artery; 5 - right posterior cerebral artery; 6 - right optic tract.
3.2. Extent of removal (Table 2) antidiuretic hormone therapy. After hospital discharge, the patients were evaluated after 1 week, at 1 month and then every 6 months. After the operations, the studied parameters were surgical complications, the extent of removal, and the visual and hormonal deficits. The extent of removal was evaluated with postoperative MRI. The results were classified into one of 3 groups: complete removal (no tumour visible on postoperative MRI); subtotal extensive removal (removal of 90% or more of the tumour mass); and partial removal (extent of removal of 50–90% of the tumour mass). The presence of endocrine deficits and the need for hormonal substitution therapy were examined in all cases. Postoperative visual deficits were also studied in all cases, to investigate the presence of visual field defects and the evolution, after surgery, of preoperative deficits. 3. Results In the 29 patients in the study, there were 18 male patients and 11 female patients (ratio 1.6:1). The age of the patients was between 4 and 71 years old, with the mean age of 29 years. The pathology of the included cases, with specimens obtained by surgical removal, showed 18 craniopharyngiomas, 5 astrocytomas, 5 germinomas and 1 ganglioglioma. The median follow-up time was 65 months (from 6 to 148 months).
Total removal was possible in 15 patients (14 craniopharyngiomas and 1 germinoma) (Figs. 7 and 8). Subtotal extensive removal was achieved in 9 cases (4 craniopharyngiomas, 2 astrocytomas, 2 germinomas and 1 ganglioglioma) (Fig. 9). Partial removal was accomplished in 5 cases: 3 astrocytomas and 2 germinomas (Fig. 10). In craniopharyngiomas, complete removal was not possible due to extension into the cavernous sinus (1 case) and the lateral ventricle (1 case), adhesion to the optic chiasm/optic tract (1 case), and strong adhesion to the basilar apex (1 case). In other pathologies, total removal was not achieved due to difficult dissection of the tumour from the involved neural structures; total removal was not the objective of surgery in cases of astrocytoma. Preservation of the pituitary stalk was possible in 8 cases, all of them (except for one case of craniopharyngioma) with incomplete tumour removal (2 craniopharyngiomas, 4 astrocytomas, 1 ganglioglioma)
3.3. Surgical complications (Table 3) One patient died in the fifth week after surgery (a patient with a giant craniopharyngioma, who developed a severe endocrine disorder, complicated by meningitis, after surgery). Regarding surgical complications, there were 3 cases of meningitis, 2 cases of hydrocephalus (both in craniopharyngiomas, requiring ventriculoperitoneal shunting), and 1 case of brain infarction (a patient with a huge astrocytoma, who developed a small, asymptomatic infarction in the right ACA territory). There was 1 case of wound infection and 1 case of deep venous thrombosis.
3.4. Endocrinological deficits
Fig. 6. Complete removal of the tumour. 1 - optic chiasm; 2 - right optic tract; 3 basilar apex.
After surgery, only 7 patients did not need permanent hormonal substitution therapy (2 craniopharyngiomas, 4 astrocytomas, 1 ganglioglioma). Panhypopituitarism developed in 22 patients (76%). Permanent postoperative diabetes insipidus was present in 18 patients (62%). Postoperative obesity developed in 2 cases of craniopharyngioma, both of which underwent total removal of the tumour. The incidence of permanent endocrinological disturbances was significantly higher in patients with total tumour removal, compared to cases of subtotal and partial removal (Fisher’s exact test - one-tailed p value = 0.031) (Table 4).
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Fig. 7. Female, 32 years old, intraventricular craniopharyngioma. (a) pre-operative; (b) after complete removal.
Fig. 8. Male, 11 years old, partially intraventricular craniopharyngioma with extension into the posterior fossa. (a) pre-operative; (b) after complete removal.
Fig. 9. Male, 32 years old, optic pathway astrocytoma. (a) pre-operative; (b) after extensive removal (>90% of tumour mass).
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Fig. 10. Female, 29 years old, optic pathway astrocytoma. (a) pre-operative; (b) after partial removal (50–90% of tumour mass).
Table 2 Extension of tumour removal based in postoperative MRI (number of patients and diagnosis). Total removal
15 (14 craniopharyngiomas, 1 germinoma)
Extensive subtotal removal (>90% of tumour) Partial removal (50–90% of tumour)
9 (4 craniopharyngiomas, 2 astrocytomas, 2 germinomas, 1 ganglioglioma) 5 (3 astrocytomas and 2 germinomas)
Table 3 Mortality and morbidity. Morbidity
Mortality
4. Discussion
Meningitis Hydrocephalus with VP shunting Asymptomatic brain infarction Wound infection Deep venous thrombosis Total Severe endocrine disorder, meningitis
3 (10.3%) 2 (6.9%) 1 (3.4%) 1 (3.4%) 1 (3.4%) 8 (27.5%) 1 (3.4%)
Table 4 Endocrinological deficits and extent of surgical removal. Hormonal substitution therapy
Total removal Subtotal or Partial Removal
Yes
No
14 8
1 6
p = 0.031.
3.5. Visual deficits (Table 5) In 25 of the 29 cases studied, there was no visual deterioration after surgery, and in 7 cases, there was a reduction in preoperative bitemporal field defects. In 4 patients (14%), there was postoperative visual deterioration, with worsening of pre-operative field defects (3 cases with increases in amputation in the temporal field) or the development of new postoperative deficits (one case of unilateral amaurosis). In these 4 patients, the surgical removal was complete.
The management of lesions involving the third ventricle represents a challenge for neurosurgeons, with a significant risk of damaging the optic pathways and the hypothalamus [1–3,6,8,10–12]. The opening of the lamina terminalis as an access to the third ventricle was described by Dandy [13] and was used by Cushing [14] for the treatment of a pituitary adenoma. It was used for intraventricular craniopharyngioma by King [15] in 1979. The lamina terminalis is a thin white matter membrane located in the inferior part of the anterior ventricular wall, between the optic tracts, and it connects the anterior commissure to the posterior limit of the optic chiasm. It is crossed by the anterior cerebral arteries and the anterior communicating artery. During surgery, the boundaries of the lamina terminalis are not easy to distinguish, particularly from the medial border of the optic tracts and from the posterior limits of the chiasm. The opening of the lamina terminalis is usually necessary for tumours extending into the anterior part of the third ventricle and especially for those that develop in its anteroinferior aspect [2,6,11]; Fahlbusch et al. [1] reported the need for lamina terminalis opening in cases of retrochiasmatic involvement. When tumours are limited within the infrachiasmatic and prechiasmatic space, the opening of the lamina terminalis is usually not necessary [2]. Opening the lamina terminalis provides access to the inferior part of the third ventricle, and it can be performed through transcranial approaches (unilateral subfrontal, bilateral subfrontal, frontal interhemispheric or several variations of pterional approaches) [3,6,8,9,11,16] and transsphenoidal approaches. The transcallosal
Table 5 Visual disturbances. 25 patients - no postoperative campimetric deficit worsening No preoperative campimetric deficit 6 patients Preoperative bitemporal deficits 12 patients Preoperative bitemporal deficits 7 patients 4 patients – postoperative campimetric deficit worsening Increase in amputation in left temporal field 2 patients Increase in amputation in right temporal field 1 patient Left amaurosis 1 patient
Stable after surgery Stable after surgery Improved after surgery
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transventricular approach has also been used in surgery for lesions in the third ventricle. The pterional approaches and their variations (pterional, orbitopterional, orbitozygomatic) allow for good visualisation of the optic nerves and chiasm bilaterally, of the anterior cerebral and anterior communicating arteries complex, and the pituitary stalk. It is suitable for most suprasellar tumours [9,17,18], but it can have disadvantages, which can be addressed by midline approaches. The lateral routes lead to narrowing of the lamina terminalis corridor and can result in a lack of visualisation of the contralateral structures and the superior aspect of third ventricle and inferior projection into the interpeduncular cistern [3]. Accordingly, pterional approaches have their main limitations when addressing tumour extension into the upper third ventricle and retrosellar space [17]. Also, an increased incidence of postoperative visual deterioration was reported with the use of pterional approaches, compared to midline approaches [6]. Subfrontal access through the anterior cranial fossa, combined with a trans-lamina terminalis approach, is another possible method for addressing lesions in this particular location [17,19]. The midline access ensures maximisation of the lamina terminalis corridor, reducing the blind spots associated with lateral approaches at the superior, inferior and contralateral levels [20]. The bilateral frontobasal approach, with dissection below both frontal lobes, provides maximum working space, with excellent visualisation of the lower third ventricle and the lamina terminalis, and it can be particularly advantageous in treating large tumours that extend bilaterally into the middle fossa and the retrosellar space [1,17]. The main disadvantages of this approach are the opening of the frontal sinus, damage to the olfactory tracts and surgical trauma to the frontal lobes. The frontobasal interhemispheric approach was developed with the aim of minimising the potential for brain tissue damage, combined with a wide operative field [11,16]. Endoscopic-assisted surgery with a subfrontal approach, using supraorbital trans-eyebrow access to the lamina terminalis and third ventricle, was recently developed [9]. The small craniotomy minimises brain exposure to surgical trauma, and the operative time is reduced due to faster opening and closure. With the use of an endoscope, there is access to both lateral walls of the third ventricle [9,21]. However, the long working distance can be problematic, and this approach has limitations in surgery for large tumours. In addition, serious problems can occur when dealing with situations of cerebral edema and brain herniation through the narrow space provided by a small craniotomy [9,22]. The transnasal transsphenoidal approach is suitable for predominantly sellar lesions with sella turcica enlargement. This approach has known major advances with combined use of the endoscope, and its indications have been expanded to supradiaphragmatic lesions [2,20]. However, retrochiasmatic and retroinfundibular aspects of tumours remain difficult to remove transnasally, and fine microdissection of the vital neurovascular structures adhering to the tumour can be very challenging via a transnasal approach. The transcallosal transventricular approach is preferable for predominant third ventricle lesions [8] with lateral ventricle projection through an enlarged foramen of Monro. This access permits direct exposure of the anteriosuperior aspect of third ventricle, thus minimising cerebral injury. The main problem with this approach is the difficulty in identifying the optic chiasm and pituitary stalk, as well as the basal portion of the tumour [3,17]. The transcallosal route often must be combined with an anterolateral or midline basal approach for tumour removal maximisation, and there are risks of injury to midline vascular (veins draining into the superior sagittal sinus, pericallosal arteries, thalamostriate and internal cerebral veins) and neuronal structures (fornix and anterior
commissure). Mutism and short-term memory disturbances have also been reported with this technique [8]. In the presented cases, a bilateral subfrontal approach was used. However, the approach initially began by subfrontal dissection only on the right side, with identification and dissection of both olfactory nerves. Liberation of the left frontal pole was performed only after the optic nerves were identified. At this point in the surgery, significant amounts of CFS have already been removed due to cisternal opening, and the brain is usually relaxed. In this manner, it was possible to minimise brain retraction and potential surgical injury and simultaneously to obtain maximal exposure of the optic-chiasmatic region and the lamina terminalis corridor. Endocrinological complications [23,24] and visual deterioration [1,24] are possible complications of surgery for lesions in this region. Significant mortality has also been described [1,25,26]. However, this morbidity might be not directly related to opening of the lamina terminalis but rather to difficult dissection of the tumour from surrounding structures. The aim of this work was to study cases with opening of the lamina terminalis and to compare the results with those described in the literature for suprasellar lesions. 4.1. Extent of tumour removal Pathology and adhesion of the tumour to neural and vascular structures are the most important issues regarding the possibility of total removal, as well as the experience of the surgical team [3,27]. Adhesion to neural structures, namely the optic nerves, optic chiasm and optic tracts, as well as the hypothalamus, can also be important regarding the onset of new visual and hormonal deficits after surgery [1–4,6,8–12]. In our series, the trans-lamina terminalis approach made possible extensive removal (more than 90% of the tumour mass) in 24 (83%) of 29 patients and total removal in 15 cases (52%). Regarding only craniopharyngiomas, complete removal was performed in 14 of 18 patients (78%) and subtotal extensive removal in the remaining 4 cases. Thus, this approach allows for the achievement of a rate of total and subtotal extensive tumour removal similar to that described for craniopharyngiomas in general (61–92%) [1,10,28] and the same rate described for intraventricular and large lesions [4]. Also important is that, considering all of the cases, it was always possible to remove more than 50% of the tumour mass, including in cases of astrocytoma of the optic pathways (in these tumours, the role of surgery is limited, and the objective of surgery was only partial removal) [29,30]. 4.2. Surgical complications The rate of surgical complications was significant in this series. Mortality in 1 case was related to serious endocrine disturbances, associated with meningitis. Infectious complications were frequent, as was hydrocephalus (14% and 7%, respectively). The importance of high-quality neurocritical care in the immediate postoperative period must be particularly emphasised with surgery for tumours in this location, because the management of endocrine deficits can be a challenging, life-threatening problem. 4.3. Postoperative endocrine disturbances Hormonal postoperative deficits were common in our cases (76% of cases with postoperative panhypopituitarism and 62% with permanent postoperative diabetes insipidus). The floor of the third ventricle was disrupted by the tumour in many cases, especially in craniopharyngiomas [31], and excision from hypothalamic structures can be particularly difficult [5,11], although sometimes it is possible to preserve the pituitary stalk. In the present series, the
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pituitary stalk was preserved in 8 cases, but only 7 patients did not require hormonal replacement after surgery. An association between this particular approach and the occurrence of endocrine deficits has been not established, because hormonal problems are common after surgery for lesions in this region, especially tumours of medium and large size, with or without opening of the lamina terminalis [1–4,6,11,16,32,33]. A high incidence of postoperative hormonal deficiencies has been commonly reported in the literature, using different approaches. Kitano et al. [2] reported postoperative hormone deficits on four different axes in 75–90% of their patients with suprasellar craniopharyngiomas submitted to extended transsphenoidal surgery; they also reported a 50% incidence of diabetes insipidus in the same study. In a series of 26 children with giant craniopharyngiomas [34], using a pterional approach in the majority of cases, they reported 63.2% of their patients developing diabetes insipidus, and each patient required a mean of 2 hormones secondary to anterior pituitary dysfunction after surgery. In their giant craniopharyngioma report, Fahlbusch et al. [1] reported that up to 90% of patients suffer from lifelong endocrine disturbances according to the literature, although they reported a lower incidence of postoperative endocrine disturbances in their series. Although other reviews have shown better results [24], a recent review of craniopharyngioma morbidity [26] stated that complete hypopituitarism is encountered in a majority of craniopharyngioma cases, with deficiencies in at least three pituitary hormones reported in 54–100% of patients and a prevalence of diabetes insipidus of 81%. In the present series, as described by other reports [1,17], there was a significant association between the extent of tumour removal and the occurrence of hormonal deficits; except in one case, in all of the patients who did not require hormonal replacement, total removal was not performed. It is possible that this high prevalence of endocrine problems was related to the size and pathological types of the tumours and their adhesion to the hypophyseal and hypothalamic structures and not directly to opening of the lamina terminalis. In this regard, opening of the lamina terminalis was not associated with an increased prevalence of postoperative hormonal deficits, with a rate of endocrinological and hypothalamic dysfunction in the same range as that described for tumours with medium and large dimensions in this region [17,26].
4.4. Postoperative visual field defects In our results, visual deficits occurred after using the translamina terminalis approach, with the development of new deficits or the enlargement of visual field defects after surgery in 4 patients (14%). However, visual disturbances are not uncommon with surgery for suprasellar pathologies [1,2,12,34], and deficits are not always attributable to opening of the lamina terminalis, even if it is probable that the postoperative enlargement of bitemporal field defects in 3 patients was related to this particular approach [4]. In the studied patients, the incidence of postoperative visual deficits was in the range described for lesions in this region [26]. In our series, extensive tumour removal was possible in most cases using the trans-lamina terminalis approach. The results regarding general postoperative complications and visual and hormonal problems were in the expected ranges for tumours with similar size and location, with or without opening of the lamina terminalis. Accordingly, this approach allowed for extensive tumour removal without a significant increase in postoperative deficits, and surgeons should be familiar with it when treating lesions in this location.
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5. Conclusion The trans-lamina terminalis approach allows for extensive removal of most suprasellar lesions involving the third ventricle or purely intraventricular tumours. Although hormonal and/or visual deficits occurred, these might be attributable to the extensive dimensions of the tumours and adhesion of the tumours to surrounding neural and vascular structures and not directly to opening of the lamina terminalis.
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