Surgical management of colloid cyst of the third ventricle—a study of 105 cases

Surgical management of colloid cyst of the third ventricle—a study of 105 cases

Neoplasm Surgical Management of Colloid Cyst of the Third Ventricle—A Study of 105 Cases Ketan I. Desai, M.Ch., Trimurti D. Nadkarni, M.Ch., Dattatra...

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Neoplasm

Surgical Management of Colloid Cyst of the Third Ventricle—A Study of 105 Cases Ketan I. Desai, M.Ch., Trimurti D. Nadkarni, M.Ch., Dattatraya P. Muzumdar, M.Ch., and Atul H. Goel, M.Ch. Department of Neurosurgery, King Edward Memorial Hospital, Seth G. S. Medical College, Parel, Mumbai, India

Colloid cyst of the third ventricle is a relatively rare intracranial tumor. It generates tremendous interest for the neurosurgeon because of its benign nature, deep location, and an excellent prognosis when diagnosed early and excised.

Eighty-six patients came for follow-up, with a range from 1 month to 25 years (average 3 years and 8 months). Postoperatively, transient recent memory deficits occurred in 14 patients, while a permanent recent memory loss was noted in 2 patients. There was no incidence of postoperative disconnection syndrome or behavioral disturbance. A CT scan was performed in 44 patients during follow-up. Recurrence was detected in 1 patient in whom the cyst had been partially excised.

METHOD

CONCLUSIONS

Desai KI, Nadkarni DP, Muzumdar DP, Goel AH. Surgical management of colloid cyst of the third ventricle—a study of 105 cases. Surg Neurol 2002;57:295–304. BACKGROUND

A retrospective analysis of 105 cases of third ventricle colloid cyst treated between 1967 to 1998 was conducted. The clinical presentation, radiological findings, different surgical approaches, and outcome were analyzed. The transcallosal and transcortical-transventricular approaches were predominantly used. Memory and psychological assessment were carried out both pre- and postoperatively. A computerized tomography (CT) scan was performed during follow-up.

Colloid cyst, although a benign tumor, is surgically challenging because of its deep midline location. Early detection and total excision of the colloid cyst carries an excellent prognosis. © 2002 by Elsevier Science Inc. KEY WORDS

Colloid cyst, third ventricle, transcallosal approach, transfrontal approach, transventricular approach.

RESULTS

The male to female ratio was 1.5:1. The age of the patients ranged from 10 to 68 years. Headache was the most common symptom. Papilledema and short-term memory disturbances were the most common signs. In 5 patients the colloid cyst was detected incidentally. Surgery for colloid cyst was performed in 93 patients. Transcallosal and transcortical-transventricular approaches were performed in 62 and 30 patients, respectively. In 1 patient the cyst was excised through the subfrontal lamina terminalis approach. Total excision was achieved in 90 patients, while partial cyst excision was done in three patients. Moderate to severe lateral ventricular enlargement was found in 76 patients at presentation. A ventriculoperitoneal shunt was the only surgical procedure performed in 7 patients. In 16 patients colloid cyst excision was conducted after cerebrospinal fluid (CSF) diversion via a shunt. No surgical treatment of any kind was performed in 5 patients. Five patients died.

Address reprint requests to: Professor Atul Goel, M.Ch., Head, Department of Neurosurgery, King Edward Memorial Hospital, Seth G. S. Medical College, Mumbai 400 012, India. Received February 24, 2000; accepted October 29, 2000. © 2002 by Elsevier Science Inc. 655 Avenue of the Americas, New York, NY 10010

hird ventricular colloid cysts constitute about 0.5 to 1% of all intracranial tumors [2,3,6,18, 56,61,80]. Surgery on this centrally located benign tumor has challenged neurosurgeons ever since Dandy successfully removed a colloid cyst in 1921 [23]. The classical postural nature of headaches that have been related to third ventricular colloid cysts by Dandy and Stooky is debatable [24,81]. With the advent of computed tomography (CT) scan and magnetic resonance imaging (MRI), detection of colloid cysts has become more frequent and accurate [4,5,15,20,32,42,44]. The operative mortality of 20% reported by Dandy has been reduced dramatically to almost nil by the use of microneurosurgical techniques [11,24,44,56,62]. Various surgical options are available ranging from invasive transcortical and transcallosal approaches to those that are minimally invasive such as stereotactic aspiration and endoscopic colloid cyst excision.

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1

Cyst Size (based on maximum diameter as measured on CT and MRI scans)

SIZE

OF THE CYST

NO. OF PATIENTS

⬍1.5 cm (small) 1.5–3 cm (medium) ⬎3 cm (large)

7 67 11

2

Age Distribution

AGE (YRS)

NO. OF PATIENTS

1–10 11–20 21–30 31–40 41–50 ⬎50

2 12 40 28 12 11

Material and Method We analyzed 105 cases of third ventricle colloid cyst managed in our department between 1967 and 1998. The clinical records, radiological findings, and operative and follow-up notes were studied retrospectively. In the pre-CT scan era, pneumoventriculograms, ventriculograms, and angiograms were done. After 1982, CT or MRI were performed in all patients. Based on the maximum diameter as measured on the CT or MRI scans, the colloid cysts were divided into three categories—small (⬍1.5 cm), medium (1.5 to 3 cm) and large (⬎3 cm), respectively (Table 1). Surgery on the colloid cyst was performed in 93 patients. The microscope was used for surgery after 1972 in 87 cases. Transfrontal-transventricular and transcallosal-transventricular were the two main approaches used. The callosal incision in the transcallosal approach was a maximum of 2.5 cm, averaging 1.5 cm. The transfrontal approach was performed through the middle frontal gyrus of the nondominant lobe. A CT scan was obtained in 44 patients during follow-up. A series of clinical tests were performed to assess the interhemispheric somatosensory and motor transfer of information and the memory function. These tests included somesthetic naming of common objects, assessment of graphesthesiae, and cross-matching of tactile localisation. Psychometric evaluation of general intelligence and memory function was performed.

Results CLINICAL FEATURES The male to female ratio was 1.5:1. The age ranged from 10 to 68 years with 64.8% of patients in the third and fourth decades (Table 2). The duration of clinical complaints at the time of presentation varied from 1 week to 4 years with an average of 8 months. Headache was the most prominent clinical symptom, occurring in 92.3% of patients. It was generalized, intermittent, and was often accompa-

nied by blurred vision and vomiting. Variation in the intensity of headaches with change of posture was noticed in 2 patients (1.9%). The presenting features are enumerated in Table 3. Recent memory was affected in 10 (9.5%) patients. The memory disturbance was noted in patients harboring large colloid cysts. Papilledema was seen in 76 (72.3%) patients. Four patients, ranging in age from 55 to 60 years, had a clinical presentation suggestive of normal pressure hydrocephalus (NPH). They had symptoms of progressive dementia and gait disturbances. Three patients in addition had urinary incontinence. The average duration of symptoms for these patients was 13 months. Four patients were admitted in a comatose state. They all had a large colloid cyst. None of these patients recovered consciousness and finally succumbed. INVESTIGATIONS In the pre-CT scan era, air and contrast ventriculograms were performed in 8 and 12 patients, respectively. Cerebral angiography was performed in 9 patients. The typical angiography picture of upward convexity of the initial segment of the internal cerebral vein was found in 2 patients. CT scan and MRI

3

Clinical Features

CLINICAL

FEATURES

Headache Ataxia Diminished vision Papilledema Urinary incontinence Short term memory deficits Seizures Coma Hemiparesis Normal pressure hydrocephalus

NO. OF PATIENTS 97 27 21 76 18 10 8 4 3 4

Colloid Cyst of Third Ventricle

4

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Surgical Approaches

SURGICAL

APPROACHES

Transfrontal-transventricular a) Transforaminal b) Subchoroidal Transcallosal-transventricular a) Transforaminal b) Interforniceal c) Subchoroidal Subfrontal-lamina terminalis

NO. OF PATIENTS 30 29 1 62 58 3 1 1

were conducted in 82 and 6 patients, respectively. CT scans were preferentially performed because of their low cost. Moderate size colloid cysts were the most common and were found in 67 patients, while 11 and 7 patients had large and small colloid cysts, respectively. The colloid cyst density was variable on plain CT scans. Hyperdense cysts were most common, occurring in 64 patients. The cyst was isodense and hypodense in 13 and 5 patients, respectively. Moderate to severe hydrocephalus was present in 76 (72.3%) patients. SURGICAL TREATMENT Surgical excision of the colloid cyst was performed in 93 (88.5%) patients. In 12 (11.4%) patients the colloid cyst was not excised. In the latter group, ventriculoperitoneal shunting was the only surgery performed in 7 patients. One patient who was admitted in a comatose state died after shunt surgery. Five patients refused surgical intervention of any kind. The cyst excision was total in 90 patients, and partial in three patients. In 77 (73.3%) patients, the colloid cyst was excised without a prior shunt operation, while in 16 (15.2%) patients the excision of the colloid cyst was conducted after a shunt operation. Shunt surgery was performed in patients treated before 1988, after which it was abandoned. The various surgical approaches adopted are enumerated in Table 4. The operating microscope was used in 87 cases. In 30 patients the colloid cyst was excised by a transfrontal-transventricular approach through the middle frontal gyrus, while in 62 patients the excision was by transcallosal route. The transfrontal-transventricular approach was abandoned after 1990. In 1 patient the cyst was excised by the subfrontal lamina terminalis approach. The transventricular corridor of entry into the third ventricle was through foramina of Monro in 87 patients, and through the interforniceal and

subchoroidal route in 3 and 2 patients, respectively. The foramen of Monro was enlarged in four patients by dividing the anterior column of the fornix. The standard practice was to rupture the cyst wall after exposure. The jelly-like cyst contents were evacuated and then the cyst wall was excised by gentle dissection. The capsule was noted to be attached “probably” to the choroid plexus of the third ventricle by a pedicle directed posteriorly in most of the patients. COMPLICATIONS OF TRANSCALLOSAL SURGERY The most common complication was cortical venous injury. Four patients developed cortical venous infarcts with associated varying grades of limb weakness. Injury to the thalamostriate vein and the pericallosal artery occurred in 3 patients each. Additional complications were cerebrospinal fluid leak in 4 patients and meningitis and wound infection in 2 patients each. There was no incidence of shunt infection or blockage. COMPLICATIONS OF TRANSCORTICAL SURGERY The most common complication encountered was seizures in 8 patients. Other complications that occurred in these patients were: intracerebral hematoma in 2, CSF leak in 4, meningitis in 3, wound infection and shunt blockage in 2 patients each. MORTALITY Death occurred in 7 (4.7%) patients. All 4 patients who were admitted in a comatose state died. One patient died within a few hours after admission before any surgical intervention could be performed. The second patient succumbed after shunt surgery. The remaining 2 patients died after excision of the colloid cyst as a result of pulmonary complications. One patient who developed a large cortical venous infarct after transcallosal cyst excision died because of severe increase in the intracranial pressure. The remaining 2 patients died of postoperative pyogenic meningitis. INCIDENTAL COLLOID CYST In 5 patients the colloid cyst was detected incidentally. In this group, 3 patients had small while 2 patients had large cysts. Patients with small cysts were treated conservatively and were asymptomatic at 3 years’ follow-up. The patients with large cysts underwent surgical excision.

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FOLLOW-UP Postoperatively 80 (76.2%) patients returned for follow-up which ranged from 1 month to 25 years (average 3 years and 8 months). Thirteen patients did not return for follow-up after surgery. A CT scan was conducted in 44 patients during follow-up. Symptomatic recurrence was noted in 1 patient after surgery. This patient had undergone a partial excision of the cyst. This cyst was re-excised. The follow-up CT scans showed resolution of the hydrocephalus in all patients. Postoperatively 16 (17.2%) patients had recent memory loss, which was transient in 14 (15%) and permanent in 2 (2%) of patients. Of these patients, the recent memory deficits had been noted in 10 (9.5%) patients preoperatively and were noted in 4 additional patients after surgery. Foraminal enlargement had been conducted in these 4 patients as they had harbored large colloid cysts. Two patients in this group had permanent recent memory loss, while 2 patients had transient recent memory loss after surgery. The 2 patients with permanent recent memory loss were followed up for 15 and 17 years, respectively. The transient memory loss was more evident during the first few weeks after surgery, was more pronounced for recent events, and recovered completely within 6 months of surgery. The memory loss in these cases was subtle and could be detected only by a battery of clinical tests. The behavioral disturbance noted preoperatively in 4 patients suffering from normal pressure hydrocephalus syndrome recovered completely after surgery. There was no clinical evidence of disconnection syndrome or mutism after transcallosal surgery in any patient. The results indicated no measurable deficits in the interhemispheric transfer of somesthetic information or complex perpetual motor learning tasks requiring continual sensory-motor integration.

Discussion Colloid cysts have provoked interest in neurosurgeons because of their controversial origin, benign histology, often dramatic clinical presentation, and the variety of possible treatment options [21,53,76, 89]. Mathiesen et al [61] and Nitta and Symon [67] documented male sex predominance, as noted in our series. Camacho et al found no sex difference in their large series from Mayo Clinic [16]. There was no specific age group predominance in any of these series; however, in our series 64.7% of patients were in their third and fourth decades. Since Wallmann reported the first documented

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case of colloid cyst of the third ventricle in 1858, there has been much debate and controversy over the site of origin of the colloid cyst [86]. For many years the cyst was thought to originate from the paraphysis [81]. Kappers in 1955 concluded that these cysts arose from the diencephalic ependymal pouches [51]. Yenerman suggested the choroid plexus as an alternate site of origin [89]. Shuangshoti et al proposed a neuroepithelial origin of the cyst [79]. The symptoms produced by colloid cysts of the third ventricle are primarily those of increased intracranial pressure and are non-localizing [16]. Excision of the colloid cyst results in amelioration of the symptoms and signs of increased intracranial pressure in addition to the resolution of the hydrocephalus. The so-called classical history of the colloid cyst of the third ventricle, manifested by paroxysmal attacks of headache associated with change in head posture, is relatively rare in our series and was observed in 2 patients [14,21,52,90]. The clinical symptoms were of relatively long duration in most of our patients. The average duration of symptoms at presentation was 8 months. The clinical features resembling normal pressure hydrocephalus were associated with colloid cyst in 4 (3.8%) patients. The possibility of a colloid cyst as a cause of normal pressure hydrocephalus needs to be considered [4,68]. Acute neurological deterioration in such patients with an associated colloid cyst has been reported after a lumbar puncture [56]. Rapid deterioration with sudden death because of impaction or acute hydrocephalus can occur, indicating the importance of early diagnosis and treatment of this benign and potentially curable condition. Four patients were admitted with a sudden neurological deterioration and in a comatose state. These patients had large colloid cysts, and all ultimately died. Chan and Thompson reported acute deterioration in 4 out of 12 patients with colloid cysts [21]. They have recommended unilateral ventriculostomy as a life-saving measure in such a condition before undertaking colloid cyst excision. The role of the fornix in the memory function has long been debated. Memory impairment is not an unusual postoperative complications of third ventricle colloid cyst surgery and represents a matter of substantial concern during surgery. Following forniceal lesion it is observed that the remote memory is intact while there is loss of memory for recent events [45,65]. A lesion of the fornix does not result in total hippocampal disconnection, as other connecting pathways remain intact [9,16,45,46,50,65, 75]. Bengochea et al sectioned the fornix bilaterally

Colloid Cyst of Third Ventricle

for treatment of epilepsy without any incidence of memory loss [88]. Nelson et al reported that patients with bilateral forniceal damage from a malignant tumor had no impact on memory function [33]. Little et al reported no incidence of memory loss or personality changes following division of the anterior column of the fornix in patients with colloid cysts [56]. However, in none of these cases was a detailed memory assessment done to substantiate the findings. Some investigators find little influence of one forniceal lesion on recent memory if the contralateral fornix is intact [88]. Sixteen patients in this series had short-term memory loss. Of these 14 patients had transient memory loss and it was permanent in two. The transient memory loss noted in 10 patients preoperatively was probably because of stretching of the fornix by the colloid cyst. In 4 patients, forniceal manipulation from mild to severe degree was carried out during surgery, and these patients developed recent memory deficits. All patients who had memory impairment had a relatively large colloid cyst. From our experience we conclude that an incision of the column of the fornix invariably results in recent memory loss of varying severity [19,77]. In the pre-CT scan era ventriculography was the most reliable investigation for the demonstration of third ventricle pathology. On angiography, a convexity in the initial segment of the internal cerebral vein was diagnostic, besides evidence of dilatation of the lateral ventricles [11,42,52,56]. The density of the colloid cyst on plain CT scan is variable. Often colloid cysts are iso- or hypodense relative to the brain parenchyma, but sometimes have a center of higher density. The density of the cyst probably depends upon the cholesterol content within the cyst [6,15,32,42,48,69,74]. In our series the majority (78%) of patients had hyperdense cysts. Colloid cysts appear heterogeneous on MRI despite a homogeneous appearance on histology. On short relaxation and echo (TR/TE) sequences the cyst has a high signal in its central part and low signal in the periphery. The high signal is related to its high cholesterol content. The pattern is reversed on the long TR/TE sequences. The density of the cyst is directly correlated with the viscosity of the cyst fluid [29,58,63,78,85]. This fact is helpful for stereotactic colloid cyst aspiration. The hyperdense cysts are difficult to aspirate compared to isodense/hypodense cysts because of the high viscosity of the hyperdense cyst fluid [6]. Improved diagnostic tests and widened indications for CT and MRI studies have increased the number of incidentally found colloid cysts [59]. The management of the asymptomatic incidental

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colloid cyst is a topic of debate. The rate of growth of colloid cysts is not known and whether all these cysts eventually become symptomatic is unclear. Sudden deterioration followed by death has not been reported in a patient with a colloid cyst of less then 1 cm in size [12,16,21,76]. In our series, the three patients with small, incidentally detected colloid cysts remained asymptomatic for almost 3 years without any surgical intervention. However, it appears that patients with cysts larger than 1.5 cm should be considered for surgical excision, as the cysts are likely to become symptomatic and may even prove fatal [47,71]. Macdonald et al stressed that younger patients are more likely to become symptomatic during their lifetime and thus, need surgery [57]. The use of microneurosurgical techniques has changed the entire outcome of colloid cyst surgery. Microneurosurgery not only helps in reducing morbidity and mortality but also improves the general prognosis of this benign but deep-seated lesion [2,5, 6,13,16,30,44,60,67]. The transcallosal approach remains the procedure of choice for colloid cyst excision. The cortical incision is avoided, thereby minimizing the risk of seizures. [22,28,34 –38,40,73, 87,91]. The cerebral venous infarct secondary to a cortical vein occlusion causing serious neurological deficits is the most significant complication [7,13, 16,20,30,36,44,54,55,60,66,67,72,80,84]. Occasional thrombosis may occur in the superior sagittal sinus because of retraction. In our series, of the 62 patients who were operated by the transcallosal route, 4 (6.4%) patients had symptomatic cortical venous infarcts with varying degrees of neurological deficits; 1 patient died as a result of this. Apuzzo et al recommended cerebral angiography before surgery to map out cortical venous anatomy [6]. Neuronavigation was not employed in any of our cases. The occurrence of disconnection syndrome depends upon the site and the length of the incision in the corpus callosum. A major callosal incision involving a large segment of the corpus callosum has been reported to result in severe impairment of interhemispheric transfer of sensory, motor, and tactile information. Jeeves et al observed impairment of the tactile data only with preservation of visual transfer on careful testing in patients who had corpus callosal incisions involving the anterior and mid corpus callosum. An incision of less than 2.5 cm in the anterior body of the corpus callosum, necessary for exposure of ventricular system, does not appear to result in any disconnection disorder [7,10,16,22,28,34 – 40,49,72,73,80,87,91]. There was no incidence of such a disorder in our patients.

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The transcortical-transventricular approach described by Dandy in 1933 involves incision in the brain parenchyma, risk of seizures, and difficulty in obtaining and maintaining adequate exposure, particularly when the ventricles are not large [5,8,19, 23,36,42,55,56,62,83]. In our series, seizures were frequent with this approach (8/30 patients, 26.6%). Hydrocephalus secondary to obstruction of the foramen of Monro by the colloid cyst is common. Sixteen patients in our series underwent a shunt procedure before cyst excision. In the last 10 years of this study, the colloid cyst was excised directly without a prior shunt procedure. The follow-up CT scan showed complete resolution of the hydrocephalus after surgery. Hall et al observed that the hydrocephalus persisted even after successful aspiration or complete surgical removal of the colloid cyst [16,43]. The minimally invasive surgical procedures such as stereotactic colloid cyst aspiration and endoscopic colloid cyst excision have been reported to have less risk of morbidity and mortality when compared with surgical excision of the colloid cyst [1,7,11,22,25–27,31,41,53,61,74].

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COMMENTARY

The article by Desai and colleagues reports their experience with surgery for colloid cysts of the third ventricle—a retrospective analysis of 105 cases spanning 31 years of experience. The majority of patients underwent surgery via the transfrontal or transcallosal approach. Surgical outcomes for these operated patients were not dissimilar from those of other large series. The recurrence rate was low, although only half the patients underwent postoperative imaging. The importance of this article is to once again identify the major risks associated with removal of colloid cysts via the transfrontal or transcallosal approach. Although the major risks are small in nature, there is significant morbidity associated with these approaches and caution should be used by those surgeons who are not familiar with the transcallosal approach. The neuropsychological sequelae in those patients who underwent transcallosal approaches were not great, and demonstrate that this surgical procedure can be useful without rendering the patient neuropsychologically disabled. Although this article focuses on conventional approaches to the removal of colloid cysts, it fails to adequately compare those results with more recent reports of minimally invasive approaches to the removal of colloid cysts. More recent reports of minimally invasive endoscopic approaches illustrate the safety of this procedure, which does not carry the risk of cortical venous infarction, and its ability to relieve hydrocephalus without shunting. In minimally invasive approaches the capsule, which is attached to the roof of the third ventricle