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Intraventricular Meningiomas: A Series of 42 Patients at a Single Institution and Literature Review
Accepted Manuscript Intraventricular Meningiomas: A Series Of 42 Patients at a Single Institution and Literature Review Danica Grujicic, MD, Luigi Maria Cavallo, MD, PhD, Teresa Somma, MD, Rosanda Illic, MD, Mihailo Milicevic, MD, Savo Raicevic, MD, Milica Skender Gazibara, MD, Alessandro Villa, MD, Dragan Savic, MD, Domenico Solari, MD, PhD, Paolo Cappabianca, MD PII:
S1878-8750(16)30898-1
DOI:
10.1016/j.wneu.2016.09.068
Reference:
WNEU 4608
To appear in:
World Neurosurgery
Received Date: 1 June 2016 Revised Date:
14 September 2016
Accepted Date: 16 September 2016
Please cite this article as: Grujicic D, Cavallo LM, Somma T, Illic R, Milicevic M, Raicevic S, Gazibara MS, Villa A, Savic D, Solari D, Cappabianca P, Intraventricular Meningiomas: A Series Of 42 Patients at a Single Institution and Literature Review, World Neurosurgery (2016), doi: 10.1016/j.wneu.2016.09.068. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT INTRAVENTRICULAR MENINGIOMAS: A SERIES OF 42 PATIENTS AT A SINGLE INSTITUTION AND LITERATURE REVIEW.
1Clinical
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Danica Grujicic, MD1, Luigi Maria Cavallo, MD, PhD2, Teresa Somma, MD2, Rosanda Illic, MD3, Mihailo Milicevic, MD1, Savo Raicevic, MD4, Milica Skender Gazibara, MD5, Alessandro Villa, MD2, Dragan Savic, MD1, Domenico Solari, MD, PhD2, Paolo Cappabianca, MD2
Center of Serbia, Clinic of Neurosurgery, Medical Faculty University of
2Department
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Belgrade, Belgrade, Serbia
of Neurosciences and Reproductive and Odontostomatological Sciences,
3
Clinical Center of Serbia, Clinic of Neurosurgery, Belgrade, Serbia
4 Clinical 5
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Division of Neurosurgery, Università degli Studi di Napoli Federico II, Naples, Italy
Center of Serbia, Department of Pathological Anatomy, Belgrade, Serbia
Clinical Center of Serbia, Department of Pathological Anatomy, Medical Faculty
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University of Belgrade, Belgrade, Serbia
Corresponding Author:
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Teresa Somma
Department of Neurosciences and Reproductive and Odontostomatological
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Sciences
Division of Neurosurgery Università degli Studi di Napoli Federico II Via Pansini 5
80131 Naples, Italy
Tel +39 081 7462490 Fax +39 081 7462594 e-mail: [email protected]
ACCEPTED MANUSCRIPT KEYWORDS: meningioma, intraventricular, lateral ventricle, third ventricle, surgical complications, surgical mortality, survival.
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ABBREVIATIONS:
CSF: cerebrospinal fluid; CT: computed tomography; GCS: Glasgow coma
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scale; GOS: Glasgow outcome scale; IVM: intraventricular meningioma; MRI:
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magnetic resonance imaging.
ACCEPTED MANUSCRIPT ABSTRACT Background: Primary intraventricular meningiomas (IVMs) make up 0.5-5% of all intracranial meningiomas and represent one of the most challenging
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lesions in neurosurgery. Methods: Between 1990 and 2013, 42 patients (30 female, 12 male, mean age of 43.6 years) underwent the resection of their IVM. The removal was
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performed by posterior-parietal approach in 19 of the 40 lateral ventricle tumors, and one in the third ventricle meningioma. The transcallosal
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approach was used for three meningiomas, while other lesions underwent temporal (7 cases) and temporo-parietal approaches (12 pts) respectively. Results: The most common presenting signs were increased intracranial pressure (83.3%), visual impairment (78.6%) and cognitive changes (50%).
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Concerning tumor location, forty lesions (95.2%) were arising in the lateral ventricles, and two (4.8%) in the third ventricle, ranging in sizes from 3 to 10 cm. Total removal was achieved in 39 cases and the pathology report
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disclosed WHO grade I lesions in 41 cases. Hydrocephalus, CSF leakage and
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cerebral edema were the postoperative complications (7.15%); one patient died of respiratory problems not directly related to surgery. Thirty-five patients (83.3%) showed a six-months Glasgow outcome scale (GOS) of 5. One patient, that underwent partial resection, presented a recurrence after 1 year that remained stable until last follow-up. Conclusions: IVMs usually reach a large size before being diagnosed. The surgical treatment is the most suitable option and total removal should
ACCEPTED MANUSCRIPT represent the main goal of the procedure. The posterior-parietal transulcal approach and the temporo-parietal approach are the most common surgical
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routes used in our series.
ACCEPTED MANUSCRIPT INTRODUCTION Intraventricular meningiomas (IVMs) are extremely rare tumors, accounting for 0.5-5% of all intracranial meningiomas1-9, 9.8-14% of all intraventricular
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tumors and 20% of lateral ventricle tumors10,11. According to the literature, their distribution is 77.8% in the lateral ventricle, 15.6% in the third ventricle and 6.6% in the fourth ventricle4-6,8,9,12-61. They arise either from the stroma of
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the choroid plexus or from the tela choroidea and do not present any dural attachments. Intraventricular meningiomas often grow slowly and may reach
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large volumes before becoming symptomatic. Surgical removal of these lesions remains challenging in modern day neurosurgery because of the close relationships with vital structures, particularly the optic radiations, which if
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injured can lead to serious postoperative visual complications19,62-64. There are few large surgical series with long follow-up. We, therefore, report our experience on a series of 42 patients who underwent surgical removal of a
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purely intraventricular meningioma over a 23-year period, presenting in detail the clinical and neuroradiological findings, surgical results and
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management of peri- and post-operative complications.
MATERIAL AND METHODS We retrospectively reviewed data of patients diagnosed with IVMs, who were surgically treated at the Clinic of Neurosurgery at the Clinical Center of
ACCEPTED MANUSCRIPT Serbia, between 1990 and 2013. All the operations were performed using microsurgical technique. The series included 42 patients, 30 female and 12 male with a sex ratio
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(female/male) of 2.5. The median age at surgery was 55 years (range: 1–67; mean: 43.6).
All patients were symptomatic and the duration of initial symptoms prior to
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definitive diagnosis lasted from 1 week up to 5 years (median 12.1 months).
Preoperative imaging was computed tomography (CT) in 24 patients,
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magnetic resonance imaging (MRI) in 3 patients and 15 patients had both CT & MRI.
Tumor recurrence was defined by the presence of new pathological tissue on repeated MRI (not noticed at an earlier control) and regrowth of residual by
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further growth of tissue already detected on the previous post-operative
RESULTS
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MRIs.
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Preoperative symptoms
Thirty-eight patients (90.5%; 38/42) had a preoperative Glasgow Coma Scale (GCS) ≥ 13. The most common clinical presentation was increased intracranial pressure (83.3%) while the more frequent neurological sign was homonymous hemianopia (42.8%). (Table 1 summarizes the neurological status of the patients upon admission). Tumor features Concerning the location, fifteen tumors were located in the right lateral
ACCEPTED MANUSCRIPT ventricle and 25 were in the left lateral ventricle; thirty-five of them (83.3%) arose in the trigone. Three lesions (7.1%) were purely in the body of lateral ventricle and 2 (4.8%) in the temporal horn. One tumor was found purely into
lateral ventricle. Tumor sizes ranged from
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the third ventricle and one near the foramen of Monro with extension into the
1 to 10 cm with four tumors being (9.5%) < 3 cm, eleven (26.2%) between 3
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and 5 cm, seventeen (40.5%) between 5 and 7 cm and ten meningiomas (23.8%) were bigger than 7 cm in diameter. An extraventricular extension was
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observed in only three cases (7.1%), while hydrocephalus was presented in 12 patients (28.6%). Surgical outcomes
An external lumbar cerebrospinal fluid (CSF) drain was left during surgery to
procedure. Out of the
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reduce the intracranial pressure and removed at the end of the surgical
39 lateral ventricular meningiomas, 20 were resected via a
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posterior parietal transcortical approach (see figure 1), 12 via temporo-
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parietal (see figure 2) and 7 via temporal transcortical approach (see figure 3); two meningiomas arising from the body of the right lateral ventricular were resected via a transcallosal approach (see figure 4). (Table 2 summarizes the surgical approaches in relation to the location of the lesion). Out of the 42 ventricular meningiomas, total resection was achieved in thirtynine cases (92.8%) and partial resection was performed in only one case; it was a big size tumor (>7 cm) treated by posterior-parietal approach followed
ACCEPTED MANUSCRIPT by radiotherapy in the early 1990s. This patient had relapse of the tumor after twelve months, that remained stable until last follow-up. Finally, a biopsy followed by radiotherapy was performed in two cases: in these patients, the
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development of intraoperative cerebral edema and the occurrence of an intraoperative gastro-intestinal bleeding hindered the surgery. Histology
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The Pathology report revealed that the most of the lateral ventricular meningiomas (72.5%) was transitional type. However, two cases of third
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ventricular meningiomas were diagnosed as transitional and fibroblastic. (Table 3 summarizes the histological features of the tumors). Surgical Complications
Thirty-nine patients (93%) did not have any intraoperative or postoperative
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complications; postoperative CSF leak occurred in one patient and it spontaneously resolved after the placement of a lumbar drain. In the early ‘90s one patient affected by a right ventricular meningioma approached by
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posterior parietal approach, had massive cerebral edema during surgery and
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developed postoperative hydrocephalus. She was successfully treated with anti-edema therapy and temporary external ventricular drainage. Another patient, who was admitted at the hospital with increased ICP and progressive deterioration of consciousness, developed postoperative massive cerebral edema and, after 25 days in the ICU, he died of a pulmonary embolism. Indeed, this is the only case to be considered in the perioperative mortality rate - defined as death within 30 days postoperatively - esteemed as 2.4% (1 of
ACCEPTED MANUSCRIPT 42). Concerning medical complications, we had one case of gastrointestinal bleeding, two patients with myocardial infarction and two cases of
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respiratory problems, one of which is the aforementioned patient with massive pulmonary embolism that caused the patient's death; the remaining 88.1% (37/42) of cases did not have any medical or surgical complications.
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Clinical outcomes
The outcome was measured with the Glasgow outcome scale (GOS)65 at their
followed from 2 to 25 years.
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day of discharge and at 6 months after the operation; the patients were
Forty patients (95.2%) had a good GOS at discharge. Improved six months after surgery.
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The patient that developed massive cerebral edema and postoperative hydrocephalus, showed GOS 2 at discharge and GOS 3 six months after surgery.
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Visual outcome was considered at discharge and six months after surgery. All
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patients were evaluated pre- and post-operatively for visual acuity, and computerized visual field examinations were performed. The hemianopia and other visual field defects presented respectively in 18 and 13 of the patients: it improved/resolved in 6.5% of patients at discharge and in 93.5% of the cases 6 months after surgery. None of the patient presented postoperative visual deterioration. Optic nerve edema resolved in all 14 cases in which they were present, while optic atrophy remained unchanged during the long-term
ACCEPTED MANUSCRIPT follow-up in 4 patients. (Table 4 and 5 summarizes the GOS and visual outcome at the discharge and 6 months after the operations).
DISCUSSION
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IVMs are uncommon and therefore, the number of clinical series in the literature is limited, with most of them reporting relatively few patients. In
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the Cushing’s personal series of 313 meningiomas, only 1% was intraventricular2. The first description of an intraventricular meningioma was
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reported in 1854 by Shaw66, who described a tumor arising at the right trigone. Over time, several case series were published and in 1965 Delandsheer62 reviewed the literature identifying 175 cases of lateral ventricular meningiomas, and, in 1986, Criscuolo and Symon9 identified 400
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cases in the world literature. More recently, other series have been published and in 2003 Nakamura et al19 identified 132 additional cases of IVMs since 1986 and Ma et al67 described the surgical management of 43 meningiomas of
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18,20-60,68-75.
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the trigone area of the lateral ventricle resulting in a total of 575 cases4-6,8,12-
Among them, 457 occurred in the lateral ventricles ( 79,.5 %), 83 in the third ventricle (14.4 %), and 35 in the fourth ventricle (6 %). Tables 6 summarizes the key findings of published surgical series involving fifteen or more patients with IVMs since 20031,19,64,76-78. Incidence Meningiomas arising within the ventricular system are reported to have an
ACCEPTED MANUSCRIPT incidence of 0.5 to 3% of all intracranial meningiomas although this type of brain tumor is the second most frequent. Concerning the gender of patients affected by intracranial meningiomas, female preponderance is well
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documented. Data in the literature shows female predominance for IVMs ranging from 41% up to a maximum of 82%, with an average female-to-male ratio of 2:1. In our series we observed a predominance of women of 71.4%
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with a ratio of women to men of 2.5:1.
Generally, the risk of developing meningioma increases with age79, being that
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intraventricular meningiomas are most common over the third decade. During the last 12 years, the reported mean age of removed IVMs has varied from 39 to 47 years (Table 6). In our series the patients’ age ranged from 1 to 67 years and the mean age was 43.6 years (median 46.5). The mean age varies
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also in relation with the meningiomas’ location: for those of lateral ventricular in the literature it ranges from 20 to 50 years. Concerning third and fourth ventricular meningiomas, mean ages are 28.7 years and 35.7 years,
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respectively. In our series the mean age of lateral ventricular meningiomas
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was 44.6 years. Additionally, patients with third ventricular meningiomas in the present series were 21 and 28 years old at the time of surgery. As summarized by Nakamura19 in 2003, 78% of the IVMs were located in the lateral ventricles (most commonly arising in the trigone5,28,61,76), 16% in the third ventricle (although this is more common in childhood9,80,81), and 7% in the fourth ventricle. In our series of 42 IVMs, 40 tumors (95.2%) were located in the lateral ventricles, two in the third ventricle (4.8%) and none in the
ACCEPTED MANUSCRIPT fourth ventricle. As noted, IVMs are slightly more common on the left3,5,76 and this trend has been confirmed (27/40; 67.5%) in our series (Table 6).
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Clinical and radiological aspects In 1938 Cushing and Eisenhardt described five clinical features of trigonal IVMs:
(1)
symptoms
of
intracranial
hypertension;
(2)
contralateral
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homonymous hemianopia; (3) contralateral sensorimotor deficit; (4) cerebellar affection (>50 %), and (5) dysphasia and/or paralexia in left-sided tumors2.
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On the other hand, in 1961 Gassel and Davis82 affirmed that the lateral ventricles are the most silent sites of the meningiomas and that IVMs often reach such dimensions to be ranked as the largest intracranial tumors. Winkler83 suggested that symptoms and signs of IVMs may be caused both by
parenchyma.
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raised intracranial pressure and direct pressure on surrounding cerebral
Usually, these tumors grow slowly and reach a large size before becoming
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symptomatic, unless the lesion is located in a region where it compromises
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the CSF circulation. Duration of initial symptoms prior to definitive diagnosis of an intraventricular tumor is reported to last from only a few months up to 20 years and the clinical presentation is variable. The most common symptoms reported are headaches, nausea and vomiting, as well as visual field defects, speech disturbances, sensomotor deficits and seizures3,4,9,84. Other frequently reported clinical features include mental disturbances and gait instability; furthermore, Smith described a case of subarachnoid
ACCEPTED MANUSCRIPT hemorrhage due to lateral ventricle meningiomas with a clinical presentation indistinguishable from aneurysmal subarachnoid hemorrhage83,85. In our series, the IVMs reached very large sizes and the duration of symptoms
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varied widely from 1 week to 5 years. Thirty-eight of the patients had a preoperative GCS ≥ 13 and the most common clinical presentation were signs related to increased intracranial pressure followed by visual disturbances,
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cognitive changes, seizures and motor deficits. Visual field defects were the most common signs on neurological examination, followed by gait instability
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(Table 1). In particular, we observed that four patients with optic atrophy had a GCS ≤ 13 (respectively GCS 7, 8, 10, and 13); this is in line with longtime damage in the brain due to the presence of the tumor.
In the past, neuroradiological diagnosis of IVMs were based on
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ventriculography and pneumoencephalography. Gradually angiography became the investigation of choice as demonstrated by data retrieved from the literature75,86,87. Today CT and MRI are the safest and most accurate
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modality for diagnosing IVMs, the last one providing the most complete
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information to plan the surgical resection. At the early stage of this series 24 patients of our series underwent only CT, due to the high cost of MRI in our region. The appearance on imaging studies is similar to that of other meningiomas, being sharply defined and round, without the typical dural attachment3,80,84; they show increased density on CT scan. On MRI, IVMs usually are hypo- to isointense on T1-weighted images and iso- to hyperintense on T2-weighted images88,89. Calcifications are reported to appear
ACCEPTED MANUSCRIPT in 47% of all cases; and peritumoral edema can be present4,10. The main differential diagnosis, according to these features should take into account choroids plexus carcinoma/papilloma, ependymoma, glioma or central
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neurocytoma10,88. Hydrocephalus produced by lateral intraventricular meningiomas is usually localized at the ipsilateral trigone and temporal horn80.
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Concerning the use of DTI, it has to be said that has been recently introduced in the clinical practice and it has been reported that it gives invaluable help in
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retrieving information in regards to relationships between fiber bundles and lesions, especially in cases of intracerebral lesions90-93. Although the use of functional exams in the surgical planning of IVM is not widely described67, the functional MRI and DTI fiber tracking certainly will assume a relevant
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role in the management of these lesions. We did not have the opportunity to perform DTI in our patients, and yet, the rate of our complications was quite the same as compared to other series reported in the literature57. Therefore,
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both the approaches, adopted in our series, permited to access to tumors
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growing inside the ventricular cavity through a small corticectomy in a non eloquent area and without transgressing the optic radiation, which runs with an infero-lateral trajectory in regards to the ventricles94,95. In our opinion good knowledge of cortical and white matter anatomy is mandatory to perform a safe approach. Finally, it should be considered that intraventricular meningeomas have a very rare pathology and keeping in mind that the use of any pre and intra-
ACCEPTED MANUSCRIPT operative image guidance assistance may reduce the risk of complications related to the small case load of this disease.
Neuropathology
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Meningiomas are of great interest because they are featured with a variety of histological characteristics96. In the pertinent literature about intraventricular
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meningiomas, there is few data on the histological subtype1,3,4,9,19. The more frequent lesion figured out to be the meningothelial and fibroblastic types. In
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our series the majority of meningiomas were of the transitional type (71.4%) and only one was atypical (Table 3). Surgical treatment
The removal of the IVMs represents a neurosurgical challenge, because of the
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deep location, the proximity of motor, sensory, and language cortex, as well as the optic radiation and the vascular structures. Different surgical approaches were described for resection of these tumors:
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temporoparietal approach, transfrontal approach, posterior middle temporal
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gyrus approach, posterior inferior temporal gyrus approach, parieto-occipital approach and, transcallosal approach2,3,97-100. The aim of all surgical approaches is to minimize the risk of postoperative deficits by using small corticotomies, minimal retraction of surrounding functional brain tissue, early access and interruption of the tumor’s blood supply and piecemeal resection1. Furthermore, as reported by Fusco and Spetzler101, the choice of the surgical approach is defined by best access to the long axis of the lesion, minimization
ACCEPTED MANUSCRIPT of transcortical transgression, spectrum of the patient’s preoperative neurological deficit, and proximity to eloquent anatomic structures and pathways.
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Nowadays, the posterior parietal, the middle temporal gyrus and the transcallosal approach are the most frequently used routes61. The posterior parietal approach permits a good exposure of the tumor but restricted access
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to the tumor’s vessels. Above all, it can be adopted via both the dominant and non-dominant hemisphere, with a low risk of direct damage to the optic
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radiation; in fact, as shown by anatomic studies, the optic radiation runs inferolaterally to the ventricles, and the ventricular trigone can be reached through a posterior parietal route without interrupting it94,95. The middle temporal gyrus approach allows the early occlusion of the tumor feeding, i.e.
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the anterior and posterior choroidal artery branches, but it is burdened by an increased risk of damaging the inferior portion of the optic radiation; adversely, when it is performed through the dominant hemisphere it could
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result in language deficits. Finally, the transcallosal approach minimizes the
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risk of postoperative seizures as well as speech and visual disturbances, but it has
the
disadvantage
of
a
possible
visual–verbal
disconnection
syndrome3,8,9,98,99,102-105. In a case report, Couillard et al26 described the advantage of a combined temporal and parietal approach, resulting in a total tumor resection and excellent clinical outcome Fornari et al. suggested a more superiorly located cortisectomy, consisting in
ACCEPTED MANUSCRIPT a sagittal paramedian incision of the parietal cortex at a distance of 4 cm from the midline, that starts 1 cm behind the post-central fissure and is continued for 4–5 cm as far as the parieto-occipital fissure. This approach may be less
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harmful at least with respect to visual function3. In our series, of the 38 lateral ventricular meningiomas, 19 were resected via a posterior parietal transulcal approach, 12 via temporo-parietal and 7 via
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temporal approach, while two meningiomas of body of the right lateral ventricular were resected via a transcallosal approach. The third ventricular
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meningioma with extension into the lateral ventricle was treated by posterior parietal approach, while the transcallosal approach was used for the purely third ventricular meningioma. The posterior-parietal transulcal approach, between the superior and inferior parietal lobe, and the temporo-parietal
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approach were the most common surgical routes used in our series. These two approaches permit a direct access to the lateral ventricle, preserving the optic radiation and the speech area.
The temporo-parietal approach is
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preferred for removing trigonal tumors located mainly at the trigone and the
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posterior part of the temporal horn in the non-dominant hemisphere, while the posterior parietal approach is used for tumor growing at the trigone and the body of the lateral ventricle. Our experience is confirmed by Ma et al67: the same two approaches were considered, however in this study, the intraoperative ultrasound guidance allowed the authors to select the eventual site of cortisectomy according to the shorter distance to the tumor and/or ventricle access zone, thus avoiding the
ACCEPTED MANUSCRIPT important eloquent areas. We did not have the intraoperative image guidance (neuronavigation) nor ultrasound available for our patients, which may be useful in achieving safe tumor removal and reducing approach morbidity.
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Our trajectory was entirely based upon a preoperative anatomical and neuroradiological assessment. It is advisable to plan the cortical incision before surgery in order to obtain the occlusion of the choroidal artery
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branches as early as possible, and perform the internal piecemeal decompression of the tumor by ultrasonic aspirator to minimize brain
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retraction. Special care should be paid to the respect of choroidal vessels: the use of visual evoked potential monitoring as suggested by Kamada et al106 allows a total removal of such tumors and good clinical outcomes. Finally, we would remind that the use of intraoperative monitoring and
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image guidance system, like navigation and ultrasonography, gives advantages in terms of safety and effectiveness of the surgical approach to these tumors, especially when performing a transtemporal approach67.
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However, most patients were operated on, before the availability of these
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intra-operative referring imaging systems; recently, they have been acquired in the surgical armamentarium at the Clinic Center for Neurosurgery of Belgrade, but the planning, also for later cases of the series was focused on detailed study of anatomy as observed at preoperative MRI. Drs. Fusco and Spetzler101 underlined the possible neurological complications, including visual field deficits, apraxias and elements of Gerstmann syndrome after posterior parietal approach to the intraventricular meningiomas. Even if we
ACCEPTED MANUSCRIPT did not experience such complications, these need to be always considered as possible consequences of this approach. We think that the preoperative accurate surgical planning based on neuroradiological detailed study is
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fundamental; furthermore, the delicate opening of the intraparietal sulcus and the dissection of the parietal white matter toward the ventricle permit the direct access to the tumor, with limited intraoperative complications,
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resulting in minimal post-operative neurological sequelae. Surgical outcome
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Mortality rates in the majority of the series ranged from 0 to 42%, however they are around 25%, as reported by Fornari et al3 in 1981. During the last years, the operative mortality has decreased and in the recent series most of the patients improved during the follow-up periods (Table 6). In our series
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the operative mortality was 0%, none of the patients died after microsurgical procedures while perioperative mortality was 2.4%, as related to complication
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of surgery. In our group, no intraventricular drain was left, even though twelve patients showed hydrocephalus at admission. We used an external
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lumbar drain during surgery to reduce significantly the intracranial pressure while initially debulking the tumor. Only one patient showed postoperative hydrocephalus, they were treated with temporary ventricular external drainage. The patient with partial resection recurred during the follow-up periods; subtotal resection is the main cause of recurrence.
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CONCLUSIONS IVMs usually grow slowly to a significant size before becoming symptomatic. The optimal treatment of these lesions is complete surgical resection, after
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which most patients have complete resolution of their symptoms and signs. The operative route should be carefully chosen according to tumor location.
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Ideally, surgery should be aided by several instruments to improve its safety and effectiveness, i.e. the ultrasonic aspirator, neuronavigation, evoked
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potential monitoring and above all else, the knowledge of the local anatomy. The posterior-parietal transulcal approach and the temporo-parietal approach are the most common surgical routes used in our series. The first one is used for larger tumors growing above the temporal horn, while the second is
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preferred for removing trigonal tumors located below the temporal horn, in
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the non-dominant hemisphere.
ACCEPTED MANUSCRIPT LEGENDS FOR FIGURES Figure 1 Preoperative axial (a) and coronal (b) MRI scans showing a case of a left lateral ventriculum meningioma; postoperative axial (c) and coronal (d) MRI
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scans demonstrating the total removal of the lesion by posterior parietal transcortical approach.
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Figure 2
Preoperative axial (a), coronal (b) and sagittal (c) MRI scans showing a case of
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a right lateral ventriculum meningioma; postoperative axial (d), coronal (e) and sagittal (f) MRI scans demonstrating the total removal of the lesion by temporo-parietal transcortical approach. Figure 3
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Preoperative axial (a) MRI scans showing a right lateral ventriculum meningioma; postoperative CT (b) scans demonstrating the total removal of
Figure 4
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the lesion by temporal transcortical approach.
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Preoperative axial (a) MRI scans showing third ventriculum meningioma; postoperative CT (b) scans demonstrating the total removal of the lesion achieved by mean of transcallosal approach.
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4.
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5.
9.
10.
11. 12.
AC C
13.
EP
7. 8.
TE D
M AN U
6.
14.
15.
16.
17.
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23.
24.
25. 26.
27.
28. 29.
AC C
30.
RI PT
22.
SC
21.
M AN U
20.
TE D
19.
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37.
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36.
47.
48.
49. 50.
51.
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57.
58.
59.
60.
61. 62. 63. 64.
65.
AC C
66.
RI PT
56.
SC
55.
M AN U
54.
TE D
53.
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52.
67.
68.
69.
70.
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76. 77.
78.
79.
80.
81.
82. 83.
AC C
84.
RI PT
75.
SC
74.
M AN U
73.
TE D
72.
Imielinski BL, Kopczynski SM. Meningioma within the lateral ventricle. Neurochirurgia (Stuttg). 1970;13(4):124-130. Kobayashi S, Okazaki H, MacCarty CS. Intraventricular meningiomas. Mayo Clin Proc. 1971;46(11):735-741. Markwalder TM, Seiler RW, Markwalder RV, Huber P, Markwalder HM. Meningioma of the anterior part of the third ventricle in a child. Surgical neurology. 1979;12(1):29-32. Pau A, Dorcaratto A, Pisani R. Third ventricular meningiomas of infancy. A case report. Pathologica. 1996;88(3):204-206. Wall AE. Meningiomas within the lateral ventricle. J Neurol Neurosurg Psychiatry. 1954;17(2):91-103. Liu M, Wei Y, Liu Y, Zhu S, Li X. Intraventricular meninigiomas: a report of 25 cases. Neurosurgical review. 2006;29(1):36-40. Wang X, Cai BW, You C, He M. Microsurgical management of lateral ventricular meningiomas: a report of 51 cases. Minim Invasive Neurosurg. 2007;50(6):346-349. Odegaard KM, Helseth E, Meling TR. Intraventricular meningiomas: a consecutive series of 22 patients and literature review. Neurosurgical review. 2013;36(1):57-64; discussion 64. Claus EB, Bondy ML, Schildkraut JM, Wiemels JL, Wrensch M, Black PM. Epidemiology of intracranial meningioma. Neurosurgery. 2005;57(6):1088-1095; discussion 1088-1095. Kendall B, Reider-Grosswasser I, Valentine A. Diagnosis of masses presenting within the ventricles on computed tomography. Neuroradiology. 1983;25(1):11-22. Markwalder TM, Markwalder RV, Markwalder HM. Meningioma of the anterior part of the third ventricle. Case report. Journal of neurosurgery. 1979;50(2):233-235. Gassel MM, Davies H. Meningiomas in the lateral ventricles. Brain. 1961;84:605-627. Winkler PAB, R., Tonn, J.C. Intraventricular meningiomas. In: Lee JH, ed. Meningiomas: diagnosis, treatment and outcome. London: Springer; 2009:491-514. Mani RL, Hedgcock MW, Mass SI, Gilmor RL, Enzmann DR, Eisenberg RL. Radiographic diagnosis of meningioma of the lateral ventricle. Review of 22 cases. Journal of neurosurgery. 1978;49(2):249-255. Smith VR, Stein PS, MacCarty CS. Subarachnoid hemorrhage due to lateral ventricular meningiomas. Surgical neurology. 1975;4(2):241-243. Ameli NO. A practical method of vertebral angiography. Br J Surg. 1952;39(156):327-330. Huang YS, Araki C. Angiographic confirmation of lateral ventricle meningiomas; a report of five cases. Journal of neurosurgery. 1954;11(4):337-352. Majos C, Cucurella G, Aguilera C, Coll S, Pons LC. Intraventricular meningiomas: MR imaging and MR spectroscopic findings in two cases. AJNR American journal of neuroradiology. 1999;20(5):882-885. Perry RD, Parker GD, Hallinan JM. CT and MR imaging of fourth ventricular meningiomas. J Comput Assist Tomogr. 1990;14(2):276-280.
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71.
85. 86. 87.
88.
89.
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95. 96.
97.
98. 99. 100. 101. 102.
AC C
103.
RI PT
94.
SC
93.
M AN U
92.
TE D
91.
Basser PJ, Pajevic S, Pierpaoli C, Duda J, Aldroubi A. In vivo fiber tractography using DT-MRI data. Magn Reson Med. 2000;44(4):625-632. Nimsky C, Ganslandt O, Hastreiter P, et al. Preoperative and intraoperative diffusion tensor imaging-based fiber tracking in glioma surgery. Neurosurgery. 2005;56(1):130-137; discussion 138. Sun GC, Chen XL, Yu XG, et al. Functional Neuronavigation-Guided Transparieto-Occipital Cortical Resection of Meningiomas in Trigone of Lateral Ventricle. World Neurosurg. 2015;84(3):756-765. Kleiser R, Staempfli P, Valavanis A, Boesiger P, Kollias S. Impact of fMRIguided advanced DTI fiber tracking techniques on their clinical applications in patients with brain tumors. Neuroradiology. 2010;52(1):37-46. Parraga RG, Ribas GC, Welling LC, Alves RV, de Oliveira E. Microsurgical anatomy of the optic radiation and related fibers in 3-dimensional images. Neurosurgery. 2012;71(1 Suppl Operative):160-171; discussion 171-162. Ebeling U, Reulen HJ. Neurosurgical topography of the optic radiation in the temporal lobe. Acta neurochirurgica. 1988;92(1-4):29-36. Louis DN, Budka H, Von Deimling A. Meningiomas. In: Kleihues P, Cavenee WK, eds. Tumours of the nervous system. International Agency for Research on Cancer. Lyon 1997:134-141. Delatorre E, Alexander E, Jr., Davis CH, Jr., Crandell DL. Tumors of the Lateral Ventricles of the Brain. Report of Eight Cases, with Suggestions for Clinical Management. Journal of neurosurgery. 1963;20:461-470. Jun CL, Nutik SL. Surgical approaches to intraventricular meningiomas of the trigone. Neurosurgery. 1985;16(3):416-420. Kempe LG, Blaylock R. Lateral-trigonal intraventricular tumors. A new operative approach. Acta neurochirurgica. 1976;35(4):233-242. Piepmeier JM, Spencer DD, Sass KJ. Lateral ventricle masses. In: Apuzzo MLJ, ed. Brain surgery. New York: Churchill Livingstone; 1993:581-599. Fusco DJ, Spetzler RF. Surgical considerations for intraventricular meningiomas. World Neurosurg. 2015;83(4):460-461. Guidetti B, Delfini R. Lateral and fourth ventricle meningiomas. In: AlMefty O, ed. Meningiomas. New York: Raven Press; 1991:569-582. Guthrie BL, Ebersold MJ, Scheithauer BW. Neoplasm of the intracranial meninges. In: Youmans JR, ed. Neurological surgery: a comprehensive reference guide to the diagnosis and management of neurosurgical problems. Philadelphia: Saunders; 1999:3250-3315. Konovalov AN, Filatov YM, Belousova OB. Intraventricular meningiomas. In: Schmidek HH, ed. Meningiomas and their surgical management. Philadelphia: Saunders; 1991:364-374. Morita A, Kelly PJ. Resection of intraventricular tumors via a computerassisted volumetric stereotactic approach. Neurosurgery. 1993;32(6):920926; discussion 926-927. Kamada K, Todo T, Morita A, et al. Functional monitoring for visual pathway using real-time visual evoked potentials and optic-radiation tractography. Neurosurgery. 2005;57(1 Suppl):121-127; discussion 121127.
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105.
106.
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signs and symptoms
total (%)
42
visual field defect psychoorganic syndrome papillary stasis
seizures motor deficit
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gait instability
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signs of increased intracranial pressure
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n. of patients
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visual impairment
35 (83.3%) 31 (73.8%) 21 (50%) 14 (33.3%) 11 (26.2%) 8 (19%) 6 (14.3%) 5 (11.9%)
Table 1. Presenting symptoms and neurological signs in 42 patients with intraventricular meningioma
posterior-parietal (%) 11 (47.8%)
body of the lateral ventricle temporal horn of the lateral ventricle trigone and body of the lateral ventricle
third ventricle
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third ventricle and body of the lateral ventricle
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trigone and occipital horn of the lateral ventricle
transcallosal (%)
2 (8.7%)
0 (0%)
1 (33.3%)
0 (0%)
0 (0%)
2 (66.7%)
0 (0%)
0 (0%)
2 (100%)
0 (0%)
6 (85.7%)
1 (14.3%)
0 (0%)
0 (0%)
0 (0%)
0 (0%)
3 (100%)
0 (0%)
1 (50%)
1 (50%)
0 (0%)
0 (0%)
0 (0%)
0 (0%)
0 (0%)
1 (100%)
1 (100%)
0 (0%)
0 (0%)
0 (0%)
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trigone and temporal horn of the lateral ventricle
temporal (%)
10 (43.5%)
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trigone of the lateral ventricle
temporo-parietal (%)
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tumor location
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Table 2. Surgical approaches in relation to the location of intraventricular meningiomas
lateral ventricle (%) 2 (5%)
fibrous (fibroblastic) transitional (mixed) psammomatous
atypical
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anaplastic (malignant)
2 (4.8%)
7 (17.5%)
1 (50%)
8 (19%)
29 (72.5%)
1 (50%)
30 (71.4%)
0 (0%)
0 (0%)
0 (0%)
1 (2.5%)
0 (0%)
1 (2.4%)
1 (2.5%)
0 (0%)
1 (2.4%)
0 (0%)
0 (0%)
0 (0%)
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angiomatous
total (%)
0 (0%)
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meningothelial
third ventricle (%)
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type
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Table 3. Histological features of intraventricular meningiomas
1. Death
GOS at discharge
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Glasgow Outcome Scale (GOS)
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GOS at 6 months
1 (2.4%)
1 (2.4%)
1 (2.4%)
0 (0%)
3. Severe disability (conscious but disabled)
12 (28.6%)
1 (2.4%)
4. Moderate disability (disabled but indipendent)
15 (35.7%)
5 (11.9%)
5. Recovery
13 (30.9%)
35 (83.3%)
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2. Persistent vegetative state
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Table 4. Glasgow Outcome Scale at discharge and at 6 months after surgery
at admission
visual field defect
31
24 (77.4%)
Improved/resolved worsening
unchanged
Improved/resolved
atrophy
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worsening
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unchanged
at 6 months
2 (6.5%)
7 (22.6%)
29 (93.5%)
0 (0%)
0 (0%)
0 (0%)
0 (0%)
14 (100%)
14 (100%)
0 (0%)
0 (0%)
4 (100%)
4 (100%)
14
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papillary stasis
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unchanged
at discharge
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visual function
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Table 5. Visual outcome at the discharge and 6 months after the operations.
Author and year year
study design
study period
n° sex of (F/M) pts
Bertalanffy et al.
2006 retro
1980-2004
Liu et al.
2006 retro
Wang et al.
1:1
side (L/R)
total removal %
recurrence
case mortality
25-77 (47)
N/A
L 81.3%, III 6.3%, IV 12.5%
2.3:1
93.7%
1
0
16
2.2:1 24-84 (N/A)
1.5%
L 93.7.%, III 0%, IV 6.2%
0.9:1
87.5%
N/A
1
1989-2003
25
2.1:1
15-63 (39)
3.7%
L 96%, III 0%, IV 4%
2.4:1
88%
2
0
2007 retro
1996-2006
51
1.6:1
14-75 (44)
Menon et al.
2009 retro
1998-2008
15
2:1
14-75 (41)
Odegaard et al.
2012 retro
1990-2010
22
2.7:1
26-81 (52)
Ma et al.
2014 retro
2007-2012
43
2.6:1
current study
2015 retro
1990-2013
42
2.5:1
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16
location
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1978-2001
incidence
N/A
N/A
N/A
94.1%
0
1
1.3%
L 100%, III 0%, IV 0%
1.1:1
86.7%
2
1
1.5%
L 91%, III 4.5%, IV 4.5%
0.7:1
95.5%
1
0
14-61 (43)
N/A
L 100%
0.6:1
100%
0
0
1-67 (44)
N/A
L 95.2%, III 4.8%, IV 0%
2.1:1
92.8%
1
0
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2003 retro
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Nakamura et al.
age range (mean)
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Table 6. Key findings of published surgical series involving fifteen or more patients with IVMs since 2003.
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SC
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SC
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ACCEPTED MANUSCRIPT Highlights
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IVMs are rare and sizable, highly vascular and deep located within the brain Total removal of IVMs represent the main goal of the treatment IVMs represent one of the most challenging lesions in neurosurgery The posterior-parietal approach is the most safe surgical routes
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• • • •
S1878-8750(16)30898-1
DOI:
10.1016/j.wneu.2016.09.068
Reference:
WNEU 4608
To appear in:
World Neurosurgery
Received Date: 1 June 2016 Revised Date:
14 September 2016
Accepted Date: 16 September 2016
Please cite this article as: Grujicic D, Cavallo LM, Somma T, Illic R, Milicevic M, Raicevic S, Gazibara MS, Villa A, Savic D, Solari D, Cappabianca P, Intraventricular Meningiomas: A Series Of 42 Patients at a Single Institution and Literature Review, World Neurosurgery (2016), doi: 10.1016/j.wneu.2016.09.068. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT INTRAVENTRICULAR MENINGIOMAS: A SERIES OF 42 PATIENTS AT A SINGLE INSTITUTION AND LITERATURE REVIEW.
1Clinical
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Danica Grujicic, MD1, Luigi Maria Cavallo, MD, PhD2, Teresa Somma, MD2, Rosanda Illic, MD3, Mihailo Milicevic, MD1, Savo Raicevic, MD4, Milica Skender Gazibara, MD5, Alessandro Villa, MD2, Dragan Savic, MD1, Domenico Solari, MD, PhD2, Paolo Cappabianca, MD2
Center of Serbia, Clinic of Neurosurgery, Medical Faculty University of
2Department
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Belgrade, Belgrade, Serbia
of Neurosciences and Reproductive and Odontostomatological Sciences,
3
Clinical Center of Serbia, Clinic of Neurosurgery, Belgrade, Serbia
4 Clinical 5
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Division of Neurosurgery, Università degli Studi di Napoli Federico II, Naples, Italy
Center of Serbia, Department of Pathological Anatomy, Belgrade, Serbia
Clinical Center of Serbia, Department of Pathological Anatomy, Medical Faculty
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University of Belgrade, Belgrade, Serbia
Corresponding Author:
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Teresa Somma
Department of Neurosciences and Reproductive and Odontostomatological
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Sciences
Division of Neurosurgery Università degli Studi di Napoli Federico II Via Pansini 5
80131 Naples, Italy
Tel +39 081 7462490 Fax +39 081 7462594 e-mail: [email protected]
ACCEPTED MANUSCRIPT KEYWORDS: meningioma, intraventricular, lateral ventricle, third ventricle, surgical complications, surgical mortality, survival.
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ABBREVIATIONS:
CSF: cerebrospinal fluid; CT: computed tomography; GCS: Glasgow coma
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scale; GOS: Glasgow outcome scale; IVM: intraventricular meningioma; MRI:
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magnetic resonance imaging.
ACCEPTED MANUSCRIPT ABSTRACT Background: Primary intraventricular meningiomas (IVMs) make up 0.5-5% of all intracranial meningiomas and represent one of the most challenging
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lesions in neurosurgery. Methods: Between 1990 and 2013, 42 patients (30 female, 12 male, mean age of 43.6 years) underwent the resection of their IVM. The removal was
SC
performed by posterior-parietal approach in 19 of the 40 lateral ventricle tumors, and one in the third ventricle meningioma. The transcallosal
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approach was used for three meningiomas, while other lesions underwent temporal (7 cases) and temporo-parietal approaches (12 pts) respectively. Results: The most common presenting signs were increased intracranial pressure (83.3%), visual impairment (78.6%) and cognitive changes (50%).
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Concerning tumor location, forty lesions (95.2%) were arising in the lateral ventricles, and two (4.8%) in the third ventricle, ranging in sizes from 3 to 10 cm. Total removal was achieved in 39 cases and the pathology report
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disclosed WHO grade I lesions in 41 cases. Hydrocephalus, CSF leakage and
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cerebral edema were the postoperative complications (7.15%); one patient died of respiratory problems not directly related to surgery. Thirty-five patients (83.3%) showed a six-months Glasgow outcome scale (GOS) of 5. One patient, that underwent partial resection, presented a recurrence after 1 year that remained stable until last follow-up. Conclusions: IVMs usually reach a large size before being diagnosed. The surgical treatment is the most suitable option and total removal should
ACCEPTED MANUSCRIPT represent the main goal of the procedure. The posterior-parietal transulcal approach and the temporo-parietal approach are the most common surgical
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routes used in our series.
ACCEPTED MANUSCRIPT INTRODUCTION Intraventricular meningiomas (IVMs) are extremely rare tumors, accounting for 0.5-5% of all intracranial meningiomas1-9, 9.8-14% of all intraventricular
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tumors and 20% of lateral ventricle tumors10,11. According to the literature, their distribution is 77.8% in the lateral ventricle, 15.6% in the third ventricle and 6.6% in the fourth ventricle4-6,8,9,12-61. They arise either from the stroma of
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the choroid plexus or from the tela choroidea and do not present any dural attachments. Intraventricular meningiomas often grow slowly and may reach
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large volumes before becoming symptomatic. Surgical removal of these lesions remains challenging in modern day neurosurgery because of the close relationships with vital structures, particularly the optic radiations, which if
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injured can lead to serious postoperative visual complications19,62-64. There are few large surgical series with long follow-up. We, therefore, report our experience on a series of 42 patients who underwent surgical removal of a
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purely intraventricular meningioma over a 23-year period, presenting in detail the clinical and neuroradiological findings, surgical results and
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management of peri- and post-operative complications.
MATERIAL AND METHODS We retrospectively reviewed data of patients diagnosed with IVMs, who were surgically treated at the Clinic of Neurosurgery at the Clinical Center of
ACCEPTED MANUSCRIPT Serbia, between 1990 and 2013. All the operations were performed using microsurgical technique. The series included 42 patients, 30 female and 12 male with a sex ratio
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(female/male) of 2.5. The median age at surgery was 55 years (range: 1–67; mean: 43.6).
All patients were symptomatic and the duration of initial symptoms prior to
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definitive diagnosis lasted from 1 week up to 5 years (median 12.1 months).
Preoperative imaging was computed tomography (CT) in 24 patients,
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magnetic resonance imaging (MRI) in 3 patients and 15 patients had both CT & MRI.
Tumor recurrence was defined by the presence of new pathological tissue on repeated MRI (not noticed at an earlier control) and regrowth of residual by
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further growth of tissue already detected on the previous post-operative
RESULTS
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MRIs.
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Preoperative symptoms
Thirty-eight patients (90.5%; 38/42) had a preoperative Glasgow Coma Scale (GCS) ≥ 13. The most common clinical presentation was increased intracranial pressure (83.3%) while the more frequent neurological sign was homonymous hemianopia (42.8%). (Table 1 summarizes the neurological status of the patients upon admission). Tumor features Concerning the location, fifteen tumors were located in the right lateral
ACCEPTED MANUSCRIPT ventricle and 25 were in the left lateral ventricle; thirty-five of them (83.3%) arose in the trigone. Three lesions (7.1%) were purely in the body of lateral ventricle and 2 (4.8%) in the temporal horn. One tumor was found purely into
lateral ventricle. Tumor sizes ranged from
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the third ventricle and one near the foramen of Monro with extension into the
1 to 10 cm with four tumors being (9.5%) < 3 cm, eleven (26.2%) between 3
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and 5 cm, seventeen (40.5%) between 5 and 7 cm and ten meningiomas (23.8%) were bigger than 7 cm in diameter. An extraventricular extension was
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observed in only three cases (7.1%), while hydrocephalus was presented in 12 patients (28.6%). Surgical outcomes
An external lumbar cerebrospinal fluid (CSF) drain was left during surgery to
procedure. Out of the
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reduce the intracranial pressure and removed at the end of the surgical
39 lateral ventricular meningiomas, 20 were resected via a
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posterior parietal transcortical approach (see figure 1), 12 via temporo-
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parietal (see figure 2) and 7 via temporal transcortical approach (see figure 3); two meningiomas arising from the body of the right lateral ventricular were resected via a transcallosal approach (see figure 4). (Table 2 summarizes the surgical approaches in relation to the location of the lesion). Out of the 42 ventricular meningiomas, total resection was achieved in thirtynine cases (92.8%) and partial resection was performed in only one case; it was a big size tumor (>7 cm) treated by posterior-parietal approach followed
ACCEPTED MANUSCRIPT by radiotherapy in the early 1990s. This patient had relapse of the tumor after twelve months, that remained stable until last follow-up. Finally, a biopsy followed by radiotherapy was performed in two cases: in these patients, the
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development of intraoperative cerebral edema and the occurrence of an intraoperative gastro-intestinal bleeding hindered the surgery. Histology
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The Pathology report revealed that the most of the lateral ventricular meningiomas (72.5%) was transitional type. However, two cases of third
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ventricular meningiomas were diagnosed as transitional and fibroblastic. (Table 3 summarizes the histological features of the tumors). Surgical Complications
Thirty-nine patients (93%) did not have any intraoperative or postoperative
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complications; postoperative CSF leak occurred in one patient and it spontaneously resolved after the placement of a lumbar drain. In the early ‘90s one patient affected by a right ventricular meningioma approached by
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posterior parietal approach, had massive cerebral edema during surgery and
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developed postoperative hydrocephalus. She was successfully treated with anti-edema therapy and temporary external ventricular drainage. Another patient, who was admitted at the hospital with increased ICP and progressive deterioration of consciousness, developed postoperative massive cerebral edema and, after 25 days in the ICU, he died of a pulmonary embolism. Indeed, this is the only case to be considered in the perioperative mortality rate - defined as death within 30 days postoperatively - esteemed as 2.4% (1 of
ACCEPTED MANUSCRIPT 42). Concerning medical complications, we had one case of gastrointestinal bleeding, two patients with myocardial infarction and two cases of
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respiratory problems, one of which is the aforementioned patient with massive pulmonary embolism that caused the patient's death; the remaining 88.1% (37/42) of cases did not have any medical or surgical complications.
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Clinical outcomes
The outcome was measured with the Glasgow outcome scale (GOS)65 at their
followed from 2 to 25 years.
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day of discharge and at 6 months after the operation; the patients were
Forty patients (95.2%) had a good GOS at discharge. Improved six months after surgery.
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The patient that developed massive cerebral edema and postoperative hydrocephalus, showed GOS 2 at discharge and GOS 3 six months after surgery.
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Visual outcome was considered at discharge and six months after surgery. All
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patients were evaluated pre- and post-operatively for visual acuity, and computerized visual field examinations were performed. The hemianopia and other visual field defects presented respectively in 18 and 13 of the patients: it improved/resolved in 6.5% of patients at discharge and in 93.5% of the cases 6 months after surgery. None of the patient presented postoperative visual deterioration. Optic nerve edema resolved in all 14 cases in which they were present, while optic atrophy remained unchanged during the long-term
ACCEPTED MANUSCRIPT follow-up in 4 patients. (Table 4 and 5 summarizes the GOS and visual outcome at the discharge and 6 months after the operations).
DISCUSSION
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IVMs are uncommon and therefore, the number of clinical series in the literature is limited, with most of them reporting relatively few patients. In
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the Cushing’s personal series of 313 meningiomas, only 1% was intraventricular2. The first description of an intraventricular meningioma was
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reported in 1854 by Shaw66, who described a tumor arising at the right trigone. Over time, several case series were published and in 1965 Delandsheer62 reviewed the literature identifying 175 cases of lateral ventricular meningiomas, and, in 1986, Criscuolo and Symon9 identified 400
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cases in the world literature. More recently, other series have been published and in 2003 Nakamura et al19 identified 132 additional cases of IVMs since 1986 and Ma et al67 described the surgical management of 43 meningiomas of
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18,20-60,68-75.
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the trigone area of the lateral ventricle resulting in a total of 575 cases4-6,8,12-
Among them, 457 occurred in the lateral ventricles ( 79,.5 %), 83 in the third ventricle (14.4 %), and 35 in the fourth ventricle (6 %). Tables 6 summarizes the key findings of published surgical series involving fifteen or more patients with IVMs since 20031,19,64,76-78. Incidence Meningiomas arising within the ventricular system are reported to have an
ACCEPTED MANUSCRIPT incidence of 0.5 to 3% of all intracranial meningiomas although this type of brain tumor is the second most frequent. Concerning the gender of patients affected by intracranial meningiomas, female preponderance is well
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documented. Data in the literature shows female predominance for IVMs ranging from 41% up to a maximum of 82%, with an average female-to-male ratio of 2:1. In our series we observed a predominance of women of 71.4%
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with a ratio of women to men of 2.5:1.
Generally, the risk of developing meningioma increases with age79, being that
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intraventricular meningiomas are most common over the third decade. During the last 12 years, the reported mean age of removed IVMs has varied from 39 to 47 years (Table 6). In our series the patients’ age ranged from 1 to 67 years and the mean age was 43.6 years (median 46.5). The mean age varies
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also in relation with the meningiomas’ location: for those of lateral ventricular in the literature it ranges from 20 to 50 years. Concerning third and fourth ventricular meningiomas, mean ages are 28.7 years and 35.7 years,
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respectively. In our series the mean age of lateral ventricular meningiomas
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was 44.6 years. Additionally, patients with third ventricular meningiomas in the present series were 21 and 28 years old at the time of surgery. As summarized by Nakamura19 in 2003, 78% of the IVMs were located in the lateral ventricles (most commonly arising in the trigone5,28,61,76), 16% in the third ventricle (although this is more common in childhood9,80,81), and 7% in the fourth ventricle. In our series of 42 IVMs, 40 tumors (95.2%) were located in the lateral ventricles, two in the third ventricle (4.8%) and none in the
ACCEPTED MANUSCRIPT fourth ventricle. As noted, IVMs are slightly more common on the left3,5,76 and this trend has been confirmed (27/40; 67.5%) in our series (Table 6).
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Clinical and radiological aspects In 1938 Cushing and Eisenhardt described five clinical features of trigonal IVMs:
(1)
symptoms
of
intracranial
hypertension;
(2)
contralateral
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homonymous hemianopia; (3) contralateral sensorimotor deficit; (4) cerebellar affection (>50 %), and (5) dysphasia and/or paralexia in left-sided tumors2.
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On the other hand, in 1961 Gassel and Davis82 affirmed that the lateral ventricles are the most silent sites of the meningiomas and that IVMs often reach such dimensions to be ranked as the largest intracranial tumors. Winkler83 suggested that symptoms and signs of IVMs may be caused both by
parenchyma.
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raised intracranial pressure and direct pressure on surrounding cerebral
Usually, these tumors grow slowly and reach a large size before becoming
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symptomatic, unless the lesion is located in a region where it compromises
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the CSF circulation. Duration of initial symptoms prior to definitive diagnosis of an intraventricular tumor is reported to last from only a few months up to 20 years and the clinical presentation is variable. The most common symptoms reported are headaches, nausea and vomiting, as well as visual field defects, speech disturbances, sensomotor deficits and seizures3,4,9,84. Other frequently reported clinical features include mental disturbances and gait instability; furthermore, Smith described a case of subarachnoid
ACCEPTED MANUSCRIPT hemorrhage due to lateral ventricle meningiomas with a clinical presentation indistinguishable from aneurysmal subarachnoid hemorrhage83,85. In our series, the IVMs reached very large sizes and the duration of symptoms
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varied widely from 1 week to 5 years. Thirty-eight of the patients had a preoperative GCS ≥ 13 and the most common clinical presentation were signs related to increased intracranial pressure followed by visual disturbances,
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cognitive changes, seizures and motor deficits. Visual field defects were the most common signs on neurological examination, followed by gait instability
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(Table 1). In particular, we observed that four patients with optic atrophy had a GCS ≤ 13 (respectively GCS 7, 8, 10, and 13); this is in line with longtime damage in the brain due to the presence of the tumor.
In the past, neuroradiological diagnosis of IVMs were based on
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ventriculography and pneumoencephalography. Gradually angiography became the investigation of choice as demonstrated by data retrieved from the literature75,86,87. Today CT and MRI are the safest and most accurate
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modality for diagnosing IVMs, the last one providing the most complete
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information to plan the surgical resection. At the early stage of this series 24 patients of our series underwent only CT, due to the high cost of MRI in our region. The appearance on imaging studies is similar to that of other meningiomas, being sharply defined and round, without the typical dural attachment3,80,84; they show increased density on CT scan. On MRI, IVMs usually are hypo- to isointense on T1-weighted images and iso- to hyperintense on T2-weighted images88,89. Calcifications are reported to appear
ACCEPTED MANUSCRIPT in 47% of all cases; and peritumoral edema can be present4,10. The main differential diagnosis, according to these features should take into account choroids plexus carcinoma/papilloma, ependymoma, glioma or central
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neurocytoma10,88. Hydrocephalus produced by lateral intraventricular meningiomas is usually localized at the ipsilateral trigone and temporal horn80.
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Concerning the use of DTI, it has to be said that has been recently introduced in the clinical practice and it has been reported that it gives invaluable help in
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retrieving information in regards to relationships between fiber bundles and lesions, especially in cases of intracerebral lesions90-93. Although the use of functional exams in the surgical planning of IVM is not widely described67, the functional MRI and DTI fiber tracking certainly will assume a relevant
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role in the management of these lesions. We did not have the opportunity to perform DTI in our patients, and yet, the rate of our complications was quite the same as compared to other series reported in the literature57. Therefore,
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both the approaches, adopted in our series, permited to access to tumors
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growing inside the ventricular cavity through a small corticectomy in a non eloquent area and without transgressing the optic radiation, which runs with an infero-lateral trajectory in regards to the ventricles94,95. In our opinion good knowledge of cortical and white matter anatomy is mandatory to perform a safe approach. Finally, it should be considered that intraventricular meningeomas have a very rare pathology and keeping in mind that the use of any pre and intra-
ACCEPTED MANUSCRIPT operative image guidance assistance may reduce the risk of complications related to the small case load of this disease.
Neuropathology
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Meningiomas are of great interest because they are featured with a variety of histological characteristics96. In the pertinent literature about intraventricular
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meningiomas, there is few data on the histological subtype1,3,4,9,19. The more frequent lesion figured out to be the meningothelial and fibroblastic types. In
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our series the majority of meningiomas were of the transitional type (71.4%) and only one was atypical (Table 3). Surgical treatment
The removal of the IVMs represents a neurosurgical challenge, because of the
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deep location, the proximity of motor, sensory, and language cortex, as well as the optic radiation and the vascular structures. Different surgical approaches were described for resection of these tumors:
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temporoparietal approach, transfrontal approach, posterior middle temporal
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gyrus approach, posterior inferior temporal gyrus approach, parieto-occipital approach and, transcallosal approach2,3,97-100. The aim of all surgical approaches is to minimize the risk of postoperative deficits by using small corticotomies, minimal retraction of surrounding functional brain tissue, early access and interruption of the tumor’s blood supply and piecemeal resection1. Furthermore, as reported by Fusco and Spetzler101, the choice of the surgical approach is defined by best access to the long axis of the lesion, minimization
ACCEPTED MANUSCRIPT of transcortical transgression, spectrum of the patient’s preoperative neurological deficit, and proximity to eloquent anatomic structures and pathways.
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Nowadays, the posterior parietal, the middle temporal gyrus and the transcallosal approach are the most frequently used routes61. The posterior parietal approach permits a good exposure of the tumor but restricted access
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to the tumor’s vessels. Above all, it can be adopted via both the dominant and non-dominant hemisphere, with a low risk of direct damage to the optic
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radiation; in fact, as shown by anatomic studies, the optic radiation runs inferolaterally to the ventricles, and the ventricular trigone can be reached through a posterior parietal route without interrupting it94,95. The middle temporal gyrus approach allows the early occlusion of the tumor feeding, i.e.
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the anterior and posterior choroidal artery branches, but it is burdened by an increased risk of damaging the inferior portion of the optic radiation; adversely, when it is performed through the dominant hemisphere it could
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result in language deficits. Finally, the transcallosal approach minimizes the
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risk of postoperative seizures as well as speech and visual disturbances, but it has
the
disadvantage
of
a
possible
visual–verbal
disconnection
syndrome3,8,9,98,99,102-105. In a case report, Couillard et al26 described the advantage of a combined temporal and parietal approach, resulting in a total tumor resection and excellent clinical outcome Fornari et al. suggested a more superiorly located cortisectomy, consisting in
ACCEPTED MANUSCRIPT a sagittal paramedian incision of the parietal cortex at a distance of 4 cm from the midline, that starts 1 cm behind the post-central fissure and is continued for 4–5 cm as far as the parieto-occipital fissure. This approach may be less
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harmful at least with respect to visual function3. In our series, of the 38 lateral ventricular meningiomas, 19 were resected via a posterior parietal transulcal approach, 12 via temporo-parietal and 7 via
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temporal approach, while two meningiomas of body of the right lateral ventricular were resected via a transcallosal approach. The third ventricular
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meningioma with extension into the lateral ventricle was treated by posterior parietal approach, while the transcallosal approach was used for the purely third ventricular meningioma. The posterior-parietal transulcal approach, between the superior and inferior parietal lobe, and the temporo-parietal
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approach were the most common surgical routes used in our series. These two approaches permit a direct access to the lateral ventricle, preserving the optic radiation and the speech area.
The temporo-parietal approach is
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preferred for removing trigonal tumors located mainly at the trigone and the
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posterior part of the temporal horn in the non-dominant hemisphere, while the posterior parietal approach is used for tumor growing at the trigone and the body of the lateral ventricle. Our experience is confirmed by Ma et al67: the same two approaches were considered, however in this study, the intraoperative ultrasound guidance allowed the authors to select the eventual site of cortisectomy according to the shorter distance to the tumor and/or ventricle access zone, thus avoiding the
ACCEPTED MANUSCRIPT important eloquent areas. We did not have the intraoperative image guidance (neuronavigation) nor ultrasound available for our patients, which may be useful in achieving safe tumor removal and reducing approach morbidity.
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Our trajectory was entirely based upon a preoperative anatomical and neuroradiological assessment. It is advisable to plan the cortical incision before surgery in order to obtain the occlusion of the choroidal artery
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branches as early as possible, and perform the internal piecemeal decompression of the tumor by ultrasonic aspirator to minimize brain
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retraction. Special care should be paid to the respect of choroidal vessels: the use of visual evoked potential monitoring as suggested by Kamada et al106 allows a total removal of such tumors and good clinical outcomes. Finally, we would remind that the use of intraoperative monitoring and
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image guidance system, like navigation and ultrasonography, gives advantages in terms of safety and effectiveness of the surgical approach to these tumors, especially when performing a transtemporal approach67.
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However, most patients were operated on, before the availability of these
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intra-operative referring imaging systems; recently, they have been acquired in the surgical armamentarium at the Clinic Center for Neurosurgery of Belgrade, but the planning, also for later cases of the series was focused on detailed study of anatomy as observed at preoperative MRI. Drs. Fusco and Spetzler101 underlined the possible neurological complications, including visual field deficits, apraxias and elements of Gerstmann syndrome after posterior parietal approach to the intraventricular meningiomas. Even if we
ACCEPTED MANUSCRIPT did not experience such complications, these need to be always considered as possible consequences of this approach. We think that the preoperative accurate surgical planning based on neuroradiological detailed study is
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fundamental; furthermore, the delicate opening of the intraparietal sulcus and the dissection of the parietal white matter toward the ventricle permit the direct access to the tumor, with limited intraoperative complications,
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resulting in minimal post-operative neurological sequelae. Surgical outcome
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Mortality rates in the majority of the series ranged from 0 to 42%, however they are around 25%, as reported by Fornari et al3 in 1981. During the last years, the operative mortality has decreased and in the recent series most of the patients improved during the follow-up periods (Table 6). In our series
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the operative mortality was 0%, none of the patients died after microsurgical procedures while perioperative mortality was 2.4%, as related to complication
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of surgery. In our group, no intraventricular drain was left, even though twelve patients showed hydrocephalus at admission. We used an external
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lumbar drain during surgery to reduce significantly the intracranial pressure while initially debulking the tumor. Only one patient showed postoperative hydrocephalus, they were treated with temporary ventricular external drainage. The patient with partial resection recurred during the follow-up periods; subtotal resection is the main cause of recurrence.
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CONCLUSIONS IVMs usually grow slowly to a significant size before becoming symptomatic. The optimal treatment of these lesions is complete surgical resection, after
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which most patients have complete resolution of their symptoms and signs. The operative route should be carefully chosen according to tumor location.
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Ideally, surgery should be aided by several instruments to improve its safety and effectiveness, i.e. the ultrasonic aspirator, neuronavigation, evoked
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potential monitoring and above all else, the knowledge of the local anatomy. The posterior-parietal transulcal approach and the temporo-parietal approach are the most common surgical routes used in our series. The first one is used for larger tumors growing above the temporal horn, while the second is
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preferred for removing trigonal tumors located below the temporal horn, in
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the non-dominant hemisphere.
ACCEPTED MANUSCRIPT LEGENDS FOR FIGURES Figure 1 Preoperative axial (a) and coronal (b) MRI scans showing a case of a left lateral ventriculum meningioma; postoperative axial (c) and coronal (d) MRI
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scans demonstrating the total removal of the lesion by posterior parietal transcortical approach.
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Figure 2
Preoperative axial (a), coronal (b) and sagittal (c) MRI scans showing a case of
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a right lateral ventriculum meningioma; postoperative axial (d), coronal (e) and sagittal (f) MRI scans demonstrating the total removal of the lesion by temporo-parietal transcortical approach. Figure 3
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Preoperative axial (a) MRI scans showing a right lateral ventriculum meningioma; postoperative CT (b) scans demonstrating the total removal of
Figure 4
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the lesion by temporal transcortical approach.
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Preoperative axial (a) MRI scans showing third ventriculum meningioma; postoperative CT (b) scans demonstrating the total removal of the lesion achieved by mean of transcallosal approach.
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37.
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36.
47.
48.
49. 50.
51.
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57.
58.
59.
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61. 62. 63. 64.
65.
AC C
66.
RI PT
56.
SC
55.
M AN U
54.
TE D
53.
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EP
52.
67.
68.
69.
70.
ACCEPTED MANUSCRIPT
76. 77.
78.
79.
80.
81.
82. 83.
AC C
84.
RI PT
75.
SC
74.
M AN U
73.
TE D
72.
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EP
71.
85. 86. 87.
88.
89.
ACCEPTED MANUSCRIPT
95. 96.
97.
98. 99. 100. 101. 102.
AC C
103.
RI PT
94.
SC
93.
M AN U
92.
TE D
91.
Basser PJ, Pajevic S, Pierpaoli C, Duda J, Aldroubi A. In vivo fiber tractography using DT-MRI data. Magn Reson Med. 2000;44(4):625-632. Nimsky C, Ganslandt O, Hastreiter P, et al. Preoperative and intraoperative diffusion tensor imaging-based fiber tracking in glioma surgery. Neurosurgery. 2005;56(1):130-137; discussion 138. Sun GC, Chen XL, Yu XG, et al. Functional Neuronavigation-Guided Transparieto-Occipital Cortical Resection of Meningiomas in Trigone of Lateral Ventricle. World Neurosurg. 2015;84(3):756-765. Kleiser R, Staempfli P, Valavanis A, Boesiger P, Kollias S. Impact of fMRIguided advanced DTI fiber tracking techniques on their clinical applications in patients with brain tumors. Neuroradiology. 2010;52(1):37-46. Parraga RG, Ribas GC, Welling LC, Alves RV, de Oliveira E. Microsurgical anatomy of the optic radiation and related fibers in 3-dimensional images. Neurosurgery. 2012;71(1 Suppl Operative):160-171; discussion 171-162. Ebeling U, Reulen HJ. Neurosurgical topography of the optic radiation in the temporal lobe. Acta neurochirurgica. 1988;92(1-4):29-36. Louis DN, Budka H, Von Deimling A. Meningiomas. In: Kleihues P, Cavenee WK, eds. Tumours of the nervous system. International Agency for Research on Cancer. Lyon 1997:134-141. Delatorre E, Alexander E, Jr., Davis CH, Jr., Crandell DL. Tumors of the Lateral Ventricles of the Brain. Report of Eight Cases, with Suggestions for Clinical Management. Journal of neurosurgery. 1963;20:461-470. Jun CL, Nutik SL. Surgical approaches to intraventricular meningiomas of the trigone. Neurosurgery. 1985;16(3):416-420. Kempe LG, Blaylock R. Lateral-trigonal intraventricular tumors. A new operative approach. Acta neurochirurgica. 1976;35(4):233-242. Piepmeier JM, Spencer DD, Sass KJ. Lateral ventricle masses. In: Apuzzo MLJ, ed. Brain surgery. New York: Churchill Livingstone; 1993:581-599. Fusco DJ, Spetzler RF. Surgical considerations for intraventricular meningiomas. World Neurosurg. 2015;83(4):460-461. Guidetti B, Delfini R. Lateral and fourth ventricle meningiomas. In: AlMefty O, ed. Meningiomas. New York: Raven Press; 1991:569-582. Guthrie BL, Ebersold MJ, Scheithauer BW. Neoplasm of the intracranial meninges. In: Youmans JR, ed. Neurological surgery: a comprehensive reference guide to the diagnosis and management of neurosurgical problems. Philadelphia: Saunders; 1999:3250-3315. Konovalov AN, Filatov YM, Belousova OB. Intraventricular meningiomas. In: Schmidek HH, ed. Meningiomas and their surgical management. Philadelphia: Saunders; 1991:364-374. Morita A, Kelly PJ. Resection of intraventricular tumors via a computerassisted volumetric stereotactic approach. Neurosurgery. 1993;32(6):920926; discussion 926-927. Kamada K, Todo T, Morita A, et al. Functional monitoring for visual pathway using real-time visual evoked potentials and optic-radiation tractography. Neurosurgery. 2005;57(1 Suppl):121-127; discussion 121127.
EP
90.
104.
105.
106.
RI PT
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signs and symptoms
total (%)
42
visual field defect psychoorganic syndrome papillary stasis
seizures motor deficit
TE D
gait instability
M AN U
signs of increased intracranial pressure
SC
n. of patients
AC C
EP
visual impairment
35 (83.3%) 31 (73.8%) 21 (50%) 14 (33.3%) 11 (26.2%) 8 (19%) 6 (14.3%) 5 (11.9%)
Table 1. Presenting symptoms and neurological signs in 42 patients with intraventricular meningioma
posterior-parietal (%) 11 (47.8%)
body of the lateral ventricle temporal horn of the lateral ventricle trigone and body of the lateral ventricle
third ventricle
AC C
third ventricle and body of the lateral ventricle
EP
trigone and occipital horn of the lateral ventricle
transcallosal (%)
2 (8.7%)
0 (0%)
1 (33.3%)
0 (0%)
0 (0%)
2 (66.7%)
0 (0%)
0 (0%)
2 (100%)
0 (0%)
6 (85.7%)
1 (14.3%)
0 (0%)
0 (0%)
0 (0%)
0 (0%)
3 (100%)
0 (0%)
1 (50%)
1 (50%)
0 (0%)
0 (0%)
0 (0%)
0 (0%)
0 (0%)
1 (100%)
1 (100%)
0 (0%)
0 (0%)
0 (0%)
TE D
trigone and temporal horn of the lateral ventricle
temporal (%)
10 (43.5%)
M AN U
trigone of the lateral ventricle
temporo-parietal (%)
SC
tumor location
RI PT
ACCEPTED MANUSCRIPT
Table 2. Surgical approaches in relation to the location of intraventricular meningiomas
lateral ventricle (%) 2 (5%)
fibrous (fibroblastic) transitional (mixed) psammomatous
atypical
EP
anaplastic (malignant)
2 (4.8%)
7 (17.5%)
1 (50%)
8 (19%)
29 (72.5%)
1 (50%)
30 (71.4%)
0 (0%)
0 (0%)
0 (0%)
1 (2.5%)
0 (0%)
1 (2.4%)
1 (2.5%)
0 (0%)
1 (2.4%)
0 (0%)
0 (0%)
0 (0%)
TE D
angiomatous
total (%)
0 (0%)
M AN U
meningothelial
third ventricle (%)
SC
type
RI PT
ACCEPTED MANUSCRIPT
AC C
Table 3. Histological features of intraventricular meningiomas
1. Death
GOS at discharge
M AN U
Glasgow Outcome Scale (GOS)
SC
RI PT
ACCEPTED MANUSCRIPT
GOS at 6 months
1 (2.4%)
1 (2.4%)
1 (2.4%)
0 (0%)
3. Severe disability (conscious but disabled)
12 (28.6%)
1 (2.4%)
4. Moderate disability (disabled but indipendent)
15 (35.7%)
5 (11.9%)
5. Recovery
13 (30.9%)
35 (83.3%)
EP
TE D
2. Persistent vegetative state
AC C
Table 4. Glasgow Outcome Scale at discharge and at 6 months after surgery
at admission
visual field defect
31
24 (77.4%)
Improved/resolved worsening
unchanged
Improved/resolved
atrophy
EP
worsening
AC C
unchanged
at 6 months
2 (6.5%)
7 (22.6%)
29 (93.5%)
0 (0%)
0 (0%)
0 (0%)
0 (0%)
14 (100%)
14 (100%)
0 (0%)
0 (0%)
4 (100%)
4 (100%)
14
TE D
papillary stasis
M AN U
unchanged
at discharge
SC
visual function
RI PT
ACCEPTED MANUSCRIPT
4
Table 5. Visual outcome at the discharge and 6 months after the operations.
Author and year year
study design
study period
n° sex of (F/M) pts
Bertalanffy et al.
2006 retro
1980-2004
Liu et al.
2006 retro
Wang et al.
1:1
side (L/R)
total removal %
recurrence
case mortality
25-77 (47)
N/A
L 81.3%, III 6.3%, IV 12.5%
2.3:1
93.7%
1
0
16
2.2:1 24-84 (N/A)
1.5%
L 93.7.%, III 0%, IV 6.2%
0.9:1
87.5%
N/A
1
1989-2003
25
2.1:1
15-63 (39)
3.7%
L 96%, III 0%, IV 4%
2.4:1
88%
2
0
2007 retro
1996-2006
51
1.6:1
14-75 (44)
Menon et al.
2009 retro
1998-2008
15
2:1
14-75 (41)
Odegaard et al.
2012 retro
1990-2010
22
2.7:1
26-81 (52)
Ma et al.
2014 retro
2007-2012
43
2.6:1
current study
2015 retro
1990-2013
42
2.5:1
SC
16
location
M AN U
1978-2001
incidence
N/A
N/A
N/A
94.1%
0
1
1.3%
L 100%, III 0%, IV 0%
1.1:1
86.7%
2
1
1.5%
L 91%, III 4.5%, IV 4.5%
0.7:1
95.5%
1
0
14-61 (43)
N/A
L 100%
0.6:1
100%
0
0
1-67 (44)
N/A
L 95.2%, III 4.8%, IV 0%
2.1:1
92.8%
1
0
TE D
2003 retro
EP
Nakamura et al.
age range (mean)
RI PT
ACCEPTED MANUSCRIPT
AC C
Table 6. Key findings of published surgical series involving fifteen or more patients with IVMs since 2003.
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
ACCEPTED MANUSCRIPT Highlights
EP
TE D
M AN U
SC
RI PT
IVMs are rare and sizable, highly vascular and deep located within the brain Total removal of IVMs represent the main goal of the treatment IVMs represent one of the most challenging lesions in neurosurgery The posterior-parietal approach is the most safe surgical routes
AC C
• • • •