Clinical Neurology and Neurosurgery 113 (2011) 564–569

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Neuroimaging and functional navigation as potential tools to reduce the incidence of surgical complications of lateral ventricular meningiomas Fei Li, Jiangkai Lin, Gang Zhu, Hui Meng, Nan Wu, Rong Hu, Hua Feng ∗ Department of Neurosurgery, Southwest Hospital, The Third Military Medical University, Chongqing 400038, The People’s Republic of China

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Article history: Received 3 February 2010 Received in revised form 7 February 2011 Accepted 28 March 2011 Available online 6 May 2011 Keywords: Lateral ventricle meningioma Surgical complications Neuronavigation Ultrasonography Neuro-endoscopy fMRI Brain mapping

a b s t r a c t Objective: Post-operative complications are common following treatment for meningiomas in the lateral ventricles because it is unavoidable to disrupt the integrity of the brain during surgery. This study discusses our experience with strategies for reducing these complications. Method: Twenty-seven cases of lateral ventricular meningiomas treated surgically were summarized. The surgical corridors of 11 patients were selected according to the traditional anatomical markers. Navigation technologies including neuronavigation, ultrasonography, neuro-endoscopy, fMRI and intraoperative brain mapping were used in the other 16 patients. The post-operative Karnofsky Performance Status (KPS) of patients with or without navigation were compared at 1 week and 3, 6 and 12 months. Results: Except for one patient who died from postoperative intracerebral hemorrhage, most of the preoperative disorders improved after surgery. Although only 4 out of 27 cases suffered from permanent complications of visual field defect or epilepsy, novel postoperative complications were found in 8 of 11 patients without navigation but in only 5 of 16 patients with navigation. The post-operative KPS of patients with navigation were better than those without navigation at 1 week and 3 months after surgery. Conclusion: The use of neuroimaging and functional navigation technologies may effectively lower the incidence of postoperative complications. © 2011 Elsevier B.V. All rights reserved.

1. Introduction The incidence of lateral ventricle meningiomas without dural attachment is approximately 0.5–3.0% [1–5]. Most of these tumors originate from stroma cells of the choroid plexus and are fed by choroid plexus vessels [2,6]. The lateral ventricle is the largest space in the ventricular system, which determines some clinical features and treatments of meningiomas in lateral ventricles [2–7]. It is necessary to cut the brain open when treating meningiomas in lateral ventricles. The operative approach should be chosen according to the location of the tumor, and the surgical complications are related to the operative approach selected [1–4,8].

2008. There were five males and 22 females, aged 14–75 years (mean 35 years). 2.1. Patient characteristics Twenty patients suffered from headache, and 6 patients suffered from vomiting. Eleven patients presented with visual disorders (visual acuity impairment, 7; visual field defect, 4). Four patients showed sensorimotor disorders (hemiparesis and/or hemihypesthesia). Cognitive and personality disorders, such as memory disorder, mental exhaustion and language disorder, were observed in 5 patients. The duration of initial symptoms prior to definite diagnosis ranged from 2 days to 10 years.

2. Materials and methods 2.2. Neuroimaging features We performed a retrospective review of 27 patients suffering from lateral ventricular meningiomas who were treated at the Department of Neurosurgery of the hospital between 2001 and

∗ Corresponding author at: Department of Neurosurgery, Southwest Hospital, the Third Military Medical University, No. 30 Gaotanyan Street, Chongqing 400038, The People’s Republic of China. Tel.: +86 023 68754153; fax: +86 023 65463954. E-mail address: [email protected] (H. Feng). 0303-8467/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.clineuro.2011.03.017

Preoperative CT and/or MRI with contrast enhancement were performed in all patients (Fig. 1). Sixteen tumors were located in the left ventricle; five were in the right ventricle, and six crossed the foramen of Monro (Fig. 1C). Nineteen tumors were located in the trigone, four in the body of the ventricle, two in the occipital horn, and two in the frontal horn. Tumor size ranged from 4.0 to 9.5 cm (mean 6.1 cm). Localized hydrocephalus (Fig. 1A and B) was found in 9 patients, and bilateral hydrocephalus was found in 4

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Fig. 1. MRI images of intraventricular meningiomas. (A and B) Local hydrocephalus caused by intraventricular meningioma. (C) Massive intraventricular meningioma crossed the foramen of Monro. (D) T1-weighted image showed hypointensity of the tumor compared to surrounding brain tissues. (E) T2-weighted image showed hyperintensity of the tumor compared to surrounding brain tissues. (F) Gadolinium-enhanced scans displayed uniform enhancement of the tumor, which had a regular borderline. Arrows indicate the tumors.

patients. CT angiography, MR angiography, and/or Digital Subtraction Angiography were performed in 15 patients. In these patients, all tumors were nourished by both anterior and posterior choroidal circulation. Tumor blush, as well as enlargement and distortion of the draining veins were observed (Fig. 2). Diffusion tensor imaging (DTI) of MRI was used to study the white matter and for surgical planning in 4 patients (Fig. 3). 2.3. Treatment The operative approach was chosen according to the location of the tumor. One meningioma in the frontal horn was resected via a frontal transcortical approach. Two tumors in the occipital horn were resected via an occipital transcortical approach. Eight out of 23 tumors in the trigone or body of the ventricle were resected via the middle/superior temporal gyrus, six via a superior parietooccipital approach, three via a transcallosal approach and six by cortical tailoring, guided by intra-operative brain mapping. The surgical corridors of 11 patients were selected according to the anatomical landmarks found by the doctor during surgery; for example, the middle temporal gyrus was located by finding the superior temporal gyrus and inferior temporal gyrus. Neuronavigation (Medtronic, USA) based on MRI or functional MRI was used in 16 patients. Ultrasonography (ALOKA, Japan) was used to correct the navigation in 8 of these patients when brain shifts were found after the bone flaps were moved (Fig. 4). Functional MRIbased navigation and intra-operative brain mapping were used to tailor the cortical incision in 6 patients with high risk of language effects (Fig. 5). Neuro-endoscopy (Zipplin, German) was used to detect the margin of the tumor during tumor resection and cleaning of the ventricles after tumor resection in 3 patients. After resection of lateral ventricular meningiomas, external ventricular drainage continued for 24–72 h, and intracranial pressure

(ICP, Codman, USA) was measured in the Intensive Care Unit. CT or MRI scans were performed 24 h after surgery. 2.4. Following-up and statistical analyses The follow-up period ranged from 12 months to 96 months (median 38 months). All patients were instructed to undergo follow-up CT or MRI at least 3, 6, or 12 months after surgery. Karnofsky Performance Status (KPS, range 10–100) was used to assess the patient’s status before and after surgery and compared by independent-samples t-test. A P value of ≤0.05 was considered statistically significant. 3. Results 3.1. Pathology The tumors were classified histologically according to the WHO criteria (WHO 2000) as fibrous meningiomas (12/27), meningothelial meningiomas (7/27), transitional (mixed) meningiomas (6/27), angiomatous meningioma (1/27) and atypical meningioma (1/27). 3.2. Overall outcomes Among the 27 patients, total tumor resection was performed in 24 patients (88.9%), and subtotal tumor resection was performed in 3 patients whose tumors had extensive calcifications and adhered to the ventricle wall. One patient died from postoperative intracerebral hemorrhage (Fig. 2D). Postoperative hydrocephalus occurred in 3 patients (Fig. 6). Postoperative neurologic evaluations indicated that signs of intracranial hypertension disappeared; furthermore, cognitive and sensorimotor disorders improved in all of the patients (9/9). Visual disorders were ameliorated in 7 out of the 11 patients.

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Fig. 2. Blood supplies to massive intraventricular meningioma. (A) CT indicated a massive tumor in the left lateral ventricle. (B and C) CTA identified the anterior and posterior cerebral arteries as the blood-supplying vessels for the tumor and revealed that the vessels were tortuous and distorted, with obvious contrast medium retention. (D) The patient developed hemorrhage at 24 h after surgery. Arrows indicate the tumors.

The follow-ups suggest that the overall therapeutic outcomes are excellent (with no neurological deficit) in 21 patients, good (with some neurologic deficit but the patient able to care for him- or herself) in 4 patients, and poor (the patient being unable to care for him- or herself) in 1 patient (Table 1).

3.3. Postoperative complications The recent-onset postoperative neurologic disorders are summarized in Table 1. These included language disorder (apathy and/or mutism) in 5 patients, hemihypesthesia in 2 patients, visual field defect in 4 patients and epilepsy in 2 patients. The preoperative KPS scores of patients with or without navigations were 76.9 ± 10.8 and 77.3 ± 12.7, respectively (P = 0.891, t = −0.139). At one week after surgery, the KPS scores of patients without

navigations were 67.0 ± 18.3 and 81.3 ± 10.3 in patients with navigation (P = 0.004, t = −3.192). At 3 months after surgery, the KPS scores of patients with or without navigations were 90.6 ± 9.3 and 81.0 ± 16.0 (P = 0.037, t = −2.224). At 12 months after surgery, the difference was 94.4 ± 7.3 vs. 90.0 ± 15.6 between patients with or without navigations (P = 0.298, t = −1.265) (Table 2). The outcomes of 6 patients with brain mapping were pretty good, with only one case of temporal language disorder for 3 days.

4. Discussion Although CT or MRI scans can detect lateral ventricular meningiomas easily [1,2,4,5,9,10], the symptoms of intraventricular meningiomas are usually not typical: most patients present with only headache initially, and some others do not have obvious

Table 1 The surgical approaches and complications in 26 lateral ventricular meningioma. Tumor locations

n

Surgical approaches

Frontal horn Trigone or body

1 23

Frontal transcortical approach Middle/superior temporal gyrus (8)

Superior parieto-occipital approach (6)

Occipital horn

2

Transcallosal approach (3) Intra-operative brain mapping (6) Occipital transcortical approach

New-onset symptoms

Permanent morbidity

Language disorders (3) Hemihypaesthesia (1) Epilepsy (1) Visual field defect (2) Hemihypaesthesia (1) Epilepsy (1) Language disorders (1) Language disorders (1) Visual field defect (2)

Epilepsy (1) Hemihypaesthesia (1)

Visual field defect (1)

Visual field defect (2)

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Fig. 3. DTI studies of the intraventricular meningioma showed that conductive fibers of white matter were disrupted and dispersed by the tumor. Arrows indicate disorder and disruption of the conductive fibers. TU, tumor. The dotted line delineates the tumor boundary.

Fig. 4. Ultrasonically assisted tumor resection. (A) MRI indicated a tumor in the body of the right lateral ventricle. (B) The tumor was localized intraoperatively by ultrasonography. (C) MRI 3 months after the operation. The dotted line delineates the tumor boundary. TU, tumor. Table 2 Intra-operation location methods and outcomes of 26 lateral ventricular meningioma. n

Anatomical Markers Navigation P value

11 16

New-onset symptoms (number of cases)

Karnofsky Performance Status (scores)

Language disorders

Visual field defect

Hemihypaesthesia

Epilepsy

Pre-operation

1 week

3 months

12 months

3 2

3 1

1 1

1 1

77.3 ± 12.7 76.9 ± 10.8 0.891

67.0 ± 18.3 81.3 ± 10.3 0.004

81.0 ± 16.0 90.6 ± 9.3 0.037

90.0 ± 15.6 94.4 ± 7.3 0.298

Navigation: Neuronavigation, ultrasonography, neuro-endoscopy, fMRI and introperative brain mapping were included.

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Fig. 5. Intra-operative brain mapping. (A and B) MRI indicated a tumor in the left lateral ventricle. (C) Post-operative CT showed the tumor was resected. (D and E) The boundary of the tumor projection was marked by letters, and the language areas were marked by numbers. (F) The tumor was removed through the cortex incision. Arrow indicates where the tumor was resected.

symptoms until intracranial hypertension causes vomiting and blurred vision. Therefore, unless meningiomas grow substantially and impede cerebrospinal circulation, causing hydrocephalus, early identification is difficult [1,5]. Many authors have reported a relationship between symptoms and tumor location [1–5,7,11]. Visual acuity impairment may result from intracranial hypertension, and visual field defect occurs mainly with tumors of the trigone of lateral ventricles and the occipital angle [8]. Temperament and mood may change in patients with tumors of the trigone of lateral ventricles, and motor and sensory disorders may occur in patients with tumors on top of the lateral ventricles. Except for malignant meningiomas that may relapse postoperatively or metastasize with cerebrospinal fluid, intraventricular meningiomas have good prognoses after surgical resection [12–19]. The selection of an operative approach is crucial because, in most cases, the cortex must be cut open. Therefore, care should be

taken to minimize the impact of the operation on cortical function. Vincenzo et al. [20] summarized the method for selection of the operative approach according to the origin and location of tumors of the lateral ventricles. Our experience indicates that most meningiomas of the lateral ventricles can be resected by corticostomy. Due to the compression of brain tissues by the relatively large tumors, accurate identification of the functional areas is difficult. In this series, although microsurgical strategies were applied, 5 out of the 27 patients developed language disorders (aphasia, mutism) and personality disorders; two had hemiparesis, and 4 presented with visual field defects. Many previous reports indicated operative approach-related complications in patients who underwent resection of ventricular meningiomas, such as hemiparalysis, language disorders, and epilepsy [4,5,8,14,19–22]. We hold that preoperative localization of brain functional areas (e.g., motor area, sensory area, language area and optic center) may help

Fig. 6. Local hydrocephalus after surgery to remove intraventricular meningioma. (A) MRI indicated a lobulated tumor of the left lateral ventricle. (B) CT scans were performed 1 week after tumor resection. (C) CT examination 1 year after surgery indicated local hydrocephalus of the left lateral ventricle. Arrow indicates where the tumor was resected; star indicates the local hydrocephalus.

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determine the displacement of functional areas, and that functional impairment can be prevented through the use of neuronavigation to select the optimal approach. Bertalanffy [23] and Fronda et al. [24] described the advantages of imaging navigation in choosing the approach for resection of tumors of the lateral ventricles. Curry et al. [25] reported the applications of functional magnetic resonance imaging (fMRI) in meningiomas of the lateral ventricles. These technologies are of greater significance to tumors in the dominant hemisphere. We had recently treated 6 patients with meningiomas in the lateral ventricles. Before tumor resection, the language area was located by fMRI. During surgery, arousal was performed using propofol, and the cortical incision was designed with the assistance of neuronavigation and brain mapping. The outcomes of 6 patients with brain mapping were good, with only one case of temporal language disorder for 3 days. Thus, we recommend the use of newly developed technologies including functional location, functional navigation and intraoperative arousal of functional areas. Aside from the neuronavigation system, many technologies such as Horseley-Clarke technique [15], intraoperative ultrasonography [16], and neuro-endoscopy facilitate intraoperative tumor location. We treated patients under real-time ultrasonic guidance to correct the navigation when brain shifts were found after the bone flaps were moved. Neuro-endoscopy is useful in tumor resection. For instance, before the surgeon could see the edge of the tumor, a neuro-endoscope was introduced between the tumor and the ventricular wall to observe blood vessels at the edge of the tumor. Following tumor resection, the neuro-endoscope can be used to observe and irrigate the ventricle. If thorough irrigation and careful observation of the ventricular space were performed using the neuro-endoscope after tumor resection, then postoperative localized hydrocephalus can be prevented, as shown in Fig. 6. Although the KPS resulted in no differences 1 year after surgery between patients treated with and without navigation technologies, the postoperative KPS was good at 1 week and 3 months among patients in whom tumor resection was performed under the directions of neuronavigation, ultrasonography, neuro-endoscopy, fMRI and intraoperative brain mapping. The results suggest that these navigation technologies can at least reduce the incidence of early surgical complications and facilitate more rapid recovery and better quality of life among patients with lateral ventricular meningiomas. We hold that a thorough understanding of the blood supply to massive meningiomas of the lateral ventricles and the use of appropriate countermeasures may reduce the incidence of fatal postoperative hemorrhage. Hemorrhage was reported in several series of patients after resection of ventricular meningiomas [5,13,17], frequently resulting in death. CTA examination of the patient who died in this series (Fig. 2) indicated abundant blood supply to the tumor in this patient. Before interventional therapy, the patient presented with cerebral hernia signs such as coma and dilation of the left pupil. The patient then underwent emergency tumor resection. Despite cerebral decompression, CT performed at 24 h postoperatively (Fig. 2D) suggested cerebral hemorrhage. The patient died 1 week after surgery due to cerebral edema. The patient developed hemorrhagic infarction due to destruction of the draining veins of normal brain tissues. This case suggested that blood vessels should be examined by using CTA, MRA and DSA in tumors with complex blood supplies, and that selective endovascular treatment may be of significance to prevent postoperative hemorrhage.

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Our experiences and lessons in this series of patients indicated that, although post-operative complications are common problems associated with meningiomas in the lateral ventricles because the tumors are large in size and it is necessary to cut the brain open during the surgery, some useful strategies could reduce these surgical complications. The use of fMRI, functional navigation, and intraoperative brain mapping can be used to plan incision of the cortex so as to avoid severe neurological deficits. In addition, neuroimaging technologies such as CTA, neuro-endoscopy, and intraoperative ultrasonography may facilitate microsurgical resection and thereby prevent disastrous consequences. References [1] Caner H, Ac¸ikgöz B, Ozgen T, Colak A, Onol B. Meningiomas of the lateral ventricle. Report on six cases. Neurosurg Rev 1992;15:303–6. [2] Liu M, Wei Y, Liu Y, Zhu S, Li X. Intraventricular meninigiomas: a report of 25 cases. Neurosurg Rev 2006;29:36–40. [3] McDermott MW. Intraventricular meningiomas. Neurosurg Clin N Am 2003;14:559–69. [4] Nakamura M, Roser F, Bundschuh O, Vorkapic P, Samii M. Intraventricular meningiomas: a review of 16 cases with reference to the literature. Surg Neurol 2003;59:491–503. [5] Wang X, Cai BW, You C, He M. Microsurgical management of lateral ventricular meningiomas: a report of 51 cases. Minim Invasive Neurosurg 2007;50:346–9. [6] Bhatoe HS, Singh P, Dutta V. Intraventricular meningiomas: a clinicopathological study and review. Neurosurg Focus 2006;20:E9. [7] Guidetti B, Delfini R, Gagliardi FM, Vagnozzi R. Meningiomas of the lateral ventricles. Clinical, neuroradiologic, and surgical considerations in 19 cases. Surg Neurol 1985;24:364–70. [8] Nagata S, Sasaki T. Lateral transsulcal approach to asymptomatic trigonal meningiomas with correlative microsurgical anatomy: technical case report. Neurosurgery 2005;56:E438. [9] Jelinek J, Smirniotopoulos JG, Parisi JE, Kanzer M. Lateral ventricular neoplasms of the brain: differential diagnosis based on clinical, CT, and MR findings. Am J Roentgenol 1990;155:365–72. [10] Kim EY, Kim ST, Kim HJ, Jeon P, Kim KH, Byun HS. Intraventricular meningiomas: radiological findings and clinical features in 12 patients. Clin Imaging 2009;33(3):175–80. [11] Buhl R, Huang H, Gottwald B, Mihajlovic Z, Mehdorn HM. Neuropsychological findings in patients with intraventricular tumors. Surg Neurol 2005;64:500–3. [12] Kamiya K, Inagawa T, Nagasako R. Malignant intraventricular meningioma with spinal metastasis through the cerebrospinal fluid. Surg Neurol 1989;32:213–8. [13] Lee EJ, Choi KH, Kang SW, Lee IW. Intraventricular hemorrhage caused by lateral ventricular meningioma: a case report. Korean J Radiol 2001;2:105–7. [14] Lyngdoh BT, Giri PJ, Behari S, Banerji D, Chhabra DK, Jain VK. Intraventricular meningiomas: a surgical challenge. J Clin Neurosci 2007;14:442–8. [15] Morita A, Kelly PJ. Resection of intraventricular tumors via a computer-assisted volumetric stereotactic approach. Neurosurgery 1993;32:920–6. [16] Philippe C, Mahmoud Z, Adel M. Microsurgical removal of an intraventricular meningioma with ultrasound guidance, and balloon dilation of operative corridors: case report and technical note. Surg Neurol 1996;45:155–60. [17] Romeike B, Joellenbeck B, Skalej M, Scherlach B, Kirches E, Mawrin C. Intraventricular meningioma with fatal haemorrhage: clinical and autopsy findings. Clin Neurol Neurosurg 2007;109:884–7. [18] Shintaku M, Hashimoto K, Okamoto S. Intraventricular meningioma with anaplastic transformation and metastasis via the cerebrospinal fluid. Neuropathology 2007;27:448–52. [19] Menon G, Nair S, Sudhir J, Rao R, Easwer HV, Krishnakumar K. Meningiomas of the lateral ventricle - a report of 15 cases. Br J Neurosurg 2009;23(3):297–303. [20] Vincenzo A, Marcelo G, Domenico C, Monte V, Bisceglia M, Carosi I. Lateral ventricle tumors: surgical strategies according to tumor origin and development—a series of 72 cases. Neurosurgery 2005;56:36–45. [21] Imaizumi S, Onuma T, Kameyama M, Ishii K. Symptom changes caused by movement of a calcified lateral ventricular meningioma: case report. Surg Neurol 2002;58:128–30. [22] Tokunaga K, Tamiya T, Date I. Transient memory disturbance after removal of an intraventricular trigonal meningioma by a parieto-occipital interhemispheric precuneus approach: case report. Surg Neurol 2006;65:167–9. [23] Bertalanffy A, Roessler K, Koperek O, et al. Intraventricular meningiomas: a report of 16 cases. Neurosurg Rev 2006;29:30–5. [24] Fronda C, Miller D, Kappus C, Bertalanffy H, Sure U. The benefit of image guidance for the contralateral interhemispheric approach to the lateral ventricle. Clin Neurol Neurosurg 2008;110:580–6. [25] Curry WT, Cosgrove GR, Buchbinder BR, Ojemann RG. Resection of a dominanthemisphere intraventricular meningioma facilitated by functional magnetic resonance imaging. Case report. Neurosurg Focus 2001;10:E1.