Exoscopic resection of atrial intraventricular meningiomas using a navigation-assisted channel-based trans-sulcal approach: Case series and literature review

Journal of Clinical Neuroscience xxx (xxxx) xxx

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Clinical study

Exoscopic resection of atrial intraventricular meningiomas using a navigation-assisted channel-based trans-sulcal approach: Case series and literature review Michelle Lin a,⇑, Joshua Bakhsheshian a, Ben Strickland a, Robert C. Rennert a, Ray M. Chu b, Kaisorn L. Chaichana c, Gabriel Zada a a

Department of Neurological Surgery, Keck School of Medicine, University of Southern California, Los Angeles, CA, United States Department of Neurological Surgery, Cedars-Sinai, Los Angeles, CA, United States c Department of Neurological Surgery, Mayo Clinic, Jacksonville, FL, United States b

a r t i c l e

i n f o

Article history: Received 11 May 2019 Accepted 21 October 2019 Available online xxxx

a b s t r a c t The surgical treatment of atrial meningiomas carries unique challenges. Recent advancements have aimed to optimize visualization and minimize insult to adjacent tissue. To investigate outcomes following resection of atrial meningiomas using an integrated tubular retraction system with neuro-navigated exoscope. A retrospective analysis of surgical outcomes in consecutive patients who underwent surgical resection of atrial meningiomas via an exoscopic tubular retraction system at three university hospital institutions. Four patients harboring intraventricular meningiomas in the atrium of the lateral ventricle were treated using an integrated navigation-assisted, channel-based trans-sulcal approach via a left temporal-occipital (1), right parieto-occipital (2), or left posterior-temporal (1) sulcal approach with exoscopic visualization. Indications for surgery included headaches (4/4, 100%), dizziness (1/4, 25%), or evidence of progression on imaging (3/4, 75%). Mean maximal tumor diameter was 25.5 mm (range 22–28 mm). No intraoperative complications were observed, and no conversion to a microscopic or open approach was required. Gross total resection (GTR) was obtained in all 4 cases. Median hospital length of stay was 3 days (range 3–4 days). Postoperative complications included homonymous hemianopsia (1) and transient bilateral lower extremity paresthesias (1). At 3-month follow up both complications had improved and all patients had returned to work. At last follow-up (3–24 months), 3 patients (75%) reported improvement of preoperative symptoms. Utilization of a channel-based, navigable retractor with the aid of an exoscope can be an excellent option for accessing the atrium of the lateral ventricles and for achieving complete surgical resection of atrial meningiomas. Ó 2019 Elsevier Ltd. All rights reserved.

1. Introduction Meningiomas are the most common primary intracranial tumor, with over 25,000 new cases diagnosed in the United States each year [1]. A small proportion of these meningiomas are found in the ventricular space, with the majority arising within the Abbreviations: OM, Operating microscope; MRI, Magnetic Resonance Imaging; GTR, gross total resection; NTR, near-total resection; STR, subtotal resection; STROBE, Strengthening the Reporting of Observational studies in Epidemiology; EVD, external ventricular drain; VPS, ventriculo-peritoneal shunt.. ⇑ Corresponding author at: University of Southern California, Department of Neurological Surgery, Keck School of Medicine, 1200 North State St. Suite 3300, Los Angeles, CA 90033, United States. E-mail addresses: [email protected] (M. Lin), [email protected] (J. Bakhsheshian).

atrium of the lateral ventricles [2,3]. The compensatory mechanisms of the fluid filled cavity and slow growing nature of meningiomas often allow for significant growth before detection [3,4]. Presentation is often delayed and nonspecific, with patients reporting headaches, nausea and vomiting that may date back over a decade [3–9]. Various surgical techniques are available, each carrying risks of iatrogenic injury to the intervening cortex and subcortical white matter [3–5,7,10–12]. Despite the benign nature of intraventricular meningiomas, their location/depth, size, consistency, and vascularity continue to pose a unique surgical challenge [3– 5,7,10,12–14]. Given the depth of these tumors, utilizing a transcortical approach to the atrial region of the lateral ventricles can cause inadvertent retraction injury to the traversed cortical tissue and subcortical white matter.

https://doi.org/10.1016/j.jocn.2019.10.017 0967-5868/Ó 2019 Elsevier Ltd. All rights reserved.

Please cite this article as: M. Lin, J. Bakhsheshian, B. Strickland et al., Exoscopic resection of atrial intraventricular meningiomas using a navigation-assisted channel-based trans-sulcal approach: Case series and literature review, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2019.10.017

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M. Lin et al. / Journal of Clinical Neuroscience xxx (xxxx) xxx

Recent advancements in surgical approaches for cranial neurosurgery have been made to optimize visualization while minimizing insult to healthy cortical and subcortical tissue, and these techniques may be efficiently utilized for the surgical management of atrial meningiomas. The operating microscope (OM) has been the primary workhorse of most neurosurgical procedures, and generally offers a wide field with stereopsis during the procedure [15,16]. Visualization of deep-seated lesions can be difficult with the OM, often resulting in poor surgical posture and early surgeon fatigue [15]. Although the endoscope can address some of these shortcomings, the endoscope requires placement within the body cavity, which may obstruct the narrow surgical corridor and is at risk for further visual obstruction by intraoperative bleeding. The development of an extracorporeal telescope (exoscope) provides visualization through projection onto a high definition monitor without obscuring the surgical corridor. In addition to the development of exoscopes, the recent refinement of navigable tubular retractors provides additional technology for gaining access to deep-seated intracranial lesions. These retractors are thought to limit damage to surrounding tissue by distributing their force evenly in a circumferential manner [17– 21]. Recent studies have demonstrated the safe and effective employment of tubular retractors integrated with frameless intraoperative navigations systems for removal of intracranial hematomas [19,22] and deep-seated tumors [17,18,20,23,24]. The authors sought to determine the safety and feasibility of a neuronavigation-assisted channel-based trans-sulcal exoscopic approach for resection of intraventricular meningiomas. We hypothesized that this approach may serve as an alternate approach for these particular lesions vis-à-vis open traditional transcortical approaches. This technique may serve as an additional and perhaps more safe and efficient method for approaching and accessing these deep-seated lesions while mitigating associated risks to surrounding brain matter.

2. Methods 2.1. Study design and setting This is a retrospective review of cases performed at the University of Southern California Keck Hospital and Cedars-Sinai Medical Center and Mayo Clinic between 2014 and 2017. Patients harboring intraventricular meningiomas treated with exoscopic resection via a tubular retractor (BrainPath NICO Corporation, Indianapolis, Indiana, USA) at either institution were included in the study. Institutional review board and ethics committee approval for a retrospective analysis were obtained from respective sites. Consent for surgery was obtained for all patients prior to the procedure in the usual fashion. This manuscript adheres to the guidelines delineated by the Preferred Reporting of Case Series in Surgery (PROCESS) [25].

2.2. Participants, study size, and bias Indications for surgical intervention included symptomatic disease and/or marked interval tumor growth on imaging. All patients had histopathology proven diagnoses of meningioma with WHO grading and at least 3 months of clinical follow up and postoperative MRI (Magnetic Resonance Imaging) at 3 months follow-up. The small sample size precluded power analysis. Consecutive patients at multiple institutions were included to minimize bias. 2.3. Variables and statistical approach Patient information was stored in a secured document and electronic medical records were reviewed for missing data. Variables included demographic and clinical information regarding patient age, gender, preoperative symptoms, hospital length of stay, shunt dependency, clinical status at follow up. Surgical data, including patient positioning, location of craniotomy, and diameter of the tubular retractor were also recorded. Perioperative morbidities and mortalities were considered perioperative if they occurred within 30 days of the surgery. The MRI was reviewed to assess the location, size of the lesion at its widest diameter, and extent of resection after surgery. Extent of resection was defined as gross total resection (GTR; 100%), near-total resection (NTR; >95%), or subtotal resection (STR; <95%). Descriptive statistics (Microsoft Excel 2017) was performed on collected variables. No patients were lost to follow up. 2.4. Operative technique Preoperative MRIs were obtained in accordance with a specified protocol for stereotactic navigation for all patients. These preoperative images aided the selection of a surgical trajectory that would minimize damage to eloquent cortex, subcortical tracts, and neurovascular structures. All cases were performed under general endotracheal anesthesia with continued somatosensory and motor evoke potential (SSEP and MEP) monitoring throughout the duration of the procedure. Patients were positioned in prone or lateral with the affected side facing the surgeon. Neuro-navigation was registered following 3-point fixation with a Mayfield clamp. A variable preoperative craniotomy was planned in the temporaloccipital or parietal-occipital region (Table 1) after identification of an appropriate sulcus overlying the lesion which affords a trajectory parallel to the optic radiations, superior and inferior longitudinal fasciculi to minimize damage to these subcortical tracts. A 3– 4 cm craniotomy was performed in line with the preoperatively planned surgical trajectory. This was followed by a cruciate durotomy approximating the size of the tubular retractor (13 mm). The arachnoid was then divided with sharp microdissection down to the sulcus under visualization with a high definition exoscope (Karl Storz Endoscopy, Tuttlingen, Germany or Synaptive Medical, Toronto, Canada). Sulcal vasculature was preserved and mobilized

Table 1 Patient characteristics. # Age Sex Tumor Diameter (mm)

Port Length (mm)

Approach

Extent of Resection

Hospital LOS (Days)

Surgical Complications

Medical Complications

CSF Diversion*

1 37

F

27

50

Left temporo-occipital junction

GTR

3

None

No

2 54 3 48

F F

28 22

60 60

GTR GTR

4 3

None None

No No

4 49

F

28

60

Right parieto-occipital sulcus Left posterior temporal via superior temporal sulcus Right intraparietal parietal

Homonymous Hemianopsia None None

GTR

3

None

None

EVD (1 day)

Abbreviations: GTR, gross total resection; EVD, external ventricular drainage.

Please cite this article as: M. Lin, J. Bakhsheshian, B. Strickland et al., Exoscopic resection of atrial intraventricular meningiomas using a navigation-assisted channel-based trans-sulcal approach: Case series and literature review, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2019.10.017

M. Lin et al. / Journal of Clinical Neuroscience xxx (xxxx) xxx

to allow for passage of the tubular retractor. The neuro-navigation probe was then placed within the BrainPath (NICO Corporation, Indianapolis, Indiana) tubular retractor. Brain path surgical ports with channel lengths of (50–60 mm) were selected based on the distance from the sulcus to a prespecified target point set at the superficial aspect of the tumor in the lateral ventricle as determined on preoperative imaging. The obturator and dilator precisely cannulated the planned trans-sulcal trajectory until the tip of probe reached the target and was docked on the tumor surface. The inner obturator was then removed from the outer sheath to form a surgical corridor through the tubular retractor. The tubular channel was then secured in place using a standard surgical retractor (e.g., Fukishima or Greenfield). All cases were performed under the guidance of an extracorporeal telescope (Karl Storz Endoscopy, Tuttlingen, Germany or Synaptive Medical, Toronto, Canada) with a focal length of 20– 60 cm. A pneumatic holder (Karl Storz Endoscopy, Tuttlingen, Germany) allowed the exoscope to be secured and mobilized with minimal drift. The tumor was then internally debulked using standard microsurgical techniques. Given the firm consistency of some meningiomas, non-thermal energy producing side cutting aspirators (Myriad from NICO Corporation, Indianapolis, Indiana) and/ or ultrasonic aspirating instruments were used. Following internal debulking, the tumor capsule was carefully dissected from the surrounding structures and folded inwards toward the retractor aperture. Folding of the tumor capsule allows for identification of all surrounding vessels, attachments to the adjacent choroid plexus, and the vascular pedicle which were then cauterized using long bayoneted bipolar forceps and cut [12,21,26]. In the event of intraoperative bleeding, temporary hemostasis was employed with the placement of cottonoids and hemostatic gelatin matrix, following by copious irrigation. Meticulous hemostasis in the surgical cavity and trajectory were ensured with standard hemostatic agents [6,27]. This was followed by copious irrigation to prevent the development of postoperative intraventricular hematoma formation. An external ventricular drain was used at the surgeon’s discretion. A standard multilayer closure was performed in all cases. Surgical highlights were displayed in the included Video. 3. Results 3.1. Patient characteristics A total of 4 patients (Table 1) harboring intraventricular meningiomas in the atrium of the lateral ventricle were treated with an integrated navigation-assisted, channel-based trans-sulcal exoscopic approach. All 4 patients were women ranging from 37 to 54 years in age (mean age 47 years old). All lesions were found in the atrium of the lateral ventricles with 2 (50%) on the left side and 2 (50%) on the right side. Mean maximal tumor diameter was 25.5 mm and ranged from 22 to 28 mm. Presenting symptoms and indications for surgical management included headaches (4/4, 100%), dizziness (1/4, 25%), and/or evidence of interval progression on serial imaging (3/4, 75%). All patients were neurologically intact at the time of operation and no patients had a prior ventricular shunt. Clinical and radiological follow up for patients ranged from 3 months to 2 years. 3.2. Surgical outcomes Surgical approaches included 1 left temporal-occipital (Fig. 1), 2 right parietal-occipital (Fig. 2) and 1 left posterior-temporal craniotomies. No intraoperative complications were observed and conversion to a microscopic or an open approach was not needed in any of the cases. Monitored somatosensory and motor evoked

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potentials for all patients remained stable throughout the procedure and no blood transfusions were required in the intraoperative and postoperative period. Gross total resection was achieved in all 4 patients (100%). An external ventricular drain was temporarily placed in 1 patient at the end of the operation for drainage of postoperative intraventricular debris and blood products and was removed on postoperative day 1. No patient’s experienced intracranial hypertension requiring the placement of an external ventricular drain in the post-operative period. The median length of stay in the hospital was 3 days (range 3–4 days). Two postoperative complications occurred. One case of incomplete homonymous heminanopsia occurred following a left temporal-occipital approach, that markedly improved at 3 months follow up, with a slight residual deficit limited to the most lateral periphery on follow-up 2 years later. One patient developed transient bilateral lower extremity paresthesias, which was attributable to residual intrathecal blood products in the CSF. There were no perioperative mortalities in our series. 3.3. Clinical outcomes All patients were functioning independently at 3-month follow up and had returned to their original work. Three patients (75%) reported improvement of preoperative symptoms following resection. One patient (25%) reported continuous symptoms of headache and dizziness, which was effectively controlled with medical management. Histopathology for all patients (100%) was diagnostic for a WHO Grade I Meningioma. There was no radiological evidence or clinical symptoms suggestive of hydrocephalous at 3-months follow-up. No patients required adjuvant radiotherapy and no recurrences had occurred at the time of this study. Follow-up MRIs showed no evidence of tumor residual or recurrence over the study period. 3.4. Illustrative case A 34-year-old woman in the second trimester of pregnancy presented with persistent headaches, and was found to have a left sided atrial ventricular mass upon imaging. Given the pregnancy, the decision was made to defer surgical management and monitor the lesion with serial imaging. Over the course of 3 years, the lesion demonstrated interval growth. MRI demonstrated an avidly enhancing, heterogeneous left atrial ventricular mass that measured 27  27  26 mm and was intimately associated with the choroid plexus without signs of hydrocephalus (Fig. 1A-C). Given persistent symptoms and marked interval growth on serial imaging, the decision was made to proceed with surgical resection (Video). The patient was positioned in a right lateral decubitus position for a left temporal-occipital craniotomy (4 cm). An approximate 13 mm durotomy (Fig. 3A) was performed overlying the selected trans-sulcal trajectory under intraoperative neuronavigation guidance. Following sulcal dissection, a 50 mm BrainPath tubular retractor was placed until the superficial extent of the lesion was encountered (Fig. 3B). The lesion was then internally debulked with microsurgical techniques and the aid of a side cutting aspirator until the tumor capsule folded and capsular dissection was completed. No residual tumor was observed intraoperatively (Fig. 3C). No transfusions were required throughout the duration of the procedure and meticulous hemostasis was confirmed prior to closing. Following the procedure, the patient was successfully extubated and monitored in the intensive care unit overnight and transferred to the surgical inpatient floor the following day. The patient was found to have a mild right homonymous hemianopsia postoperatively. No other perioperative complications occurred and the patient was discharged home on postoperative day 3. Marked improvement of the patient’s visual

Please cite this article as: M. Lin, J. Bakhsheshian, B. Strickland et al., Exoscopic resection of atrial intraventricular meningiomas using a navigation-assisted channel-based trans-sulcal approach: Case series and literature review, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2019.10.017

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M. Lin et al. / Journal of Clinical Neuroscience xxx (xxxx) xxx

Fig. 1. Preoperative and postoperative imaging of Case #1. A 27  27  26 mm mass with minimal perilesional edema is found in the left lateral ventricle on MRI (1A – Axial T2W FLAIR, B – Axial T2 Fat saturation, C – Coronal Fast Field Echo Post-Contrast). There is no associated hydrocephalous, ventricle trapping, or midline shift. Gross total resection without recurrence is appreciated on imaging one year after the operation (D – Axial FLAIR, E – Axial T1W Post-contrast, F – Coronal T1W Post-contrast). There is no evidence of retractor associated edema or ischemia along the surgical trajectory. MRI – Magnetic Resonance Imaging, T2W – T2 Weighted, FLAIR – Fluid attenuated inversion recovery, T1W – T1 Weighted).

Fig. 2. Preoperative and postoperative imaging of Case #2. Patient was found to have 3 cm lesion in the right occipital horn exerting significant mass effect on the surrounding tissue (A-C) consisted with an atrial meningioma. The lesion is hypointense to grey matter on T1-weighted MRI, hyperintense to grey matter on T2-weighted MRI with prominent surrounding vasogenic edema (A – Axial T1W Post-contrast, B – Axial T2W FLAIR, C – Coronal T1W Post contrast). Due to the marked edema and size of the lesion the patient was not an ideal candidate for radiosurgery and surgical resection was offered. A right parieto-occipital approach was performed. Postoperative imaging demonstrated complete resection of the intraventricular lesion with marked resolution of surrounding edema and no evidence of hydrocephalous (D – Axial T1W Fat saturation, E – Axial T2W FLAIR, F – Coronal T1W Post-contrast). MRI – Magnetic Resonance Imaging, T2W – T2 Weighted, FLAIR – Fluid attenuated inversion recovery, T1W – T1 Weighted.

Please cite this article as: M. Lin, J. Bakhsheshian, B. Strickland et al., Exoscopic resection of atrial intraventricular meningiomas using a navigation-assisted channel-based trans-sulcal approach: Case series and literature review, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2019.10.017

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M. Lin et al. / Journal of Clinical Neuroscience xxx (xxxx) xxx

Fig. 3. Case 1 surgical highlights. (A) An approximate 13 mm durotomy was performed overlying the selected trans-sulcal trajectory under intraoperative neuro-navigation guidance. (B) The BrainPath tubular retractor was placed until the superficial extent of the lesion was encountered. (C) No residual tumor was observed after resection was completed. A gross total intraoperative resection was achieved.

field deficits were noted at 2-week follow-up, with her homonymous hemianopsia only being appreciated in the most lateral extent of her right visual field at 2-year follow-up. The patient reported complete resolution of her headaches and had returned to full time work and driving by 3 months follow-up. Postoperative MRI demonstrated a GTR of the lesion (Fig. 1 D-F). 4. Discussion The following surgical case-series demonstrated the potential benefits of a less invasive channel-based trans-sulcal approach for intraventricular meningiomas localized to the atrial region. This underscores the benefits of a navigable tubular retractor and exoscope for accessing deep-seated tumors otherwise approached via open transcortical approaches requiring extensive retraction of normal cortical and subcortical structures. The channel-based approach can be especially useful for deep-seated tumors that require two-handed microdissection maneuvers without normal brain tissue obscuring the surgical field. Gross total resection was achieved in all included cases of atrial intraventricular meningiomas with transient or minimal persisting neurological deficits. When approaching intraventricular meningiomas, a crucial consideration is that these lesions are notoriously vascular. This often presents a particular technical challenge in the ventricular system and is the primary prohibitive variable against the use of a pure channel-based or endoscopic approach in such procedures. Gaining early access to the vascular origin is essential in minimizing intraoperative blood loss and preventing the formation of dangerous intraventricular hematomas in the post-operative period [14,26,28,29]. Some authors have even advocated for the use of preoperative angiography to localize the vascular supply [3,30]. Atrial meningiomas commonly derive their vascular supply from the choroidal arteries. These arterial vessels are typically not large enough for catheterization without a substantial risk of vasopasm [5,12], unless they have undergone marked hypertrophy [30]. Control of the vascular pedicle was successful in all patients in this surgical series. There exists some concern that hostile sulcal vasculature can also be encountered during a trans-sulcal approach especially in cases where the sulcus is compressed from preoperative intracranial hypertension [13,29,31,32]. However, no

patients in the current series had evidence of preoperative hydrocephalus and the sulcal vasculature could be mobilized in all cases without iatrogenic injury. One patient presented to an urgent care in the postoperative period complaining of postoperative paresthesias, which was likely attributable to residual intrathecal blood products. Multiple surgical approaches to the atrium of the lateral ventricle have been described (Table 2). One previously described approach that offers early access to the vascular pedicle is through a posterior middle or inferior transtemporal gyrus approach [33]. This approach provides the shortest distance to lesions of the inferior atrium, and the inferior transtemporal approach can facilitate retraction in cases of temporal horn entrapment [5,10,12,29]. Utilizing a parallel trajectory is thought to minimize the risk of injury to the optic radiations. However, this approach still carries a substantial risk of visual field deficits and aphasia on the dominant side [5,10,12,29]. When employing a posterior temporal approach, surgeons must also remain cognizant of the trajectory’s proximity to cortical venous vasculature, most notably the anastomotic Vein of Labbe [29,32,34]. A parieto-occipital approach mitigates some of the risks associated with the transtemporal approach and is one of the most frequently utilized approaches to the atrial regions [4,6,7,12,14,26,28,29]. The optic radiations are less disturbed when using this approach because they course in the lateral wall of the atrium and the posterior horn. In large atrial lesions with marked superior extension, a superior parietal trans-sulcal approach can be used while taking into consideration the risk for postoperative Gerstmann’s syndrome when operating in the nondominant hemisphere [29]. Various interhemispheric transcallosal approaches have also been described such as Yasargil’s precuneal approach and Kempe & Blaylock’s posterior transcallosal approach [35,36]. However, these approaches carry a risk of dissociation syndrome if the corpus callosotomy is greater than 2 in. in length. The channel-based approach detailed in our series allows surgeons to avoid some of the complications associated with these aforementioned procedures. While we did not compare the risk of retraction injury between patients treated with a channel based versus traditional open craniotomies, previous studies have demonstrated the safety of channel-based approaches as a retrac-

Table 2 Summary of most frequently utilized surgical approaches to atrial meningiomas previously described in the literature. Surgical approach

Study

Parietal/Parietooccipital

Bertalanffy, Menon, Nakamura, Nanda, Wang

Benefits – Chosen for large atrial lesions with superior extension – Less damage to Wernicke’s area

Middle Temporal Gyrus

Lyngdoh, Menon, Nayar, Wang

Transcallosal

Liu, Nakamura, Nayar, Wang

– – – – –

Early access to vascular pedicle Decompression of trapped temporal horn Shortest trajectory to atrial lesions Ideal for frontal horn lesions Avoidance of corticectomy

Risks – – – – – –

Gerstmann’s Syndrome Potential motor deficits Late access to vascular pedicle Damage to optic radiations Damage to optic radiations Aphasia when in the dominant hemisphere – Dissociation Syndrome – Venous Insufficiency – Short term memory loss

Please cite this article as: M. Lin, J. Bakhsheshian, B. Strickland et al., Exoscopic resection of atrial intraventricular meningiomas using a navigation-assisted channel-based trans-sulcal approach: Case series and literature review, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2019.10.017

Study

Study Approach Size*

Preoperative Morbidity Hydrocephalus

Mortality GTR Rate

Follow up (Mo.)

Recurrence

VPS Required

Bertalanffy et al. (2006)

15

Parietal (Superior parietal lobule, Interparietal Sulcus, Parieto-occipital) – 14 Suboccipital – 1

N/A

6.7%

93%

N/A

N/A

N/A

Bhatoe et al. (2006)

12

Parieto-occipital Transcortical – 9 Transcortical Tranventricular – 1 Not specified – 2

N/A

8.3%

N/A

36– 120

0%

N/A

Eliyas et al. (2015) Hong et al. (2016) Kim et al. (2008)

2 1 12

Transsulcal via Tubular Retractor – 2 Transsulcal via Tubular Retractor – 1 Not Specified

0% N/A 83%

Motor Deficit – 1 VF Deficits – 1 New Onset Seizures – 1 CN Deficits – 1 Transient aphasia – 2 CSF leak – 1 Meningitis – 1 Oropharyngeal Paralysis – 1 None N/A N/A

0% N/A N/A

100% 100% 100%

6–27 N/A 13–64

0% N/A N/A

Liu et al. (2006)

24

N/A

87.5% 6–180

9

11.1%

88.9% 4–120

N/A

11.1%

Ma et al. (2014)

43

0%

100%

0%

4.7%

Menon et al. (2009)

15

Parieto-occipital Transcortical – 11 Middle Temporal Gyrus – 4

N/A

0%

86.7% 12–96

13.3%

0%

Nakamura et al. (2003)

16

87.5%

0%

93.8% 6–132

6.25%

N/A

Nanda et al. (2015)

17

Nayar et al. (2010)

13

Odegaard et al. (2013)

22

Ratre et al. (2016) Wang et al. (2007)

12 51

Zanini et al. (2011)

6

Zhu et al. (2013) Present Study

2 4

Parieto-occipital Transcortical – 10 Transcallosal – 3 Frontal – 1 Median Suboccipital – 2 Parieto-occipital Transcortical – 9 Superior Parietal Transcortical – 1 Middle Temporal Gyrus – 1 Transcallosal – 1 Suboccipital Telovelar – 3 Superior Parietal Lobule – 5 Middle Temporal Gyrus – 6 Transcallosal – 2 Parieto-occipital Transcortical – 20 Anterior Transcortical – 1 Posterior Fossa – 1 Transsulcal via Tubular Retractor – 12 Parieto-occipital Transcortical – 38 Middle Temporal Gyrus – 9 Transcallosal – 4 Transparietal Transcortical – 3 Middle Temporal Gyrus – 2 Parieto-Occipital Interhemispheric Precuneus – 1 Interhemispheric Transfalcine Transprecuneus – 2 Transsulcal via Tubular Retractor – 4

VF Deficit – 2 New Onset Seizures – 1 Motor Deficit – 3 Motor Deficit – 1 VF Deficit – 1 Meningitis – 1 Intracranial Hypertension requiring surgical intervention – 2 Epidural Hematoma requiring evacuation – 2 Localized hydrocephalus – 3 Motor Deficit – 3 VF Deficit – 2 New Onset Seizures – 2 Dysphagia – 1 VF Deficit – 2 New Onset Seizure – 1

0%

Lyngdoh et al. (2007)

Parieto-occipital Transcortical – 20 Transcallosal – 2 Frontal transcortical – 2 Posterior Middle Temporal Gyrus – 5 Superior Parietal Lobule – 2 Midline Suboccipital – 2 Transsulcal Parietal or Temporal – 43

0% N/A 17% (All recurrences in WHO Grade IV lesions) 8.3% (2/3 STR developed recurrences)

44.4%

14%

2–71

N/A

44.4%

New Onset Hydrocephalus – 2 New Onset Seizure – 3

0%

100%

6–230

28%

17.6%

N/A

0%

100%

N/A

0%

N/A

N/A

Alexia, aphasia, agraphia – 2 VF Deficits – 1 Short term memory loss – 1 N/A

0%

95%

12– 120

4.6% (Recurrence in WHO Grade II)

N/A

N/A N/A

N/A VF Deficit or Sensory Aphasia – 2

N/A 1.9%

N/A N/A 94.1% 6–120

N/A 0%

N/A 0%

50%

None

0%

100%

23

0%

N/A

N/A 0%

None VF Deficit – 1

0% 0%

100% 100%

15 3–12

0% 0%

0% 0%

Select studies did not include additional information on the specified approach and were therefore not included in the table summary.

M. Lin et al. / Journal of Clinical Neuroscience xxx (xxxx) xxx

*

6

Please cite this article as: M. Lin, J. Bakhsheshian, B. Strickland et al., Exoscopic resection of atrial intraventricular meningiomas using a navigation-assisted channel-based trans-sulcal approach: Case series and literature review, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2019.10.017

Table 3 Summary of comparative investigations demonstrating surgical management of intraventricular meningiomas.

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tion system. Several studies have evaluated peri-trajectory retraction injury, as represented by cytotoxic edema (T2W FLAIR / ADC signal). When comparing the pre and postoperative imaging of patients undergoing channel-based resection of deep-seated lesions, Recinos et al. found no difference in FLAIR/ADC signal in the majority (8/9, 88%) of their patients [37]. In the one patient with increased FLAIR/ADC signal, there was no associated clinical deficit. This has since been further validated in similar studies with both pediatric and adult patients with larger sample sizes [18,38]. As a result of this, we hypothesized that the risk of post-operative seizures, aphasia, and Gerstmann’s syndrome are limited using a channel-based approach. However, as evidenced by the illustrative case, the risk of postoperative visual field deficits continues to persist even when attempting an approach in line with the optic radiations. It is unclear if this occurred during resection or due to cannulation [7]. This may have been prevented with the use of diffusion tensor imaging (DTI) tractography of the optic radiation for planning the surgical trajectory or continuous visual evoked potential monitoring [39]. As the use of tubular retractors gains momentum in neurosurgical practice, its scope of utility has gradually expanded from less invasive spinal procedures to management of deep-seated intracranial neoplasms and intracranial hemorrhages [17–23]. It is felt that the soft consistency of intracranial hematomas is one of the characteristics that make them particularly amenable to resection with channel-based approaches [19,23]. In patients harboring meningiomas, extent of resection is highly correlated with differences in long term outcomes. Recurrences following surgical resection occur at an appreciable rate even in low-grade lesions [3,5–7,14,33,40]. There is some concern as to whether the narrow surgical corridor provided by a channel-based approach provides an adequate enough exposure for complete resection of fibrous meningiomas [40]. In the current series, a gross total resection was obtained in all of the patients with the use of a tubular retractor (Table 1). This is comparable to rates reported by other surgical series (87–100%) in the literature (Table 3) [2–5,7,10,12–14,29,31 ,40]. Despite the firm fibrous consistency of lesions in this series, employment of side-cutting and ultrasonic aspirators allowed for complete resection of all meningiomas [41,42]. Previous authors have proposed methods to predict tumor consistency [43,44] and degree of meningioma-brain adhesion [45] on preoperative imaging, suggesting that hyperintensity relative to grey matter on T2weighted imaging can be predictive for softer intraoperative tumor consistency. Standardized grading systems for intraoperative meningioma consistency have been proposed, and have shown 90% inter-user agreement [42]. These proposed systems may aid surgeons in identifying which lesions are more likely amenable to gross total resection even with less invasive surgical approaches. Further research is needed to substantiate this application. In addition to the utilization of tubular retractors, our employment of exoscopes for visualization also deviated from the traditional open craniotomy. Exoscopes are a telescopic visualization system in which the camera is situated above the operative field, where it does not limit access to the operative real estate. The first reported use of exoscopes for cranial neurosurgery came from Mamelak et al. in 2010 [16]. Initial limitations in maneuverability and lack of stereopsis have since been mitigated with the development of high definition 3D systems and improvements in the camera arm holder [46]. One of the benefits of the exoscope is its minimal profile in comparison to the cumbersome traditional operative microscope which requires a hydraulic counterbalance system [47]. Similarly, the low profile hardware is translated into a more affordable visualization system. The most lauded benefit of the exoscope is surgeon comfort, compared to the ergonomics of a traditional microscope, surgeons are able to operate without bending their neck [16,46,48]. Additionally, the long focal distance

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of the exoscope permits visualization of a wider operative field limiting the frequency of refocusing [49], resulting in ease of achieving hemostasis when unexpected bleeding occurs [49]. This is in contrast to the extended irrigation required with endoscopy when lenses are obscured by blood and fog, requiring frequent cleanings that disrupt the work flow. In a cadaveric model, Sack et al. demonstrated comparable operative times in standard neurosurgical cranial procedures between operative microscopes and exoscopes. Furthermore, the projection of the operative field onto high resolution screens, holds tremendous educational potential, and contributed to a cohesive operative work flow for the surgical team [49]. As with all novel procedures, one of the main drawbacks of the exoscope is the learning curve, particularly for the assistant who must adjust to the primary surgeon’s visual perspective. However, this has not proved to be prohibitive in clinical settings [46,49]. Limitations to this study include the retrospective nature of its design, the limited extent of follow up, and a small sample size. Patients were not randomized to a channel-based approach resulting in inherent patient selection bias. The lesions in our series are also smaller than those previously reported in the literature [26]. However, the primary purpose of this study was to demonstrate the safety and feasibility in performing a neuro-navigationassisted channel-based trans-sulcal exoscopic approach to intraventricular meningiomas. 5. Conclusions Recent technological advances have introduced new operative tools to the surgical armamentarium that expand the access of less invasive procedures to even deep-seated intraventricular lesions. The vascularity and fibrous nature of intraventricular meningiomas presents a unique surgical challenge but does not preclude surgeons from achieving complete resections through a channelbased approach, where neurosurgical principles of two-handed microdissection and bipolar cautery can be maintained. The current series demonstrated that a neuro-navigation-assisted channel-based trans-sulcal exoscopic approach to intraventricular meningioma is safe and effective for accessing deep-seated intraventricular meningiomas and facilitating complete resection Disclosures US Food and Drug Administration–approved access system (BrainPath, NICO Corporation, Indianapolis, Indiana). The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper. Conflict of interest None. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.jocn.2019.10.017. References [1] Ostrom QT, Gittleman H, Fulop J, et al. CBTRUS Statistical Report: Primary Brain and Central Nervous System Tumors Diagnosed in the United States in 20082012. Neuro-oncology. 2015;17 Suppl 4:iv1-iv62. [2] 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(6):491–503. discussion 503-494. [3] Liu M, Wei Y, Liu Y, Zhu S, Li X. Intraventricular meninigiomas: a report of 25 cases. Neurosurg Rev 2006;29(1):36–40.

Please cite this article as: M. Lin, J. Bakhsheshian, B. Strickland et al., Exoscopic resection of atrial intraventricular meningiomas using a navigation-assisted channel-based trans-sulcal approach: Case series and literature review, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2019.10.017

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Please cite this article as: M. Lin, J. Bakhsheshian, B. Strickland et al., Exoscopic resection of atrial intraventricular meningiomas using a navigation-assisted channel-based trans-sulcal approach: Case series and literature review, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2019.10.017