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Robert Lynagh, Mark Ishak, Joseph Georges, Danielle Lopez, Hany Osman, Michael Kakareka, Brandon Boyer, H. Warren Goldman, Jennifer Eschbacher, Mark C. Preul, Peter Nakaji, Alan Turtz, Steven Yocom and Denah Appelt

OBJECTIVE

Accurate histopathological diagnoses are often necessary for treating neuro-oncology patients. However, stereotactic biopsy (STB), a common method for obtaining suspicious tissue from deep or eloquent brain regions, fails to yield diagnostic tissue in some cases. Failure to obtain diagnostic tissue can delay initiation of treatment and may result in further invasive procedures for patients. In this study, the authors sought to determine if the coupling of in vivo optical imaging with an STB system is an effective method for identification of diagnostic tissue at the time of biopsy.

METHODS

A minimally invasive fiber optic imaging system was developed by coupling a 0.65-mm-diameter coherent fiber optic fluorescence microendoscope to an STB system. Human U251 glioma cells were transduced for stable expression of blue fluorescent protein (BFP) to produce U251-BFP cells that were utilized for in vitro and in vivo experiments. In vitro, blue fluorescence was confirmed, and tumor cell delineation by fluorescein sodium (FNa) was quantified with fluorescence microscopy. In vivo, transgenic athymic rats implanted with U251-BFP cells (n = 4) were utilized for experiments. Five weeks postimplantation, the rats received 5–10 mg/kg intravenous FNa and underwent craniotomies overlying the tumor implantation site and contralateral normal brain. A clinical STB needle containing our 0.65-mm imaging fiber was passed through each craniotomy and images were collected. Fluorescence images from regions of interest ipsilateral and contralateral to tumor implantation were obtained and quantified.

RESULTS

Live-cell fluorescence imaging confirmed blue fluorescence from transduced tumor cells and revealed a strong correlation between tumor cells quantified by blue fluorescence and FNa contrast (R2 = 0.91, p < 0.001). Normalized to background, in vivo FNa-mediated fluorescence intensity was significantly greater from tumor regions, verified by blue fluorescence, compared to contralateral brain in all animals (301.7 ± 34.18 relative fluorescence units, p < 0.001). Fluorescence intensity measured from the tumor margin was not significantly greater than that from normal brain (p = 0.89). Biopsies obtained from regions of strong fluorescein contrast were histologically consistent with tumor.

CONCLUSIONS

The authors found that in vivo fluorescence imaging with an STB needle containing a submillimeter-diameter fiber optic fluorescence microendoscope provided direct visualization of neoplastic tissue in an animal brain tumor model prior to biopsy. These results were confirmed in vivo with positive control cells and by post hoc histological assessment. In vivo fluorescence guidance may improve the diagnostic yield of stereotactic biopsies.

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Ali Tayebi Meybodi, Leandro Borba Moreira, Michael T. Lawton, Jennifer M. Eschbacher, Evgenii G. Belykh, Michelle M. Felicella and Mark C. Preul

OBJECTIVE

In the current neurosurgical and anatomical literature, the intracanalicular segment of the ophthalmic artery (OphA) is usually described to be within the optic nerve dural sheath (ONDS), implying direct contact between the nerve and the artery inside the optic canal. In the present study, the authors sought to clarify the exact relationship between the OphA and ONDS.

METHODS

Ten cadaveric heads were subjected to endoscopic endonasal and transcranial exposures of the OphA in the optic canal (5 for each approach). The relationship between the OphA and ONDS was assessed. Histological examination of one specimen of the optic nerve and the accompanying OphA was also performed to confirm the relationship with the ONDS.

RESULTS

In all specimens, the OphA coursed between the two layers of the dura (endosteal and meningeal) and was not in direct contact with the optic nerve, except for the first few millimeters of the proximal optic canal before it pierced the ONDS. Upon reaching the orbit, the two layers of the dura separated and allowed the OphA to literally float within the orbital fat. The meningeal dura continued as the ONDS, whereas the endosteal dura became the periorbita.

CONCLUSIONS

This study clarifies the interdural course of the OphA within the optic canal. This anatomical nuance has important neurosurgical implications regarding safe exposure and manipulation of the OphA.

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Ali Tayebi Meybodi, Leandro Borba Moreira, Andrew S. Little, Michael T. Lawton and Mark C. Preul

OBJECTIVE

Endoscopic endonasal approaches (EEAs) are increasingly being incorporated into the neurosurgeon’s armamentarium for treatment of various pathologies, including paraclinoid aneurysms. However, few anatomical assessments have been performed on the use of EEA for this purpose. The aim of the present study was to provide a comprehensive anatomical assessment of the EEA for the treatment of paraclinoid aneurysms.

METHODS

Five cadaveric heads underwent an endonasal transplanum-transtuberculum approach to expose the paraclinoid area. The feasibility of obtaining proximal and distal internal carotid artery (ICA) control as well as the topographic location of the origin of the ophthalmic artery (OphA) relative to dural landmarks were assessed. Limitations of the EEA in exposing the supraclinoid ICA were also recorded to identify favorable paraclinoid ICA aneurysm projections for EEA.

RESULTS

The extracavernous paraclival and clinoidal ICAs were favorable segments for establishing proximal control. Clipping the extracavernous ICA risked injury to the trigeminal and abducens nerves, whereas clipping the clinoidal segment put the oculomotor nerve at risk. The OphA origin was found within 4 mm of the medial opticocarotid point on a line connecting the midtubercular recess point to the medial vertex of the lateral opticocarotid recess. An average 7.2-mm length of the supraclinoid ICA could be safely clipped for distal control. Assessments showed that small superiorly or medially projecting aneurysms were favorable candidates for clipping via EEA.

CONCLUSIONS

When used for paraclinoid aneurysms, the EEA carries certain risks to adjacent neurovascular structures during proximal control, dural opening, and distal control. While some authors have promoted this approach as feasible, this work demonstrates that it has significant limitations and may only be appropriate in highly selected cases that are not amenable to coiling or clipping. Further clinical experience with this approach helps to delineate its risks and benefits.

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Ali Tayebi Meybodi, Sirin Gandhi, Mark C. Preul and Michael T. Lawton

OBJECTIVE

Exposure of the vertebral artery (VA) between C-1 and C-2 vertebrae (atlantoaxial VA) may be necessary in a variety of pathologies of the craniovertebral junction. Current methods to expose this segment of the VA entail sharp dissection of muscles close to the internal jugular vein and the spinal accessory nerve. The present study assesses the technique of exposing the atlantoaxial VA through a newly defined muscular triangle at the craniovertebral junction.

METHODS

Five cadaveric heads were prepared for surgical simulation in prone position, turned 30°–45° toward the side of exposure. The atlantoaxial VA was exposed through the subatlantic triangle after reflecting the sternocleidomastoid and splenius capitis muscles inferiorly. The subatlantic triangle was formed by 3 groups of muscles: 1) the levator scapulae and splenius cervicis muscles inferiorly and laterally, 2) the longissimus capitis muscle inferiorly and medially, and 3) the inferior oblique capitis superiorly. The lengths of the VA exposed through the triangle before and after unroofing the C-2 transverse foramen were measured.

RESULTS

The subatlantic triangle consistently provided access to the whole length of atlantoaxial VA. The average length of the VA exposed via the subatlantic triangle was 19.5 mm. This average increased to 31.5 mm after the VA was released at the C-2 transverse foramen.

CONCLUSIONS

The subatlantic triangle provides a simple and straightforward pathway to expose the atlantoaxial VA. The proposed method may be useful during posterior approaches to the craniovertebral junction should early exposure and control of the atlantoaxial VA become necessary.

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Ali Tayebi Meybodi, Sirin Gandhi, Justin Mascitelli, Baran Bozkurt, Gyang Bot, Mark C. Preul and Michael T. Lawton

OBJECTIVE

Access to the ventrolateral pontomesencephalic area may be required for resecting cavernous malformations, performing revascularization of the upper posterior circulation, and treating vascular lesions such as aneurysms. However, such access is challenging because of nearby eloquent structures. Commonly used corridors to this surgical area include the optico-carotid, supracarotid, and carotid-oculomotor triangles. However, the window lateral to the oculomotor nerve can also be used and has not been studied. The authors describe the anatomical window formed between the oculomotor nerve and the medial tentorial edge (the oculomotor-tentorial triangle [OTT]) to the ventrolateral pontomesencephalic area, and assess techniques to expand it.

METHODS

Four cadaveric heads (8 sides) underwent orbitozygomatic craniotomy. The OTT was exposed via a pretemporal approach. The contents of the OTT were determined and their anatomical features were recorded. Also, dimensions of the brainstem surface exposed lateral and inferior to the oculomotor nerve were measured. Measurements were repeated after completing a transcavernous approach (TcA), and after resection of temporal lobe uncus (UnR).

RESULTS

The s1 segment and proximal s2 segment of the superior cerebellar artery (SCA) and P2A segment of the posterior cerebral artery (PCA) were the main contents of the OTT, with average exposed lengths of 6.4 ± 1.3 mm and 5.5 ± 1.6 mm for the SCA and PCA, respectively. The exposed length of the SCA increased to 9.6 ± 2.7 mm after TcA (p = 0.002), and reached 11.6 ± 2.4 mm following UnR (p = 0.004). The exposed PCA length increased to 6.2 ± 1.6 mm after TcA (p = 0.04), and reached 10.4 ± 1.8 mm following UnR (p < 0.001). The brainstem surface was exposed 7.1 ± 0.5 mm inferior and 5.6 ± 0.9 mm lateral to the oculomotor nerve initially. The exposure inferior to the oculomotor nerve increased to 9.3 ± 1.7 mm after TcA (p = 0.003), and to 9.9 ± 2.5 mm after UnR (p = 0.21). The exposure lateral to the oculomotor nerve increased to 8.0 ± 1.7 mm after TcA (p = 0.001), and to 10.4 ± 2.4 mm after UnR (p = 0.002).

CONCLUSIONS

The OTT is an anatomical window that provides generous access to the upper ventrolateral pontomesencephalic area, s1- and s2-SCA, and P2A-PCA. This window may be efficiently used to address various pathologies in the region and is considerably expandable by TcA and/or UnR.

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Evgenii Belykh, Kaan Yağmurlu, Ting Lei, Sam Safavi-Abbasi, Mark E. Oppenlander, Nikolay L. Martirosyan, Vadim A. Byvaltsev, Robert F. Spetzler, Peter Nakaji and Mark C. Preul

OBJECTIVE

The best approach to deep-seated lateral and third ventricle lesions is a function of lesion characteristics, location, and relationship to the ventricles. The authors sought to examine and compare angles of attack and surgical freedom of anterior ipsilateral and contralateral interhemispheric transcallosal approaches to the frontal horn of the lateral ventricle using human cadaveric head dissections. Illustrative clinical experiences with a contralateral interhemispheric transcallosal approach and an anterior interhemispheric transcallosal transchoroidal approach are also related.

METHODS

Five formalin-fixed human cadaveric heads (10 sides) were examined microsurgically. CT and MRI scans obtained before dissection were uploaded and fused into the navigation system. The authors performed contralateral and ipsilateral transcallosal approaches to the lateral ventricle. Using the navigation system, they measured areas of exposure, surgical freedom, angles of attack, and angle of view to the surgical surface. Two clinical cases are described.

RESULTS

The exposed areas of the ipsilateral (mean [± SD] 313.8 ± 85.0 mm2) and contralateral (344 ± 87.73 mm2) interhemispheric approaches were not significantly different (p = 0.12). Surgical freedom and vertical angles of attack were significantly larger for the contralateral approach to the most midsuperior reachable point (p = 0.02 and p = 0.01, respectively) and to the posterosuperior (p = 0.02 and p = 0.04) and central (p = 0.04 and p = 0.02) regions of the lateral wall of the lateral ventricle. Surgical freedom and vertical angles of attack to central and anterior points on the floor of the lateral ventricle did not differ significantly with approach. The angle to the surface of the caudate head region was less steep for the contralateral (135.6° ± 15.6°) than for the ipsilateral (152.0° ± 13.6°) approach (p = 0.02).

CONCLUSIONS

The anterior contralateral interhemispheric transcallosal approach provided a more expansive exposure to the lower two-thirds of the lateral ventricle and striothalamocapsular region. In normal-sized ventricles, the foramen of Monro and the choroidal fissure were better visualized through the lateral ventricle ipsilateral to the craniotomy than through the contralateral approach.

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Michael A. Mooney, Joseph Georges, Mohammedhassan Izady Yazdanabadi, Katherine Y. Goehring, William L. White, Andrew S. Little, Mark C. Preul, Stephen W. Coons, Peter Nakaji and Jennifer M. Eschbacher

OBJECTIVE

The objective of this study was to evaluate the feasibility of using confocal reflectance microscopy (CRM) ex vivo to differentiate adenoma from normal pituitary gland in surgical biopsy specimens. CRM allows for rapid, label-free evaluation of biopsy specimens with cellular resolution while avoiding some limitations of frozen section analysis.

METHODS

Biopsy specimens from 11 patients with suspected pituitary adenomas were transported directly to the pathology department. Samples were immediately positioned and visualized with CRM using a confocal microscope located in the same area of the pathology department where frozen sections are prepared. An H & E–stained slide was subsequently prepared from imaged tissue. A neuropathologist compared the histopathological characteristics of the H & E–stained slide and the matched CRM images. A second neuropathologist reviewed images in a blinded fashion and assigned diagnoses of adenoma or normal gland.

RESULTS

For all specimens, CRM contrasted cellularity, tissue architecture, nuclear pleomorphism, vascularity, and stroma. Pituitary adenomas demonstrated sheets and large lobules of cells, similar to the matched H & E–stained slides. CRM images of normal tissue showed scattered small lobules of pituitary epithelial cells, consistent with matched H & E–stained images of normal gland. Blinded review by a neuropathologist confirmed the diagnosis in 15 (94%) of 16 images of adenoma versus normal gland.

CONCLUSIONS

CRM is a simple, reliable approach for rapidly evaluating pituitary adenoma specimens ex vivo. This technique can be used to accurately differentiate between pituitary adenoma and normal gland while preserving biopsy tissue for future permanent analysis, immunohistochemical studies, and molecular studies.

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Eberval G. Figueiredo, Manoel J. Teixeira and Leonardo C. Welling

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Kaan Yağmurlu, Hasan A. Zaidi, M. Yashar S. Kalani, Albert L. Rhoton Jr., Mark C. Preul and Robert F. Spetzler

Pineal region tumors are challenging to access because they are centrally located within the calvaria and surrounded by critical neurovascular structures. The goal of this work is to describe a new surgical trajectory, the anterior interhemispheric transsplenial approach, to the pineal region and falcotentorial junction area. To demonstrate this approach, the authors examined 7 adult formalin-fixed silicone-injected cadaveric heads and 2 fresh human brain specimens. One representative case of falcotentorial meningioma treated through an anterior interhemispheric transsplenial approach is also described. Among the interhemispheric approaches to the pineal region, the anterior interhemispheric transsplenial approach has several advantages. 1) There are few or no bridging veins at the level of the pericoronal suture. 2) The parietal and occipital lobes are not retracted, which reduces the chances of approach-related morbidity, especially in the dominant hemisphere. 3) The risk of damage to the deep venous structures is low because the tumor surface reached first is relatively vein free. 4) The internal cerebral veins can be manipulated and dissected away laterally through the anterior interhemispheric route but not via the posterior interhemispheric route. 5) Early control of medial posterior choroidal arteries is obtained. The anterior interhemispheric transsplenial approach provides a safe and effective surgical corridor for patients with supratentorial pineal region tumors that 1) extend superiorly, involve the splenium of the corpus callosum, and push the deep venous system in a posterosuperior or an anteroinferior direction; 2) are tentorial and displace the deep venous system inferiorly; or 3) originate from the splenium of the corpus callosum.

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Feres Chaddad-Neto, Marcos Devanir Silva da Costa, Baran Bozkurt, Hugo Leonardo Doria-Netto, Daniel de Araujo Paz, Ricardo da Silva Centeno, Andrew W. Grande, Sergio Cavalheiro, Kaan Yağmurlu, Robert F. Spetzler and Mark C. Preul

OBJECTIVE

The authors report a novel surgical route from a superior anatomical aspect—the contralateral anterior interhemispheric-transcallosal-transrostral approach—to a lesion located in the subcallosal region. The neurosurgical approach to the subcallosal region is challenging due to its deep location and close relationship with important vascular structures. Anterior and inferior routes to the subcallosal region have been described but risk damaging the branches of the anterior cerebral artery.

METHODS

Three formalin-fixed and silicone-injected adult cadaveric heads were studied to demonstrate the relationships between the transventricular surgical approach and the subcallosal region. The surgical, clinical, and radiological history of a 39-year-old man with a subcallosal cavernous malformation was retrospectively used to document the neurological examination and radiographic parameters of such a case.

RESULTS

The contralateral anterior interhemispheric-transcallosal-transrostral approach provides access to the subcallosal area that also includes the inferior portion of the pericallosal cistern, lamina terminalis cistern, the paraterminal and paraolfactory gyri, and the anterior surface of the optic chiasm. The approach avoids the neurocritical perforating branches of the anterior communicating artery.

CONCLUSIONS

The contralateral anterior interhemispheric-transcallosal-transrostral approach may be an alternative route to subcallosal area lesions, with less risk to the branches of the anterior cerebral artery, particularly the anterior communicating artery perforators.