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The history of therapeutic hypothermia and its use in neurosurgery

Michael A. Bohl, Nikolay L. Martirosyan, Zachary W. Killeen, Evgenii Belykh, Joseph M. Zabramski, Robert F. Spetzler, and Mark C. Preul

Despite an overwhelming history demonstrating the potential of hypothermia to rescue and preserve the brain and spinal cord after injury or disease, clinical trials from the last 50 years have failed to show a convincing benefit. This comprehensive review provides the historical context needed to consider the current status of clinical hypothermia research and a view toward the future direction for this field. For millennia, accounts of hypothermic patients surviving typically fatal circumstances have piqued the interest of physicians and prompted many of the early investigations into hypothermic physiology. In 1650, for example, a 22-year-old woman in Oxford suffered a 30-minute execution by hanging on a notably cold and wet day but was found breathing hours later when her casket was opened in a medical school dissection laboratory. News of her complete recovery inspired pioneers such as John Hunter to perform the first complete and methodical experiments on life in a hypothermic state. Hunter’s work helped spark a scientific revolution in Europe that saw the overthrow of the centuries-old dogma that volitional movement was created by hydraulic nerves filling muscle bladders with cerebrospinal fluid and replaced this theory with animal electricity. Central to this paradigm shift was Giovanni Aldini, whose public attempts to reanimate the hypothermic bodies of executed criminals not only inspired tremendous scientific debate but also inspired a young Mary Shelley to write her novel Frankenstein. Dr. Temple Fay introduced hypothermia to modern medicine with his human trials on systemic and focal cooling. His work was derailed after Nazi physicians in Dachau used his results to justify their infamous experiments on prisoners of war. The latter half of the 20th century saw the introduction of hypothermic cerebrovascular arrest in neurosurgical operating rooms. The ebb and flow of neurosurgical interest in hypothermia that has since persisted reflect our continuing struggle to achieve the neuroprotective benefits of cooling while minimizing the systemic side effects.

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Quantitative anatomical analysis and clinical experience with mini-pterional and mini-orbitozygomatic approaches for intracranial aneurysm surgery

Kaan Yagmurlu, Sam Safavi-Abbasi, Evgenii Belykh, M. Yashar S. Kalani, Peter Nakaji, Albert L. Rhoton Jr., Robert F. Spetzler, and Mark C. Preul

OBJECTIVE

The aim of this investigation was to modify the mini-pterional and mini-orbitozygomatic (mini-OZ) approaches in order to reduce the amount of tissue traumatization caused and to compare the use of the 2 approaches in the removal of circle of Willis aneurysms based on the authors' clinical experience and quantitative analysis.

METHODS

Three formalin-fixed adult cadaveric heads injected with colored silicone were examined. Surgical freedom and angle of attack of the mini-pterional and mini-OZ approaches were measured at 9 anatomical points, and the measurements were compared. The authors also retrospectively reviewed the cases of 396 patients with ruptured and unruptured single aneurysms in the circle of Willis treated by microsurgical techniques at their institution between January 2006 and November 2014.

RESULTS

A significant difference in surgical freedom was found in favor of the mini-pterional approach for access to the ipsilateral internal carotid artery (ICA) and middle cerebral artery (MCA) bifurcations, the most distal point of the ipsilateral posterior cerebral artery (PCA), and the basilar artery (BA) tip. No statistically significant differences were found between the mini-pterional and mini-OZ approaches for access to the posterior clinoid process, the most distal point of the superior cerebellar artery (SCA), the anterior communicating artery (ACoA), the contralateral ICA bifurcation, and the most distal point of the contralateral MCA. A trend toward increasing surgical freedom was found for the mini-OZ approach to the ACoA and the contralateral ICA bifurcation. The lengths exposed through the mini-OZ approach were longer than those exposed by the mini-pterional approach for the ipsilateral PCA segment (11.5 ± 1.9 mm) between the BA and the most distal point of the P2 segment of the PCA, for the ipsilateral SCA (10.5 ± 1.1 mm) between the BA and the most distal point of the SCA, and for the contralateral anterior cerebral artery (ACA) (21 ± 6.1 mm) between the ICA bifurcation and the most distal point of the A2 segment of the ACA. The exposed length of the contralateral MCA (24.2 ± 8.6 mm) between the contralateral ICA bifurcation and the most distal point of the MCA segment was longer through the mini-pterional approach. The vertical angle of attack (anteroposterior direction) was significantly greater with the mini-pterional approach than with the mini-OZ approach, except in the ACoA and contralateral ICA bifurcation. The horizontal angle of attack (mediolateral direction) was similar with both approaches, except in the ACoA, contralateral ICA bifurcation, and contralateral MCA bifurcation, where the angle was significantly increased in the mini-OZ approach.

CONCLUSIONS

The mini-pterional and mini-OZ approaches, as currently performed in select patients, provide less tissue traumatization (i.e., less temporal muscle manipulation, less brain parenchyma retraction) from the skin to the aneurysm than standard approaches. Anatomical quantitative analysis showed that the mini-OZ approach provides better exposure to the contralateral side for controlling the contralateral parent arteries and multiple aneurysms. The mini-pterional approach has greater surgical freedom (maneuverability) for ipsilateral circle of Willis aneurysms.

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Arteriovenous malformation with unique drainage through the emissary vein of the foramen ovale: illustrative case

Xiaochun Zhao, Alexander R Evans, Ali Tayebi Meybodi, Nicholas Hopkins, Ira Bowen, Shyian S Jen, Mark C Preul, and Karl Balsara

BACKGROUND

As part of the laterotrigeminal venous system (LTVS), the emissary vein of the foramen ovale (EVFO) is an underrecognized venous structure communicating between the cavernous sinus and pterygoid plexus. The sphenobasal sinus is an anatomical variation of the sphenoparietal sinus that drains directly into the EVFO. The authors present the case of a ruptured arteriovenous malformation (AVM) with a unique drainage pattern through the sphenobasal sinus and EVFO.

OBSERVATIONS

A 9-year-old female initially presented with loss of consciousness and was subsequently found to have a ruptured AVM in the left basal frontal area. She underwent an immediate decompressive hemicraniectomy, with a computed tomography angiogram demonstrating a unique anatomical variation in which the sphenobasal sinus communicated with the EVFO and LTVS. The final venous drainage returned to the pterygoid plexus and external jugular vein. Postoperatively, the patient made a substantial recovery, with generalized right-sided weakness remaining as the sole deficit.

LESSONS

The authors present the case of a ruptured AVM with unique venous drainage into the sphenobasal sinus and EVFO, for which the current literature remains limited. As exemplified by this illustrative case, technique modification may be warranted in the setting of this unique anatomical variation to avoid venous sinus injury.

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Contralateral interoptic approach to paraclinoid aneurysms: a patient-selection algorithm based on anatomical investigation and clinical validation

Xiaochun Zhao, Ali Tayebi Meybodi, Mohamed A. Labib, Sirin Gandhi, Evgenii Belykh, Komal Naeem, Mark C. Preul, Peter Nakaji, and Michael T. Lawton

OBJECTIVE

Aneurysms that arise on the medial surface of the paraclinoid segment of the internal carotid artery (ICA) are surgically challenging. The contralateral interoptic trajectory, which uses the space between the optic nerves, can partially expose the medial surface of the paraclinoid ICA. In this study, the authors quantitatively measure the area of the medial ICA accessible through the interoptic triangle and propose a potential patient-selection algorithm that is based on preoperative measurements on angiographic imaging.

METHODS

The contralateral interoptic trajectory was studied on 10 sides of 5 cadaveric heads, through which the medial paraclinoid ICA was identified. The falciform ligament medial to the contralateral optic canal was incised, the contralateral optic nerve was gently elevated, and the medial surface of the paraclinoid ICA was inspected via different viewing angles to obtain maximal exposure. The accessible area on the carotid artery was outlined. The distance from the distal dural ring (DDR) to the proximal and distal borders of this accessible area was measured. The superior and inferior borders were measured using the clockface method relative to a vertical line on the coronal plane. To validate these parameters, preoperative measurements and intraoperative findings were reviewed in 8 clinical cases.

RESULTS

In the sagittal plane, the mean (SD) distances from the DDR to the proximal and distal ends of the accessible area on the paraclinoid ICA were 2.5 (1.52) mm and 8.4 (2.32) mm, respectively. In the coronal plane, the mean (SD) angles of the superior and inferior ends of the accessible area relative to a vertical line were 21.7° (14.84°) and 130.9° (12.75°), respectively. Six (75%) of 8 clinical cases were consistent with the proposed patient-selection algorithm.

CONCLUSIONS

The contralateral interoptic approach is a feasible route to access aneurysms that arise from the medial paraclinoid ICA. An aneurysm can be safely clipped via the contralateral interoptic trajectory if 1) both proximal and distal borders of the aneurysm neck are 2.5–8.4 mm distal to the DDR, and 2) at least one border of the aneurysm neck on the coronal clockface is 21.7°–130.9° medial to the vertical line.

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Interdural course of the ophthalmic artery in the optic canal

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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Infraorbital nerve: a surgically relevant landmark for the pterygopalatine fossa, cavernous sinus, and anterolateral skull base in endoscopic transmaxillary approaches

Ali M. Elhadi, Hasan A. Zaidi, Kaan Yagmurlu, Shah Ahmed, Albert L. Rhoton Jr., Peter Nakaji, Mark C. Preul, and Andrew S. Little

OBJECTIVE

Endoscopic transmaxillary approaches (ETMAs) address pathology of the anterolateral skull base, including the cavernous sinus, pterygopalatine fossa, and infratemporal fossa. This anatomically complex region contains branches of the trigeminal nerve and external carotid artery and is in proximity to the internal carotid artery. The authors postulated, on the basis of intraoperative observations, that the infraorbital nerve (ION) is a useful surgical landmark for navigating this region; therefore, they studied the anatomy of the ION and its relationships to critical neurovascular structures and the maxillary nerve (V2) encountered in ETMAs.

METHODS

Endoscopic anatomical dissections were performed bilaterally in 5 silicone-injected, formalin-fixed cadaveric heads (10 sides). Endonasal transmaxillary and direct transmaxillary (Caldwell-Luc) approaches were performed, and anatomical correlations were analyzed and documented. Stereotactic imaging of each specimen was performed to correlate landmarks and enable precise measurement of each segment.

RESULTS

The ION was readily identified in the roof of the maxillary sinus at the beginning of the surgical procedure in all specimens. Anatomical dissections of the ION and the maxillary branch of the trigeminal nerve (V2) to the cavernous sinus suggested that the ION/V2 complex has 4 distinct segments that may have implications in endoscopic approaches: 1) Segment I, the cutaneous segment of the ION and its terminal branches (5–11 branches) to the face, distal to the infraorbital foramen; 2) Segment II, the orbitomaxillary segment of the ION within the infraorbital canal from the infraorbital foramen along the infraorbital groove (length 12 ± 3.2 mm); 3) Segment III, the pterygopalatine segment within the pterygopalatine fossa, which starts at the infraorbital groove to the foramen rotundum (13 ± 2.5 mm); and 4) Segment IV, the cavernous segment from the foramen rotundum to the trigeminal ganglion (15 ± 4.1 mm), which passes in the lateral wall of the cavernous sinus. The relationship of the ION/V2 complex to the contents of the cavernous sinus, carotid artery, and pterygopalatine fossa is described in the text.

CONCLUSIONS

The ION/V2 complex is an easily identifiable and potentially useful surgical landmark to the foramen rotundum, cavernous sinus, carotid artery, pterygopalatine fossa, and anterolateral skull base during ETMAs.

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Editorial

Cavernous malformations

Issam A. Awad

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In vivo intraoperative confocal microscopy for real-time histopathological imaging of brain tumors

Clinical article

Jennifer Eschbacher, Nikolay L. Martirosyan, Peter Nakaji, Nader Sanai, Mark C. Preul, Kris A. Smith, Stephen W. Coons, and Robert F. Spetzler

Object

Frozen-section analysis is the current standard for the intraoperative diagnosis of brain tumors. Intraoperative confocal microscopy is an emerging technology with the potential to visualize tumor histopathological features and cell morphology in real time. The authors report their findings using this new intraoperative technology in vivo with sodium fluorescein contrast during the course of 50 microsurgical tumor resections.

Methods

Eighty-eight regions were visualized with confocal microscopy, and corresponding biopsy samples were examined with routine neuropathological analysis. The tumors studied included meningiomas, schwannomas, gliomas of various grades, and a hemangioblastoma. The confocal microscopic features of each tumor and of various artifacts inherent to the technology were documented. A pathologist working in a blinded fashion reviewed a subset of the images in a further evaluation of the usefulness of the device as a diagnostic tool.

Results

Overall, intraoperative confocal imaging correlated surprisingly well with corresponding traditional histological findings, including the identification of many pathognomonic cytoarchitectural features of various brain tumors. In the blinded study, 26 (92.9%) of 28 lesions were diagnosed correctly.

Conclusions

Further study will be necessary for better definition of the role of intraoperative confocal microscopy as a routine adjunct for intraoperative brain tumor diagnosis.

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The fate of medical knowledge and the neurosciences during the time of Genghis Khan and the Mongolian Empire

Sam Safavi-Abbasi, Leonardo B. C. Brasiliense, Ryan K. Workman, Melanie C. Talley, Iman Feiz-Erfan, Nicholas Theodore, Robert F. Spetzler, and Mark C. Preul

✓In 25 years, the Mongolian army of Genghis Khan conquered more of the known world than the Roman Empire accomplished in 400 years of conquest. The recent revised view is that Genghis Khan and his descendants brought about “pax Mongolica” by securing trade routes across Eurasia. After the initial shock of destruction by an unknown barbaric tribe, almost every country conquered by the Mongols was transformed by a rise in cultural communication, expanded trade, and advances in civilization. Medicine, including techniques related to surgery and neurological surgery, became one of the many areas of life and culture that the Mongolian Empire influenced.

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Magnetic resonance imaging volumetric assessment of the extent of contrast enhancement and resection in oligodendroglial tumors

Clinical article

Tejas Sankar, Nina Z. Moore, Joshua Johnson, Lynn S. Ashby, Adrienne C. Scheck, William R. Shapiro, Kris A. Smith, Robert F. Spetzler, and Mark C. Preul

Object

Oligodendrogliomas that enhance on MR images are associated with poor prognosis. However, the importance of the volume of enhancing tumor tissue, and the extent of its resection, is uncertain. The authors examined the prognostic significance of preoperative and residual postoperative enhancing tissue volumes in a large single-center series of patients with oligodendroglioma. They also examined the relationship between enhancement and characteristic genetic signatures in oligodendroglial tumors, specifically deletion of 1p and 19q (del 1p/19q).

Methods

The authors retrospectively analyzed 100 consecutive cases of oligodendroglioma involving patients who had undergone T1-weighted gadolinium-enhanced MRI at diagnosis and immediately after initial surgical intervention. The presence of preoperative enhancement was determined by consensus. Preoperative and residual postoperative volumes were measured using a quantitative, semiautomated method by a single blinded observer. Intrarater reliability for preoperative volumes was confirmed by remeasurement in a subset of patients 3 months later. Intrarater and interrater reliability for residual postoperative volumes was confirmed by remeasurement of these volumes by both the original and a second blinded observer. Multivariate analysis was used to assess the influence of contrast enhancement at diagnosis and the volume of pre- and postoperative contrast-enhancing tumor tissue on time to relapse (TTR) and overall survival (OS), while controlling for confounding clinical, pathological, and genetic factors.

Results

Sixty-three of 100 patients had enhancing tumors at initial presentation. Presence of contrast enhancement at diagnosis was related to reduced TTR and OS on univariate analysis but was not significantly related on multivariate analysis. In enhancing tumors, however, greater initial volume of enhancing tissue correlated with shortened TTR (p = 0.00070). Reduced postoperative residual enhancing volume and a relatively greater resection of enhancing tissue correlated with longer OS (p = 0.0012 and 0.0041, respectively). Interestingly, patients in whom 100% of enhancing tumor was resected had significantly longer TTR (174 vs 64 weeks) and OS (392 vs 135 weeks) than those with any residual enhancing tumor postoperatively. This prognostic benefit was not consistently maintained with greater than 90% or even greater than 95% resection of enhancing tissue. There was no relationship between presence or volume of enhancement and del 1p/19q.

Conclusions

In enhancing oligodendrogliomas, completely resecting enhancing tissue independently improves outcome, irrespective of histological grade or genetic status. This finding supports aggressive resection and may impact treatment planning for patients with these tumors.