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Jan-Karl Burkhardt, Ethan A. Winkler, and Michael T. Lawton

OBJECTIVE

Deep medial parietooccipital arteriovenous malformations (AVMs) and cerebral cavernous malformations (CCMs) are traditionally resected through an ipsilateral posterior interhemispheric approach (IPIA), which creates a deep, perpendicular perspective with limited access to the lateral margins of the lesion. The contralateral posterior interhemispheric approach (CPIA) flips the positioning, with the midline positioned horizontally for retraction due to gravity, but with the AVM on the upper side and the approach from the contralateral, lower side. The aim of this paper was to analyze whether the perpendicular angle of attack that is used in IPIA would convert to a parallel angle of attack with the CPIA, with less retraction, improved working angles, and no significant increase in risk.

METHODS

A retrospective review of pre- and postoperative clinical and radiographic data was performed in 8 patients who underwent a CPIA.

RESULTS

Three AVMs and 5 CCMs were resected using the CPIA, with an average nidus size of 2.3 cm and CCM diameter of 1.7 cm. All lesions were resected completely, as confirmed on postoperative catheter angiography or MRI. All patients had good neurological outcomes, with either stable or improved modified Rankin Scale scores at last follow-up.

CONCLUSIONS

The CPIA is a safe alternative approach to the IPIA for deep medial parietooccipital vascular malformations that extend 2 cm or more off the midline. Contralaterality and retraction due to gravity optimize the interhemispheric corridor, the surgical trajectory to the lesion, and the visualization of the lateral margin, without resection or retraction of adjacent normal cortex. Although the falx is a physical barrier to accessing the lesion, it stabilizes the ipsilateral hemisphere while gravity delivers the dissected lesion through the transfalcine window. Patient positioning, CSF drainage, venous preservation, and meticulous dissection of the deep margins are critical to the safety of this approach.

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Michael M. Safaee, Aaron J. Clark, Jan-Karl Burkhardt, Ethan A. Winkler, and Michael T. Lawton

OBJECTIVE

Spinal dural arteriovenous fistulas (dAVFs) are rare vascular abnormalities caused by arteriovenous shunting. They often form at the dural root sleeve between a radicular feeding artery and draining medullary vein causing venous congestion and edema, decreased perfusion, and ischemia of the spinal cord. Treatment consists of either surgical ligation of the draining vein or selective embolization via an endovascular approach. There is a paucity of data on which modality provides more durable and effective outcomes.

METHODS

The authors performed a retrospective review of a prospectively maintained database by the senior author to assess clinical outcomes in patients undergoing surgical treatment of spinal dAVFs. Preoperative and postoperative motor and Aminoff-Logue Scale (ALS) scores were collected.

RESULTS

A total of 41 patients with 44 spinal dAVFs were identified, with a mean patient age of 64 years. The mean symptom duration was 14 months, with weakness (82%), urinary symptoms (47%), and sensory symptoms (29%) at presentation. The fistula locations were as follows: 30 thoracic, 9 lumbar, 3 sacral, and 2 cervical. Five patients had normal motor and ALS scores at presentation. Among the remaining 36 patients with motor deficits or abnormal gait and micturition at presentation, 78% experienced an improvement while the remaining 22% continued to be stable. There was a trend toward improved outcomes in patients with shorter symptom duration; mean symptom duration among patients with clinical improvement was 13 months compared with 22 months among those without improvement. Additionally, rates of improvement were higher for lower thoracic and lumbosacral dAVFs (85% and 83%) compared with those in the upper thoracic spine (57%). No patient developed recurrent fistulas or worsening neurological deficits.

CONCLUSIONS

Surgery is associated with excellent outcomes in the treatment of spinal dAVFs. Early diagnosis and treatment are critical, with a trend toward improved outcomes. No patient in this study had fistula recurrence or worsening of symptoms. Among patients with abnormal motor or ALS scores, 78% improved after surgery. Therapeutic embolization is an option for some lesions, but for cases with unfavorable anatomy where embolization is not feasible, surgery is a safe option associated with high success.

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Jan-Karl Burkhardt, Ethan A. Winkler, George F. Lasker, John K. Yue, and Michael T. Lawton

OBJECTIVE

Compressive cranial nerve syndromes can be useful bedside clues to the diagnosis of an enlarging intracranial aneurysm and can also guide subsequent evaluation, as with an acute oculomotor nerve (cranial nerve [CN] III) palsy that is presumed to be a posterior communicating artery aneurysm and a surgical emergency until proven otherwise. The CN VI has a short cisternal segment from the pontomedullary sulcus to Dorello’s canal, remote from most PICA aneurysms but in the hemodynamic pathway of a rupturing PICA aneurysm that projects toward Dorello’s canal. The authors describe a cranial nerve syndrome for posterior inferior cerebellar artery (PICA) aneurysms that associates subarachnoid hemorrhage (SAH) and an isolated abducens nerve (CN VI) palsy.

METHODS

Clinical and radiological data from 106 surgical patients with PICA aneurysms (66 ruptured and 40 unruptured) were retrospectively reviewed. Data from a group of 174 patients with other aneurysmal SAH (aSAH) were analyzed in a similar manner to control for nonspecific effects of SAH. Univariate statistical analysis compared incidence and risk factors associated with CN VI palsy in subarachnoid hemorrhage.

RESULTS

Overall, 13 (4.6%) of 280 patients had CN VI palsy at presentation, and all of them had ruptured aneurysms (representing 13 [5.4%] of the 240 cases of ruptured aneurysms). CN VI palsies were observed in 12 patients with ruptured PICA aneurysms (12/66 [18.1%]) and 1 patient with other aSAH (1/174 [0.1%], p < 0.0001). PICA aneurysm location in ruptured aneurysms was an independent predictor for CN VI palsy on multivariate analysis (p = 0.001). PICA aneurysm size was not significantly different in patients with or without CN VI palsy (average size 4.4 mm and 5.2 mm, respectively). Within the PICA aneurysm cohort, modified Fisher grade (p = 0.011) and presence of a thick cisternal SAH (modified Fisher Grades 3 and 4) (p = 0.003) were predictors of CN VI palsy. In all patients with ruptured PICA aneurysms and CN VI palsy, dome projection and presumed direction of rupture were directed toward the ipsilateral and/or contralateral Dorello’s canal, in agreement with laterality of the CN palsy. In patients with bilateral CN VI palsies, a medial projection with extensive subarachnoid blood was observed near bilateral canals.

CONCLUSIONS

This study establishes a localizing connection between an isolated CN VI palsy, SAH, and an underlying ruptured PICA aneurysm. CN VI palsy is an important clinical sign in aSAH and when present on initial clinical presentation may be assumed to be due to ruptured PICA aneurysms until proven otherwise. The deficit may be ipsilateral, contralateral, or bilateral and is determined by the direction of the aneurysm dome projection and extent of subarachnoid bleeding toward Dorello’s canal, rather than by direct compression.

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Jan-Karl Burkhardt, Ethan A. Winkler, Joshua S. Catapano, Robert F. Spetzler, and Michael T. Lawton

OBJECTIVE

Studies of resection of brain arteriovenous malformations (AVMs) in the elderly population are scarce. This study examined factors influencing patient selection and surgical outcome among elderly patients.

METHODS

Patients 65 years of age and older who underwent resection of an unruptured or ruptured brain AVM treated by two surgeons at two centers were identified. Patient demographic characteristics, AVM characteristics, clinical presentation, and outcomes measured using the modified Rankin Scale (mRS) were analyzed. For subgroup analyses, patients were dichotomized into two age groups (group 1, 65–69 years old; group 2, ≥ 70 years old).

RESULTS

Overall, 112 patients were included in this study (group 1, n = 61; group 2, n = 51). Most of the patients presented with hemorrhage (71%), a small nidus (< 3 cm, 79%), and a low Spetzler-Martin (SM) grade (grade I or II, 63%) and were favorable surgical candidates according to the supplemented SM grade (supplemented SM grade < 7, 79%). A smaller AVM nidus was statistically significantly more likely to be present in patients with infratentorial AVMs (p = 0.006) and with a compact AVM nidus structure (p = 0.02). A larger AVM nidus was more likely to be treated with preoperative embolization (p < 0.001). Overall outcome was favorable (mRS scores 0–3) in 71% of the patients and was statistically independent from age group or AVM grading. Patients with ruptured AVMs at presentation had significantly better preoperative mRS scores (p < 0.001) and more favorable mRS scores at the last follow-up (p = 0.04) than patients with unruptured AVMs.

CONCLUSIONS

Outcomes were favorable after AVM resection in both groups of patients. Elderly patients with brain AVMs treated microsurgically were notable for small nidus size, AVM rupture, and low SM grades. Microsurgical resection is an important treatment modality for elderly patients with AVMs, and supplemented SM grading is a useful tool for the selection of patients who are most likely to achieve good neurological outcomes after resection.

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Jan-Karl Burkhardt, Michelle H. Chua, Ethan A. Winkler, W. Caleb Rutledge, and Michael T. Lawton

OBJECTIVE

During the microsurgical clipping of known aneurysms, angiographically occult (AO) aneurysms are sometimes found and treated simultaneously to prevent their growth and protect the patient from future rupture or reoperation. The authors analyzed the incidence, treatment, and outcomes associated with AO aneurysms to determine whether limited surgical exploration around the known aneurysm was safe and justified given the known limitations of diagnostic angiography.

METHODS

An AO aneurysm was defined as a saccular aneurysm detected using the operative microscope during dissection of a known aneurysm, and not detected on preoperative catheter angiography. A prospective database was retrospectively reviewed to identify patients with AO aneurysms treated microsurgically over a 20-year period.

RESULTS

One hundred fifteen AO aneurysms (4.0%) were identified during 2867 distinct craniotomies for aneurysm clipping. The most common locations for AO aneurysms were the middle cerebral artery (60 aneurysms, 54.1%) and the anterior cerebral artery (20 aneurysms, 18.0%). Fifty-six AO aneurysms (50.5%) were located on the same artery as the known saccular aneurysm. Most AO aneurysms (95.5%) were clipped and there was no attributed morbidity. The most common causes of failed angiographic detection were superimposition of a large aneurysm (type 1, 30.6%), a small aneurysm (type 2, 18.9%), or an adjacent normal artery (type 3, 36.9%). Multivariate analysis identified multiple known aneurysms (odds ratio [OR] 3.45, 95% confidence interval [CI] 2.16–5.49, p < 0.0001) and young age (OR 0.981, 95% CI 0.965–0.997, p = 0.0226) as independent predictors of AO aneurysms.

CONCLUSIONS

Meticulous inspection of common aneurysm sites within the surgical field will identify AO aneurysms during microsurgical dissection of another known aneurysm. Simultaneous identification and treatment of these additional undiagnosed aneurysms can spare patients later rupture or reoperation, particularly in those with multiple known aneurysms and a history of subarachnoid hemorrhage. Limited microsurgical exploration around a known aneurysm can be performed safely without additional morbidity.

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Jan-Karl Burkhardt, George F. Lasker, Ethan A. Winkler, Helen Kim, and Michael T. Lawton

OBJECTIVE

Few outcomes studies have been published on microsurgical resection of arteriovenous malformations (AVMs) in elderly patients, and most are limited by a small sample size and the heterogeneous application of treatment modalities. This study aimed to determine whether functional outcomes at last follow-up (LFU) in patients 60 years or older differed when stratified by age.

METHODS

Patients 60 years or older (n = 104) who had undergone microsurgical AVM resection (total, n = 72; 60–65 years, n = 35; and > 65 years, n = 37) or observation (n = 32) were identified from a prospective database. Age, sex, Spetzler-Martin (SM) grade, supplemented SM grade, clinical presentation, AVM location, AVM-associated aneurysms, and functional outcome measured using the modified Rankin Scale (mRS score 0–2 [favorable] vs mRS score > 2 [unfavorable]) at LFU were analyzed.

RESULTS

AVM patients undergoing microsurgical resection were younger, had lower AVM grades, and were more likely to present with rupture. Overall outcome in the surgical group was favorable in 71% of the patients and was statistically significantly better in patients 60–65 years old (p = 0.039). In patients older than 65 years, outcome was dependent on SM grade and level of preexisting functional dependence. Patients with supplemented SM grades of greater than 6 points had favorable outcomes that were age dependent (p = 0.029). This difference was not observed in patients with lower supplemented SM grades or in those with low or high preoperative SM grades (SM grade ≤ 2 and grade ≥ 4, respectively).

CONCLUSIONS

This study demonstrates that favorable outcomes can be achieved with microsurgical resection of AVMs in elderly patients, with careful patient selection. Outcomes in more elderly patients (> 65 years of age) are more dependent on preoperative SM and supplemented SM grading than those in younger cohorts.

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Ethan A. Winkler, Jan-Karl Burkhardt, W. Caleb Rutledge, Jonathan W. Rick, Carlene P. Partow, John K. Yue, Harjus Birk, Ashley M. Bach, Kunal P. Raygor, and Michael T. Lawton

OBJECTIVE

Shunt-dependent hydrocephalus is an important cause of morbidity following aneurysmal subarachnoid hemorrhage (aSAH) in excess of 20% of cases. Hydrocephalus leads to prolonged hospital and ICU stays, well as to repeated surgical interventions, readmissions, and complications associated with ventriculoperitoneal (VP) shunts, including shunt failure and infection. Whether variations in surgical technique at the time of aneurysm treatment may modify rates of shunt dependency remains a matter of debate. Here, the authors report on their experience with tandem fenestration of the lamina terminalis (LT) and membrane of Liliequist (MoL) at the time of open microsurgical repair of the ruptured aneurysm.

METHODS

The authors conducted a retrospective review of 663 consecutive patients with aSAH treated from 2005 to 2015 by open microsurgery via a pterional or orbitozygomatic craniotomy by the senior author (M.T.L.). Data collected from review of the electronic medical record included age, Hunt and Hess grade, Fisher grade, need for an external ventricular drain, and opening pressure. Patients were stratified into those undergoing no fenestration and those undergoing tandem fenestration of the LT and MoL at the time of surgical repair. Outcome variables, including VP shunt placement and timing of shunt placement, were recorded and statistically analyzed.

RESULTS

In total, shunt-dependent hydrocephalus was observed in 15.8% of patients undergoing open surgical repair following aSAH. Tandem microsurgical fenestration of the LT and MoL was associated with a statistically significant reduction in shunt dependency (17.9% vs 3.2%, p < 0.01). This effect was confirmed with multivariate analysis of collected variables (multivariate OR 0.09, 95% CI 0.03–0.30). Number-needed-to-treat analysis demonstrated that tandem fenestration was required in approximately 6.8 patients to prevent a single VP shunt placement. A statistically significant prolongation in days to VP shunt surgery was also observed in patients treated with tandem fenestration (26.6 ± 19.4 days vs 54.0 ± 36.5 days, p < 0.05).

CONCLUSIONS

Tandem fenestration of the LT and MoL at the time of open microsurgical clipping and/or bypass to secure ruptured anterior and posterior circulation aneurysms is associated with reductions in shunt-dependent hydrocephalus following aSAH. Future prospective randomized multicenter studies are needed to confirm this result.

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Davis G. Taylor, Ching-Jen Chen, Thomas J. Buell, Min S. Park, J. Javier Provencio, and M. Yashar S. Kalani

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Joseph H. Garcia, Ramin A. Morshed, Ethan A. Winkler, Yi Li, Christine K. Fox, Heather J. Fullerton, Caleb Rutledge, Angad S. Beniwal, Michael T. Lawton, Adib A. Abla, Nalin Gupta, and Steven W. Hetts

OBJECTIVE

Moyamoya is a progressive arteriopathy that predisposes patients to stroke due to stenosis of the intracranial internal carotid arteries and their proximal branches. Despite the morbidity caused by this condition, the ability to accurately predict prognosis for individual patients remains challenging. The goal of this study was to develop a systematic scoring method based on parenchymal findings on preoperative brain MRI to predict long-term outcomes for surgically treated pediatric patients with moyamoya.

METHODS

A retrospective surgical cohort of pediatric patients (≤ 18 years of age at the time of the initial surgery) with moyamoya from a single center were studied. Radiological variables with existing correlations between outcomes in moyamoya or other vascular diseases were chosen to score preoperative MRI based on easily defined parenchymal findings that could be rapidly assessed and used to make a numeric score. Calculated scores were correlated with clinical outcome measures using the Pearson correlation coefficient and area under the receiver operating characteristic curve (AUROC).

RESULTS

A total of 35 children with moyamoya disease or moyamoya syndrome were included in the study, with a median follow-up time of 2.6 years from the time of surgery. The pediatric moyamoya MRI score (PMMS) consists of ischemic changes (0–2; 0 = none, 1 = focal, 2 = diffuse), encephalomalacia (0–2; 0 = none, 1 = focal, 2 = diffuse), and hemorrhage (0–1; 0 = not present, 1 = present). PMMSs were highly correlated with pediatric modified Rankin Scale scores at the last follow-up (r = 0.7, 95% CI 0.44–0.84; p < 0.001) as a six-point scale, and when dichotomized (AUROC = 0.85).

CONCLUSIONS

The PMMS was found to be a simple tool based on preoperative MRI data that could be quickly and easily calculated and correlated with disability. This scoring method may aid future development of predictive models of outcomes for children with moyamoya disease and moyamoya syndrome.