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Michael T. Lawton and Michael J. Lang

Despite the erosion of microsurgical case volume because of advances in endovascular and radiosurgical therapies, indications remain for open resection of pathology and highly technical vascular repairs. Treatment risk, efficacy, and durability make open microsurgery a preferred option for cerebral cavernous malformations, arteriovenous malformations (AVMs), and many aneurysms. In this paper, a 21-year experience with 7348 cases was reviewed to identify trends in microsurgical management. Brainstem cavernous malformations (227 cases), once considered inoperable and managed conservatively, are now resected in increasing numbers through elegant skull base approaches and newly defined safe entry zones, demonstrating that microsurgical techniques can be applied in ways that generate entirely new areas of practice. Despite excellent results with microsurgery for low-grade AVMs, brain AVM management (836 cases) is being challenged by endovascular embolization and radiosurgery, as well as by randomized trials that show superior results with medical management. Reviews of ARUBA-eligible AVM patients treated at high-volume centers have demonstrated that open microsurgery with AVM resection is still better than many new techniques and less invasive approaches that are occlusive or obliterative. Although the volume of open aneurysm surgery is declining (4479 cases), complex aneurysms still require open microsurgery, often with bypass techniques. Intracranial arterial reconstructions with reimplantations, reanastomoses, in situ bypasses, and intracranial interpositional bypasses (third-generation bypasses) augment conventional extracranial-intracranial techniques (first- and second-generation bypasses) and generate innovative bypasses in deep locations, such as for anterior inferior cerebellar artery aneurysms. When conventional combinations of anastomoses and suturing techniques are reshuffled, a fourth generation of bypasses results, with eight new types of bypasses. Type 4A bypasses use in situ suturing techniques within the conventional anastomosis, whereas type 4B bypasses maintain the basic construct of reimplantations or reanastomoses but use an unconventional anastomosis. Bypass surgery (605 cases) demonstrates that open microsurgery will continue to evolve. The best neurosurgeons will be needed to tackle the complex lesions that cannot be managed with other modalities. Becoming an open vascular neurosurgeon will be intensely competitive. The microvascular practice of the future will require subspecialization, collaborative team effort, an academic medical center, regional prominence, and a large catchment population, as well as a health system that funnels patients from hospital networks outside the region. Dexterity and meticulous application of microsurgical technique will remain the fundamental skills of the open vascular neurosurgeon.

Free access

Jacob F. Baranoski, Ankush Bajaj, Colin J. Przybylowski, Joshua S. Catapano, Fabio A. Frisoli, Michael J. Lang, and Michael T. Lawton

Supracerebellar transtentorial (SCTT) approaches have become a popular option for treatment of a variety of pathologies in the medial and basal temporal and occipital lobes and thalamus. Transtentorial approaches provide numerous advantages over transcortical approaches, including obviating the need to traverse eloquent cortex, not requiring parenchymal retraction, and circumventing critical vascular structures. All of these approaches require a tentorial opening, and numerous techniques for retraction of the incised tentorium have been described, including sutures, fixed retractors, and electrocautery. However, all of these techniques have considerable drawbacks and limitations. The authors describe a novel application of clip retraction of the tentorium to the supracerebellar approaches in which an aneurysm clip is used to suspend the tentorial flap, and an illustrative case is provided. Clip retraction of the tentorium is an efficient, straightforward adaptation of an established technique, typically used for subtemporal approaches, that improves visualization and surgical ergonomics with little risk to nearby venous structures. The authors find this technique particularly useful for the contralateral SCTT approaches.

Restricted access

Ali Tayebi Meybodi, Michael T. Lawton, Leandro Borba Moreira, Xiaochun Zhao, Michael J. Lang, Peter Nakaji, and Mark C. Preul

OBJECTIVE

Harvesting the occipital artery (OA) is challenging. The subcutaneous OA is usually found near the superior nuchal line and followed proximally, requiring a large incision and risking damage to the superficially located OA. The authors assessed the anatomical feasibility and safety of exposing the OA through a retromastoid-transmuscular approach.

METHODS

Using 10 cadaveric heads, 20 OAs were harvested though a 5-cm retroauricular incision placed 5 cm posterior to the external auditory meatus. The underlying muscle layers were sequentially cut and recorded before exposing the OA. Changes in the orientation of muscle fibers were used as a roadmap to expose the OA without damaging it.

RESULTS

The suboccipital segment of the OA was exposed without damage after incising two consecutive layers of muscles and their investing fasciae. These muscles displayed different fiber directions: the superficially located sternocleidomastoid muscle with vertically oriented fibers, and the underlying splenius capitis with anteroposteriorly (and mediolaterally) oriented fibers. The OA could be harvested along the entire length of the skin incision in all specimens. If needed, the incision can be extended proximally and/or distally to follow the OA and harvest greater lengths.

CONCLUSIONS

This transmuscular technique for identification of the OA is a reliable method and may facilitate exposure and protection of the OA during a retrosigmoid approach. This technique may obviate the need for larger incisions when planning a bypass to nearby arteries in the posterior circulation via a retrosigmoid craniotomy. Additionally, the small skin incision can be enlarged when a different craniotomy and/or bypass is planned or when a greater length of the OA is needed to be harvested.

Open access

Sirin Gandhi, Tsinsue Chen, Justin R. Mascitelli, Claudio Cavallo, Mohamed A. Labib, Michael J. Lang, and Michael T. Lawton

This video illustrates a contralateral supracerebellar transtentorial (cSCTT) approach for resection of a ruptured thalamic cavernous malformation in a 56-year-old woman with progressive right-sided homonymous hemianopsia. The patient was placed in the sitting position, and a torcular craniotomy was performed for the cSCTT approach. The lesion was resected completely. Postoperatively, the patient had intact motor strength and baseline visual field deficits with moderate right-sided paresthesias. The cSCTT approach maximizes the lateral surgical reach without the cortical transgression seen with alternative transcortical routes. Contralaterality is a defining feature, with entry of the neurosurgeon’s instruments from the craniotomy edge of the craniotomy, contralateral to the lesion, allowing access to the lateral aspect of the lesion. The sitting position facilitates gravity-assisted cerebellar retraction and enhances the superior reach of this approach (Used with permission from Barrow Neurological Institute, Phoenix, Arizona).

The video can be found here: https://youtu.be/lqB9mu_T8NQ.

Free access

Michael Opoku-Darko, Stefan T. Lang, James Artindale, J. Gregory Cairncross, Robert J. Sevick, and John J. P. Kelly

OBJECTIVE

Occasionally, diffusely infiltrating low-grade gliomas (LGGs) are identified as incidental findings in patients who have no signs or symptoms that can be ascribed to the tumors. The diagnosis of incidental, asymptomatic LGGs has become more frequent due to the vast increase in access to medical imaging technology. While management of these lesions remains controversial, early surgery has been suggested to improve outcome. The authors set out to identify and review the characteristics and surgical outcomes of patients who underwent surgical intervention for incidental LGG.

METHODS

All cases of LGG surgically treated between 2004 and 2016 at the authors’ institution were analyzed to identify those that were discovered incidentally. Patients with incidentally discovered LGGs were identified, and their cases were retrospectively reviewed. An “incidental” finding was defined as an abnormality on imaging that was obtained for a reason not attributable to the glioma, such as trauma, headache, screening, or research participation. Kaplan-Meier analysis was performed to determine actuarial rates of overall survival, progression-free survival, and malignant progression–free survival.

RESULTS

In 34 (6.8%) of 501 adult patients who underwent surgery for LGG, the tumors were discovered incidentally. Headache (26%, n = 9) and screening (21%, n = 7) were the most common indications for brain imaging in this group. Four of these 34 patients had initial biopsy after the tumor was identified on imaging. In 5 cases, the patients opted for immediate resection; the remaining cases were managed with a “watch-and-wait” approach, with intervention undertaken only after radiological or clinical evidence of disease progression. The mean duration of follow-up for all 34 cases was 5 years. Twelve patients (35.3%) had disease progression, with an average time to progression of 43.8 months (range 3–105 months). There were 5 cases (14.7%) of malignant progression and 4 deaths (11.8%). Oligodendroglioma was diagnosed in 16 cases (47%) and astrocytoma in 15 (44%). Twenty-five patients (74%) had IDH1 mutation and demonstrated prolonged survival. Only 2 patients had mild surgery-related complications, and 16 patients (47%) developed epilepsy during the course of the disease.

CONCLUSIONS

In this retrospective analysis of cases of incidentally discovered LGGs, the tumors were surgically removed with minimal surgical risk. In patients with incidental LGGs there is improved overall survival relative to median survival for patients with symptomatic LGGS, which is likely attributable to the underlying favorable biology of the disease indicated by the presence of IDH1 mutation in 74% of the cases.

Restricted access

Chul Han, Michael J. Lang, Candice L. Nguyen, Ernesto Luna Melendez, Shwetal Mehta, Gregory H. Turner, Michael T. Lawton, and S. Paul Oh

OBJECTIVE

Hereditary hemorrhagic telangiectasia is the only condition associated with multiple inherited brain arteriovenous malformations (AVMs). Therefore, a mouse model was developed with a genetics-based approach that conditionally deleted the causative activin receptor-like kinase 1 (Acvrl1 or Alk1) gene. Radiographic and histopathological findings were correlated, and AVM stability and hemorrhagic behavior over time were examined.

METHODS

Alk1-floxed mice were crossed with deleter mice to generate offspring in which both copies of the Alk1 gene were deleted by Tagln-Cre to form brain AVMs in the mice. AVMs were characterized using MRI, MRA, and DSA. Brain AVMs were characterized histopathologically with latex dye perfusion, immunofluorescence, and Prussian blue staining.

RESULTS

Brains of 55 Tagln-Cre+;Alk1 f/f mutant mice were categorized into three groups: no detectable vascular lesions (group 1; 23 of 55, 42%), arteriovenous fistulas (AVFs) with no nidus (group 2; 10 of 55, 18%), and nidal AVMs (group 3; 22 of 55, 40%). Microhemorrhage was observed on MRI or MRA in 11 AVMs (50%). AVMs had the angiographic hallmarks of early nidus opacification, a tangle of arteries and dilated draining veins, and rapid shunting of blood flow. Latex dye perfusion confirmed arteriovenous shunting in all AVMs and AVFs. Microhemorrhages were detected adjacent to AVFs and AVMs, visualized by iron deposition, Prussian blue staining, and macrophage infiltration using CD68 immunostaining. Brain AVMs were stable on serial MRI and MRA in group 3 mice (mean age at initial imaging 2.9 months; mean age at last imaging 9.5 months).

CONCLUSIONS

Approximately 40% of transgenic mice satisfied the requirements of a stable experimental AVM model by replicating nidal anatomy, arteriovenous hemodynamics, and microhemorrhagic behavior. Transgenic mice with AVFs had a recognizable phenotype of hereditary hemorrhagic telangiectasia but were less suitable for experimental modeling. AVM pathogenesis can be understood as the combination of conditional Alk1 gene deletion during embryogenesis and angiogenesis that is hyperactive in developing and newborn mice, which translates to a congenital origin in most patients but an acquired condition in patients with a confluence of genetic and angiogenic events later in life. This study offers a novel experimental brain AVM model for future studies of AVM pathophysiology, growth, rupture, and therapeutic regression.

Free access

Roberta K. Sefcik, Daniel A. Tonetti, Shashvat M. Desai, Stephanie M. Casillo, Michael J. Lang, Ashutosh P. Jadhav, and Bradley A. Gross

OBJECTIVE

Acute basilar artery occlusion (BAO) harbors a more guarded prognosis after thrombectomy compared with anterior circulation large-vessel occlusion. Whether this is a function of a greater proportion of atherosclerotic/intrinsic lesions is not well studied. The authors aimed to elucidate the prevalence and predictors of intracranial intrinsic atherosclerotic disease in patients with acute BAO and to compare angiographic and clinical outcomes between patients with BAO secondary to embolic versus intrinsic disease.

METHODS

A prospectively maintained stroke database was reviewed for all patients presenting between January 2013 and December 2019 to a tertiary care academic comprehensive stroke center with acute, nontandem BAO. Patient data were extracted, subdivided by stroke mechanism and treatment modality (embolic [thrombectomy only] and intrinsic [thrombectomy + stenting]), and angiographic and clinical results were compared.

RESULTS

Of 107 patients, 83 (78%) had embolic occlusions (thrombectomy only) and 24 (22%) had intrinsic disease (thrombectomy + stenting). There was no significant difference in patient age, presenting National Institutes of Health Stroke Scale score, time to presentation, selected medical comorbidities (hypertension, hyperlipidemia, diabetes, and atrial fibrillation), prior stroke, and posterior circulation Alberta Stroke Program Early CT Score. Patients with intrinsic disease were more likely to be active smokers (50% vs 26%, p = 0.04) and more likely to be male (88% vs 48%, p = 0.001). Successful recanalization, defined as a modified Thrombolysis in Cerebral Infarction (mTICI) grade of 2b or 3, was achieved in 90% of patients and did not differ significantly between the embolic versus intrinsic groups (89% vs 92%, p > 0.99). A 90-day good outcome (modified Rankin Scale [mRS] score 0–2) was found in 37% of patients overall and did not differ significantly between the two groups (36% vs 41%, p = 0.41). Mortality was 40% overall and did not significantly differ between groups (41% vs 36%, p = 0.45).

CONCLUSIONS

In the current study, demographic and clinical results for acute BAO showed that compared with intrinsic disease, thromboembolic disease is a more common mechanism of acute BAO, with 78% of patients undergoing thrombectomy alone. However, there was no significant difference in revascularization and outcome results between patients with embolic disease and those with intrinsic disease.

Free access

Peyton L. Nisson, Salman A. Fard, Christina M. Walter, Cameron M. Johnstone, Michael A. Mooney, Ali Tayebi Meybodi, Michael Lang, Helen Kim, Heidi Jahnke, Denise J. Roe, Travis M. Dumont, G. Michael Lemole Jr., Robert F. Spetzler, and Michael T. Lawton

OBJECTIVE

The objective of this study was to evaluate the existing Spetzler-Martin (SM), Spetzler-Ponce (SP), and Lawton-Young (LY) grading systems for cerebellar arteriovenous malformations (AVMs) and to propose a new grading system to estimate the risks associated with these lesions.

METHODS

Data for patients with cerebellar AVMs treated microsurgically in two tertiary medical centers were retrospectively reviewed. Data from patients at institution 1 were collected from September 1999 to February 2013, and at institution 2 from October 2008 to October 2015. Patient outcomes were classified as favorable (modified Rankin Scale [mRS] score 0–2) or poor (mRS score 3–6) at the time of discharge. Using chi-square and logistic regression analysis, variables associated with poor outcomes were assigned risk points to design the proposed grading system. The proposed system included neurological status prior to treatment (poor, +2 points), emergency surgery (+1 point), age > 60 years (+1 point), and deep venous drainage (deep, +1 point). Risk point totals of 0–1 comprised grade 1, 2–3 grade 2, and 4–5 grade 3.

RESULTS

A total of 125 cerebellar AVMs of 1328 brain AVMs were reviewed in 125 patients, 120 of which were treated microsurgically and included in the study. With our proposed grading system, we found poor outcomes differed significantly between each grade (p < 0.001), while with the SM, SP, and LY grading systems they did not (p = 0.22, p = 0.25, and p = 1, respectively). Logistic regression revealed grade 2 had 3.3 times the risk of experiencing a poor outcome (p = 0.008), while grade 3 had 9.9 times the risk (p < 0.001). The proposed grading system demonstrated a superior level of predictive accuracy (area under the receiver operating characteristic curve [AUROC] of 0.72) compared with the SM, SP, and LY grading systems (AUROC of 0.61, 0.57, and 0.51, respectively).

CONCLUSIONS

The authors propose a novel grading system for cerebellar AVMs based on emergency surgery, venous drainage, preoperative neurological status, and age that provides a superior prognostication power than the formerly proposed SM, SP, and LY grading systems. This grading system is clinically predictive of patient outcomes and can be used to better guide vascular neurosurgeons in clinical decision-making.

Restricted access

Carrie E. Andrews, Nikolaos Mouchtouris, Evan M. Fitchett, Fadi Al Saiegh, Michael J. Lang, Victor M. Romo, Nabeel Herial, Pascal Jabbour, Stavropoula I. Tjoumakaris, Robert H. Rosenwasser, and M. Reid Gooch

OBJECTIVE

Mechanical thrombectomy (MT) is now the standard of care for acute ischemic stroke (AIS) secondary to large-vessel occlusion, but there remains a question of whether elderly patients benefit from this procedure to the same degree as the younger populations enrolled in the seminal trials on MT. The authors compared outcomes after MT of patients 80–89 and ≥ 90 years old with AIS to those of younger patients.

METHODS

The authors retrospectively analyzed records of patients undergoing MT at their institution to examine stroke severity, comorbid conditions, medical management, recanalization results, and clinical outcomes. Univariate and multivariate logistic regression analysis were used to compare patients < 80 years, 80–89 years, and ≥ 90 years old.

RESULTS

All groups had similar rates of comorbid disease and tissue plasminogen activator (tPA) administration, and stroke severity did not differ significantly between groups. Elderly patients had equivalent recanalization outcomes, with similar rates of readmission, 30-day mortality, and hospital-associated complications. These patients were more likely to have poor clinical outcome on discharge, as defined by a modified Rankin Scale (mRS) score of 3–6, but this difference was not significant when controlled for stroke severity, tPA administration, and recanalization results.

CONCLUSIONS

Octogenarians, nonagenarians, and centenarians with AIS have similar rates of mortality, hospital readmission, and hospital-associated complications as younger patients after MT. Elderly patients also have the capacity to achieve good functional outcome after MT, but this potential is moderated by stroke severity and success of treatment.

Restricted access

Nikolaos Mouchtouris, Michael J. Lang, Kaitlyn Barkley, Guilherme Barros, Justin Turpin, Ahmad Sweid, Robert M. Starke, Nohra Chalouhi, Pascal Jabbour, Robert H. Rosenwasser, and Stavropoula Tjoumakaris

OBJECTIVE

The authors sought to determine the predictors of late neurological and hospital-acquired medical complications (HACs) in patients with low-grade aneurysmal subarachnoid hemorrhage (aSAH).

METHODS

The authors conducted a retrospective study of 424 patients with low-grade aSAH admitted to their institution from 2008 to 2015. Data collected included patient comorbidities, Hunt and Hess (HH) grade, ICU length of stay (LOS), and complications. A logistic regression analysis was performed to determine the predictors for neurological and hospital-associated complications.

RESULTS

Out of 424 patients, 50 (11.8%) developed neurological complications after the first week, with a mean ICU stay of 16.3 ± 6.5 days. Of the remaining 374 patients without late neurological complications, 83 (22.2%) developed late HACs with a mean LOS of 15.1 ± 7.6 days, while those without medical complications stayed 11.8 ± 6.2 days (p = 0.001). Of the 83 patients, 55 (66.3%) did not have any HACs in the first week. Smoking (p = 0.062), history of cardiac disease (p = 0.043), HH grade III (p = 0.012), intraventricular hemorrhage (IVH) (p = 0.012), external ventricular drain (EVD) placement (p = 0.002), and early pneumonia/urinary tract infection (UTI)/deep vein thrombosis (DVT) (p = 0.001) were independently associated with late HACs. Logistic regression showed early pneumonia/UTI/DVT (p = 0.026) and increased HH grade (p = 0.057) to be significant risk factors for late medical complications.

CONCLUSIONS

While an extended ICU admission allows closer monitoring, low-grade aSAH patients develop HACs despite being at low risk for neurological complications. The characteristics of low-grade aSAH patients who would benefit from early discharge are reported in detail.