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Yan Michael Li, Dima Suki, Kenneth Hess and Raymond Sawaya

OBJECT

Glioblastoma multiforme (GBM) is the most common and deadliest primary brain tumor. The value of extent of resection (EOR) in improving survival in patients with GBM has been repeatedly confirmed, with more extensive resections providing added advantages. The authors reviewed the survival of patients with significant EORs and assessed the relative benefit/risk of resecting 100% of the MRI region showing contrast-enhancement with or without additional resection of the surrounding FLAIR abnormality region, and they assessed the relative benefit/risk of performing this additional resection.

METHODS

The study cohort included 1229 patients with histologically verified GBM in whom ≥ 78% resection was achieved at The University of Texas MD Anderson Cancer Center between June 1993 and December 2012. Patients with > 1 tumor and those 80 years old or older were excluded. The survival of patients having 100% removal of the contrast-enhancing tumor, with or without additional resection of the surrounding FLAIR abnormality region, was compared with that of patients undergoing 78% to < 100% EOR of the enhancing mass. Within the first subgroup, the survival durations of patients with and without resection of the surrounding FLAIR abnormality were subsequently compared. The data on patients and their tumor characteristics were collected prospectively. The incidence of 30-day postoperative complications (overall and neurological) was noted.

RESULTS

Complete resection of the T1 contrast-enhancing tumor volume was achieved in 876 patients (71%). The median survival time for these patients (15.2 months) was significantly longer than that for patients undergoing less than complete resection (9.8 months; p < 0.001). This survival advantage was achieved without an increase in the risk of overall or neurological postoperative deficits and after correcting for established prognostic factors including age, Karnofsky Performance Scale score, preoperative contrast-enhancing tumor volume, presence of cyst, and prior treatment status (HR 1.53, 95% CI 1.33–1.77, p < 0.001). The effect remained essentially unchanged when data from previously treated and previously untreated groups of patients were analyzed separately. Additional analyses showed that the resection of ≥ 53.21% of the surrounding FLAIR abnormality beyond the 100% contrast-enhancing resection was associated with a significant prolongation of survival compared with that following less extensive resections (median survival times 20.7 and 15.5 months, respectively; p < 0.001). In the multivariate analysis, the previously treated group with < 53.21% resection had significantly shorter survival than the 3 other groups (that is, previously treated patients who underwent FLAIR resection ≥ 53.21%, previously untreated patients who underwent FLAIR resection < 53.21%, and previously untreated patients who underwent FLAIR resection ≥ 53.21%); the previously untreated group with ≥ 53.21% resection had the longest survival.

CONCLUSIONS

What is believed to be the largest single-center series of GBM patients with extensive tumor resections, this study supports the established association between EOR and survival and presents additional data that pushing the boundary of a conventional 100% resection by the additional removal of a significant portion of the FLAIR abnormality region, when safely feasible, may result in the prolongation of survival without significant increases in overall or neurological postoperative morbidity. Additional supportive evidence is warranted.

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Editorial

Neurosurgical “pearls” and neurosurgical evidence

E. Antonio Chiocca

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Benjamin D. Fox, Akash Patel, Dima Suki and Ganesh Rao

Object

Metastatic sarcoma to the brain is rare and represents a therapeutic challenge due to its relative resistance to radio- and chemotherapy. Resection has traditionally been the mainstay of treatment. The authors reviewed a series of patients with metastatic sarcoma to the brain treated surgically to determine outcomes and identify predictors of survival in these patients.

Methods

A retrospective review of prospectively collected data was undertaken on patients undergoing surgery between 1993 and 2005 for metastatic sarcoma to the brain at The University of Texas, M.D. Anderson Cancer Center.

Results

During the study period, 62 patients underwent 84 operations for metastatic sarcoma to the brain. The median postoperative overall and progression-free survival rates were 7.5 and 4.7 months, respectively. Fifty-nine (95%) of 62 patients had a gross-total resection. The 30-day mortality rate was 4.2%. The Karnofsky Performance Scale scores at discharge from the hospital and 3 months postoperatively were the same or improved in 50 (85%) of 59 and 26 (51%) of 51, respectively. Overall postcraniotomy survival was 62% at 6 months, 39% at 1 year, 21% at 2 years, and 8% at 5 years. In multivariate and univariate analysis, control of systemic disease, and sarcomas originating from bone, cartilage, or soft tissue were predictors of survival. Patients with control of systemic disease had survival advantage when compared with those who did not. In patients with alveolar soft-part sarcoma, there was a significantly increased survival advantage compared with all other histological subgroups.

Conclusions

The authors' results suggest that in selected patients, resection of metastatic sarcoma to the brain is associated with a relatively low risk of operative death and results in improvement in neurological function. Patients with systemic control of their primary disease and certain histological subtypes (specifically alveolar soft-part sarcoma) have improved overall and progression-free survival.

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Dima Suki, Hiba Abouassi, Akash J. Patel, Raymond Sawaya, Jeffrey S. Weinberg and Morris D. Groves

Object

The authors tested the hypothesis that patients with metastatic posterior fossa lesions (MPFLs) treated with resection have a higher risk of leptomeningeal disease (LMD) than those with MPFLs treated with stereotactic radiosurgery (SRS).

Methods

Between 1993 and 2004, 379 patients with MPFLs were treated with resection or SRS at The University of Texas M. D. Anderson Cancer Center. The authors' primary study outcome was the incidence of LMD, as diagnosed with cerebrospinal fluid cytological analysis and/or neuroimaging.

Results

Resection was performed in 260 patients, whereas 119 patients underwent SRS. The median patient age was 56 years, 51% of patients were male, and 93% had a Karnofsky Performance Scale score $ 70. The most common primary cancers were those of the lung, breast, and kidney, as well as melanoma. Leptomeningeal dissemination of cancer occurred in 33 patients: 26 in the resection group and 7 in the SRS group (resection group: rate ratio [RR] 2.06, 95% confidence interval [CI] 0.89–4.75, p = 0.09). Piecemeal tumor resection (137 cases) was associated with a significantly higher risk of LMD than en bloc resection (123 cases; RR 3.4, 95% CI 1.43–8.12, p = 0.006) or SRS (RR 3.37, 95% CI 1.41–8.04, p = 0.006), and there was no significant difference in the risk for LMD between en bloc resection and SRS (en bloc resection: RR 0.98, 95% CI 0.34–2.81, p = 0.98). The multivariate RR and significance associated with piecemeal resection, however, were consistent, with a strong effect (RR 2.45, 95% CI 1.19–5.02, p = 0.02) and no indication of biases associated with tumor size, location, or cystic/necrotic appearance.

Conclusions

There is an increased risk of LMD after piecemeal resection of an MPFL. This increase, although clinically and statistically significant, is not as alarming as previously reported and is absent when en bloc removal is achieved. Further assessment of the role of resection in a controlled prospective setting is warranted.

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Paul J. Holman, Dima Suki, Ian McCutcheon, Jean-Paul Wolinsky, Laurence D. Rhines and Ziya L. Gokaslan

Object. The surgical treatment of metastatic spinal tumors is an essential component of the comprehensive care of cancer patients. In most large series investigators have focused on the treatment of thoracic lesions because 70% of cases involve this region. The lumbar spine is less frequently involved (20% cases), and it is unclear whether its unique anatomical and biomechanical features affect surgery-related outcomes. The authors present a retrospective study of a large series of patients with lumbar metastatic lesions, assessing neurological and pain outcomes, complications, and survival.

Methods. The authors retrospectively reviewed data obtained in 139 patients who underwent 166 surgical procedures for lumbar metastatic disease between August 1994 and April 2001. The impact of operative approach on outcomes was also analyzed.

Among the wide variety of metastatic lesions, pain was the most common presenting symptom (96%), including local pain, radicular pain, and axial pain due to instability. Patients underwent anterior, posterior, and combined approaches depending on the anatomical distribution of disease. One month after surgery, complete or partial improvement in pain was demonstrated in 94% of the cases. The median survival duration for the entire population was 14.8 months.

Conclusions. The surgical treatment of metastatic lesions in the lumbar spine improved neurological and ambulatory function, significantly reducing axial spinal pain; results were comparable with those for other spinal regions. Analysis of results obtained in the present study suggests that outcomes are similar when the operative approach mirrors the anatomical distribution of disease. When lumbar vertebrectomy is necessary, however, anterior approaches minimize blood loss and wound-related complications.

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Daniel K. Fahim, Claudio E. Tatsui, Dima Suki, Joy Gumin, Frederick F. Lang and Laurence D. Rhines

Object

There is currently no reproducible animal model of human primary malignant bone tumors in the spine to permit laboratory investigation of the human disease. Therefore, the authors sought to adapt their previously developed orthotopic model of spinal metastasis to a model for primary malignant bone tumors of the spine.

Methods

A transperitoneal surgical approach was used to implant osteosarcoma (Krib-1) into the L-3 vertebral body of nude mice via a drill hole. Motor function was evaluated daily using the previously validated qualitative key milestones of tail dragging, dorsal stepping, hindlimb sweeping, and paralysis. A subset of these animals was euthanized upon reaching the various milestones, and the spines were removed, sectioned, and stained. The degree of spinal cord compression was correlated with the occurrence of milestones and assessed by a ratio between the neural elements divided by the area of the spinal canal. Another subset of animals received stably transfected Krib-1 cells with the luciferase gene, and bioluminescence was measured at 10, 20, and 30 days postimplantation.

Results

Osteosarcoma xenografts grew in all animals according to a reliable and reproducible time course; the mean time for development of behavioral milestones was noted in relation to the day of implantation (Day 1). Tail dragging (Milestone 1) occurred on Day 19.06 (95% CI 16.11–22.01), dorsal stepping (Milestone 2) occurred on Day 28.78 (95% CI 26.79–30.77), hindlimb sweeping (Milestone 3) occurred on Day 35.61 (95% CI 32.9–38.32), and paralysis of the hindlimb (Milestone 4) occurred on Day 41.78 (95% CI 39.31–44.25). These clinically observed milestones correlated with increasing compression of the spinal cord on histological sections. The authors observed a progressive increase in the local bioluminescence (in photons/cm2/sec) of the implanted level over time with a mean of 2.17 (range 0.0–8.61) at Day 10, mean 4.68 (range 1.17–8.52) at Day 20, and mean 5.54 (range 1.22–9.99) at Day 30.

Conclusions

The authors have developed the first orthotopic murine model of a primary malignant bone tumor in the spine, in which neurological decline reproducibly correlates with tumor progression as evidenced by pathological confirmation and noninvasive bioluminescence measurements. Although developed for osteosarcoma, this model can be expanded to study other types of primary malignant bone tumors in the spine. This model will potentially allow animal testing of targeted therapies against specific primary malignant tumor types.

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Dima Suki, Rami Khoury Abdulla, Minming Ding, Soumen Khatua and Raymond Sawaya

Object

Metastasis to the brain is frequent in adult cancer patients but rare among children. Advances in primary tumor treatment and the associated prolonged survival are said to have increased the frequency of brain metastasis in children. The authors present a series of cases of brain metastases in children diagnosed with a solid primary cancer, evaluate brain metastasis trends, and describe tumor type, patterns of occurrence, and prognosis.

Methods

Patients with brain metastases whose primary cancer was diagnosed during childhood were identified in the 1990–2012 Tumor Registry at The University of Texas M.D. Anderson Cancer Center. A review of their hospital records provided demographic data, history, and clinical data, including primary cancer sites, number and location of brain metastases, sites of extracranial metastases, treatments, and outcomes.

Results

Fifty-four pediatric patients (1.4%) had a brain metastasis from a solid primary tumor. Sarcomas were the most common (54%), followed by melanoma (15%). The patients' median ages at diagnosis of the primary cancer and the brain metastasis were 11.37 years and 15.03 years, respectively. The primary cancer was localized at diagnosis in 48% of patients and disseminated regionally in only 14%. The primary tumor and brain metastasis presented synchronously in 15% of patients, and other extracranial metastases were present when the primary cancer was diagnosed. The remaining patients were diagnosed with brain metastasis after initiation of primary cancer treatment, with a median presentation interval of 17 months after primary cancer diagnosis (range 2–77 months). At the time of diagnosis, the brain metastasis was the first site of systemic metastasis in only 4 (8%) of the 51 patients for whom data were available. Up to 70% of patients had lung metastases when brain metastases were found. Symptoms led to the brain metastasis diagnosis in 65% of cases. Brain metastases were single in 60% of cases and multiple in 35%; 6% had only leptomeningeal disease. The median Kaplan-Meier estimates of survival after diagnoses of primary cancer and brain metastasis were 29 months (95% CI 24–34 months) and 9 months (95% CI 6–11 months), respectively. Untreated patients survived for a median of 0.9 months after brain metastasis diagnosis (95% CI 0.3–1.5 months). Those receiving treatment survived for a median of 8 months after initiation of therapy (95% CI 6–11 months).

Conclusions

The results of this study challenge the current notion of an increased incidence of brain metastases among children with a solid primary cancer. The earlier diagnosis of the primary cancer, prior to its dissemination to distant sites (especially the brain), and initiation of presumably more effective treatments may support such an observation. However, although the actual number of cases may not be increasing, the prognosis after the diagnosis of a brain metastasis remains poor regardless of the management strategy.

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Claudio E. Tatsui, Frederick F. Lang, Joy Gumin, Dima Suki, Naoki Shinojima and Laurence D. Rhines

Object

There is currently no reproducible animal model of human spinal metastasis that allows for laboratory study of the human disease. Consequently, the authors sought to develop an orthotopic model of spinal metastasis by using a human lung cancer cell line, and to correlate neurological decline with tumor growth.

Methods

To establish a model of spinal metastasis, the authors used a transperitoneal surgical approach to implant PC-14 lung tumors into the L-3 vertebral body of nude mice via a drill hole. In 24 animals, motor function was scored daily by using the validated semiquantitative Basso-Beattie-Bresnahan (BBB) scale. A second group of 26 animals (6 or 7 per time point) were sacrificed at specific times, and the spines were removed, sectioned, and stained. Canal compromise was analyzed quantitatively by determining the ratio of the area of the neural elements to the area of the spinal canal on histological sections (neural/canal ratio). Correlations between BBB score and histological evaluation of tumor growth were assessed.

Results

Lung cancer xenografts grew in all animals undergoing functional evaluation (24 mice) according to a reliable and reproducible time course, with paraplegia occurring at a median interval of 30 days following tumor implantation (95% CI 28.1–31.9 days). Importantly, the analysis defined 4 key milestones based on components of the BBB score; these were observed in all animals, were consistent, and correlated with histological progression of tumor. From Days 1 to 14, the mean BBB score declined from 21 to 19. The animals progressed from normal walking with the tail up to walking with the tail constantly touching the ground (milestone 1). The median time to tail dragging was 12 days (95% CI 10.8–13.2). Histological studies on Day 14 demonstrated that tumor had progressed from partial to complete VB infiltration, with initial compression of the neural elements and epidural tumor extension to adjacent levels (mean neural/canal ratio 0.32 ± 0.05, 7 mice). From Days 15 to 20/21 (left/right leg), the mean BBB score declined from 19 to 14. Animals showed gait deterioration, with the development of dorsal stepping (milestone 2). The median time to dorsal stepping was 21 days (95% CI 19.4–22.6) in the left hindlimb and 23 days (95% CI 20.6–25.4) in the right hindlimb. Histological studies on Day 21 demonstrated an increase in the severity of the neural element compression, with tumor extending to adjacent epidural and osseous levels (mean neural/canal ratio 0.19 ± 0.05, 6 mice). From Days 22 to 26/27 (left/right leg), the mean BBB score declined from 14 to 8. Animals had progressive difficulty ambulating, to the point where they showed only sweeping movements of the hindlimb (milestone 3). The median time to hindlimb sweeping was 26 days (95% CI 23.6–28.4) and 28 days (95% CI 27.1–28.9) in the left and right hindlimbs, respectively. Histological studies on Day 28 revealed progressive obliteration of the spinal canal (mean neural/canal ratio 0.09 ± 0.01, 7 mice). From Days 29 to 36, the animals progressed to paralysis (milestone 4). The median time to paralysis was 29 days (95% CI 27.6–30.4) and 30 days (95% CI 28.1–31.9) in the left and right hindlimbs, respectively.

Conclusions

The authors have developed an orthotopic murine model of human spinal metastasis in which neurological decline reproducibly correlates with severity of tumor progression. Although developed for lung cancer, this model can be expanded to study other types of metastatic or primary spinal tumors. Ultimately, this will allow testing of targeted therapies against specific tumor types.

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Franco Demonte, Peyman Tabrizi, Scott A. Culpepper, Dima Suki, Charles N. S. Soparkar and James R. Patrinely

Object. Partial resection of the orbital bones is not uncommon during the excision of anterior and anterolateral skull base tumors. Controversy exists regarding the need for and extent of reconstruction after this procedure. The authors studied this factor in a series of patients.

Methods. The authors conducted a retrospective review of 56 patients in whom resection of 57 anterior or anterolateral skull base tumors and partial excision of the orbital bone were performed. Adverse ophthalmological outcomes were noted in 16 patients, in nine of whom adverse outcomes were believed to be directly related to resection of the orbital walls. Some degree of orbital reconstruction was performed during 23 of the 57 procedures. An adverse orbital outcome was strongly associated with resection of the orbital floor and resection of two thirds or more of two or more orbital walls, but not with the presence or absence of orbital reconstruction. The latter finding, however, is likely a function of selection bias.

Conclusions. In most patients elaborate orbital reconstruction is not necessary after partial excision of the orbital bones. Isolated medial and lateral orbital wall defects, or combined superior and lateral orbital wall defects, especially in cases in which the periorbita is intact, probably do not require primary reconstruction. In cases of orbital floor defects, whether isolated or part of a multiple-wall resection, primary reconstruction is recommended.

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Christopher M. McPherson, Dima Suki, Ian E. McCutcheon, Ziya L. Gokaslan, Laurence D. Rhines and Ehud Mendel

Object.

Metastastic lesions have been reported in 5 to 40% of patients with spinal and sacrococcygeal chordoma, but few contemporary series of chordoma metastastic disease exist in the literature. Additionally, the outcome in patients with chordoma-induced metastastic neoplasms remains unclear. The authors performed a retrospective review of the neurosurgery database at the University of Texas M. D. Anderson Cancer Center in Houston to determine the incidence of metastatic disease in a contemporary series of spinal and sacrococcygeal chordoma as well as to determine the outcomes.

Methods.

Thirty-seven patients underwent surgery for spinal and sacrococcygeal chordoma between June 1, 1993, and March 31, 2004. All records were reviewed, and appropriate statistical analyses were used to compare patient data for preoperative characteristics, treatments, and outcomes.

The authors identified seven patients (19%) in whom metastatic disease developed; in three the disease had metastasized to the lungs only, in two to the lungs and liver, and in two to distant locations in the spine. There were no significant differences in age, sex, tumor location, or history of radiation treatments between patients with and those without metastases. In cases with local recurrent tumors, metastastic disease was more likely to develop than in those without recurrence (28 compared with 0%, respectively; p = 0.07). In two (12%) of 17 patients who underwent en bloc resection, metastatic disease developed, whereas it developed in five (25%) of 20 patients treated by curettage (p = 0.42). The median time from first surgery to the appearance of metastatic disease, as calculated using the Kaplan–Meier method, was 143.4 months (95% confidence interval [CI] 66.8–219.9). The median survival duration of patients with metastatic disease after the first surgery was 106 months (95% CI 55.7–155.7), and this did not differ significantly from that in patients in whom no metastases developed (p = 0.93).

Conclusions.

Spinal chordoma metastasized to other locations in 19% of the patients in this series. In patients with local disease recurrence, metastatic lesions are more likely to develop. Metastatic lesions were shown to be aggressive in some cases. Surgery and chemotherapy can play a role in controlling metastatic disease.