J Neurosurg 116:1182–1186, 2012
Morbidity profile following aggressive resection of parietal lobe gliomas Clinical article Nader Sanai, M.D., Juan Martino, M.D., and Mitchel S. Berger, M.D. Department of Neurological Surgery, University of California, San Francisco, California Object. The impact of parietal lobe gliomas is typically studied in the context of parietal lobe syndromes. However, critical language pathways traverse the parietal lobe and are susceptible during tumor resection. The authors of this study reviewed their experience with parietal gliomas to characterize the impact of resection and the morbidity associated with language. Methods. The study population included adults who had undergone resection of parietal gliomas of all grades. Tumor location was identified according to a proposed classification system for parietal region gliomas. Low- and high-grade tumors were volumetrically analyzed using FLAIR and T1-weighted contrast-enhanced MR imaging. Results. One hundred nineteen patients with parietal gliomas were identified—34 with low-grade gliomas and 85 with high-grade gliomas. The median patient age was 45 years, and most patients (53) presented with seizures, whereas only 4 patients had an appreciable parietal lobe syndrome. The median preoperative tumor volume was 31.3 cm3, the median extent of resection was 96%, and the median postoperative tumor volume was 0.9 cm3. Surprisingly, the most common early postoperative neurological deficit was dysphasia (16 patients), not weakness (12 patients), sensory deficits (14 patients), or parietal lobe syndrome (10 patients). A proposed parietal glioma classification system, based on surgical anatomy, was predictive of language deficits. Conclusions. This is the largest reported experience with parietal lobe gliomas. The findings suggested that parietal language pathways are compromised at a surprisingly high rate. The proposed parietal glioma classification system is predictive of postoperative morbidity associated with language and can assist with preoperative planning. Taken together, these data emphasize the value of identifying language pathways when operating within the parietal lobe. (http://thejns.org/doi/abs/10.3171/2012.2.JNS111228)
Key Words • parietal lobe • extent of resection • glioma • parietal syndrome • oncology
P
gliomas are an underrepresented entity in the neurosurgical literature and yet are seated within a critical junction of motor, visual, language, and sensory pathways. Although 30% of all high-grade gliomas and 10% of all low-grade gliomas reside in this area, previous work, consisting almost entirely of case reports, documents such cases only in the context of specific parietal lobe syndromes.1–3,5–7,9,10 While this body of work has focused on detecting tumor-associated sensory and receptive symptoms, as well as variations of the Gerstmann syndrome, many of these neurological deficits are not devastating and do not severely compromise quality of life following tumor resection. In contrast, visual- and language-associated postoperative deficits often substantially affect functional survival after resection.4 Importantly, the right parietal lobe, as well as the left, correlates with language performance. We reviewed our institutional experience with microsurgical removal of parietal lobe gliomas in the dominant 1182
arietal
and nondominant hemispheres 1) to characterize the neurological morbidity profile associated with parietal glioma resection, 2) to define the anatomical and pathological diversity of these lesions, 3) to develop a classification system that predicts functional systems at risk during resection, and 4) to identify the utility of intraoperative mapping paradigms during parietal glioma resection.
Methods
The University of California, San Francisco, Committee on Human Research approved this study. Patient Selection
In this retrospective study we examined the records
This article contains some figures that are displayed in color online but in black-and-white in the print edition.
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Neurological morbidity of parietal glioma resection of 119 consecutive patients with parietal gliomas treated by the senior author (M.S.B.). These patients were adults (age ≥ 18 years) who had undergone surgery at the University of California, San Francisco, between 2000 and 2007 as well as preoperative and immediately postoperative (< 48 hours after surgery) MR imaging. Central pathology review was performed based on WHO guidelines. Patients with Grade I histology were excluded from analysis, as were those with multifocal lesions or gliomatosis cerebri. Clinical data were collected from patient records and telephone interviews. Patient Outcome Measurements
Preoperatively and at each follow-up appointment, patients had undergone neurological examination. Two clinicians had conducted each examination: the senior attending neurosurgeon and a neurosurgical resident or an attending neurooncologist. Neurological morbidity was defined by tracking new-onset or worsening deficits related to motor, sensory, visual, or language function. Our protocol for language function testing has been described elsewhere.8 Differences between the findings of the 2 examiners were adjudicated by accepting the results showing greater impairment, although there was a 96% rate of concordance between the examiners. Routine detailed clinical examinations were performed at 10 days, 4–6 weeks, and 3–6 months after surgery. Patients with no improvement at the 6-month follow-up visit were considered to have a permanent deficit. Parietal lobe syndromes were defined by one or more of the following: right-left confusion, acalculia, agraphesthesia, finger agnosia, sensory extinction, astereoagnosis, contralateral neglect, a- nosognosia, loss of 2-point discrimination, drawing difficulty, inability to recall a string of digits, constructional apraxia, ocular apraxia, simultanagnosia, optic ataxia, agnosia, visual extinction, and personality change. Patients did not undergo specific parietal lobe syndrome batteries, as our objective was to detect symptoms that significantly affected patient quality of life. All patients with nonfocal postoperative examinations had written documentation of a normal neurological examination in the chart. Magnetic resonance imaging results were also reviewed to confirm that the patients’ symptoms were not a function of tumor recurrence or ischemia. Volumetric Analyses
The primary neurosurgeon (M.S.B.) conducted volumetric measurements of pre- and postoperative imaging. For low-grade gliomas, manual segmentation was performed with region-of-interest analysis to measure tumor volumes (cm3) on the basis of FLAIR or T2 axial slices, as previously described. Extent of resection was calculated as (preoperative tumor volume − postoperative tumor volume)/preoperative tumor volume. For high-grade gliomas, a similar calculation was made using the volume of contrast-enhancing tissue seen on T1-weighted MR imaging. The determination of volumes was made without consideration of clinical outcome.
Proposed Parietal Glioma Classification System
Based on clinical and radiographic observations, 4
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primary parietal regions were delineated, with 2 additional modified subregions. Collectively, these locations identified 6 distinct parietal “areas” (Fig. 1). Parietal Areas 1–3 are most evident on the superior view of the parietal lobe, where Area 1 is in the supramarginal gyrus, Area 1+ extends into the postcentral gyrus, Area 2 designates the superior parietal lobule, Area 2+ extends into the postcentral gyrus, and Area 3 refers only to the angular gyrus. From a medial perspective of the parietal lobe, Areas 2 and 2+ are also identifiable, as is Area 4, which comprises the cingulum. The location of each tumor with respect to one or more of these parietal areas was identified both pre- and postoperatively, enabling identification of the areas resected during the course of surgery.
Results
One hundred nineteen patients with parietal lobe gliomas underwent 119 microsurgical removals. Patients had a median age of 45.0 years (range 18–81 years) and presented with a median Karnofsky Performance Scale score of 75 (range 20–100). The mean clinical follow-up was 6.8 months (range 1–116 months), and no patient was lost to follow-up. The most common sign or symptom at presentation was seizure (44.5%), followed by sensory changes (21.8%) and language deficits (21.8%). Purely parietal lobe functions were rarely compromised preoperatively (3.4%). Tumors were most frequently located within the supramarginal gyrus (58.8%), superior parietal lobule (43.7%), or angular gyrus (42%). In the majority of cases, tumors were superficially located (84.9%), as opposed to deep (15.1%). The median preoperative tumor volume was 31.3 cm3 (range 3.7–375.7 cm3). The distribution of WHO grades was as follows: II (28.6%), III (19.3%), and IV (52.1%). Seventy-two patients (60.5%) underwent primary resection and 47 (39.5%) underwent secondary resection following either prior biopsy or prior resection. The median postoperative tumor volume was 0.9 cm3 (range 0–51.9 cm3), equating to a 96.3% extent of resection (range 41.6%–100%). Intraoperative cortical stimulation mapping was conducted in select cases, when appropriate. Twenty-four patients (20.2%) underwent awake craniotomy with language mapping, and 71 (59.6%) underwent asleep motor mapping. Twenty-four patients (20.2%) had no cortical stimulation mapping during resection. No patient had subcortical stimulation to identify motor or language sites. Early transient neurological morbidity following resection most frequently manifested as language deficits (13.4%) and vision changes (9.2%). However, by 6 months postoperatively, the rate of permanent deficits was 8.4% for language function and 6.7% for vision (Fig. 2). Interestingly, of the 95 patients who underwent asleep or awake intraoperative cortical stimulation mapping, the rates of permanent language deficits were significantly lower (3 patients [3.2%], p = 0.02) than in the 24 patients without mapping (7 patient [29.2%]). Importantly, of the 10 patients with permanent postoperative language deficits, 2 (20%) had lesions in the right parietal lobe. Other perioperative complications were rare but included 1183
N. Sanai, J. Martino, and M. S. Berger
Fig. 1. A proposed parietal glioma classification system. Drawings showing the 4 distinct areas delineating the common regions for glioma infiltration within the parietal lobe. Plus sign indicates tumors that also extend forward into the somatosensory cortex. Standard MR imaging in the axial (A) and sagittal (B and C) planes is sufficient to assign an area to each lesion. Printed with the permission of M. S. Berger, 2012.
wound flap infection (2.5%) and deep venous thrombosis (0.8%). There were no operative or perioperative deaths. Parietal lobe syndromes were rarely appreciated by the physician or patient following microsurgical lesion removal (Fig. 2). Ten patients (8.4%) exhibited parietal lobe symptoms in the early postoperative period, and only 3 of these patients (2.5%) had these deficits permanently (Table 1). The most common parietal lobe symptom following resection was right-left confusion, which occurred in 6 patients (5%) during the early postoperative period and 3 patients (2.5%) in the late postoperative interval. Glioma location within the parietal lobe was evenly distributed. Within the left and right hemispheres, the most common sites were Area 2 (28.6% and 15.1%, respectively) and Area 3 (26.9% and 15.1%, respectively). Extent of resection was slightly greater for right hemisphere lesions, but this difference was not significant (p = 0.20) and did not correspond to the incidence of neurological deficits (p = 0.34; Fig. 3). Most permanent neurological deficits were associated with left hemisphere resections. Specifically, permanent language deficits were most commonly seen after the resection of Area 1 lesions within the supramarginal gyrus (p < 0.01; Fig. 4), whereas permanent visual deficits were predicted by the resection of Area 3 lesions within the angular gyrus (p < 0.01). 1184
Fig. 2. Bar graph showing distribution of parietal lobe symptoms. Routine detailed neurological examinations revealed a subset of known parietal lobe symptoms. For most patients, symptoms subsided from the 1-week (early) to the 6-week (late) time points.
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Neurological morbidity of parietal glioma resection TABLE 1: Distribution of parietal lobe symptoms No. of Patients Symptom
Early (1 wk)
Late (6 wks)
right-left confusion acalculia agraphesthesia finger agnosia sensory extinction astereoagnosis
6 1 2 2 3 1
3 0 0 2 1 1
Discussion
Although parietal lobe gliomas have not been a major focus of investigative efforts to date, the substantial morbidity profile seen in this study suggests that these tumors should be examined in greater detail. The current study is the largest reported experience with parietal lobe gliomas and suggests that parietal language pathways can be compromised at a surprisingly high rate (13.4% transient and 8.4% permanent) as compared with our overall experience with gliomas located in and around language pathways.8 Although patients undergoing parietal tumor resection are at risk for “syndromic” parietal lobe dysfunction, the postoperative incidence of clinically detectable symptoms is low. While it remains possible that actual incidence would be higher but beyond the detection of even a detailed neurological examination, it is likely that such subtle parietal lobe deficits would not impact patient functionality or quality of life. Instead, our results indicated that language and visual deficits are both highly associated with parietal tumor resections. This is particularly evident for lesions within the supramarginal (Area 1) and angular (Area 3) gyri, which are adjacent to
Fig. 4. Bar graph showing the duration of postoperative neurological deficits. Postoperative language deficits were primarily incurred by patients with tumors in Areas 1 and 1+. Some resolution was observed from early (1-week) to late (6-week) time points, but the overall permanent rate of language deficits was 8.4%, including 2 of 10 patients with right-sided lesions. Number of patients is represented on the x axis.
language and visual pathways, respectively. For patients with lesions in these areas, preoperative diffusion tensor imaging tractography combined with intraoperative cortical and subcortical language mapping may reduce the incidence of devastating postoperative deficits. Importantly, 20% of observed permanent language deficits were attributable to right-sided parietal tumors in right-handed patients, suggesting that intraoperative language mapping should be considered for this subset of patients as well. Our proposed anatomical classification system for parietal lobe gliomas is a surgically intuitive set of cortical and subcortical domains with functional implications. Preoperative identification of the parietal area(s) associated with a planned tumor resection allows for anticipation of the neurological risks of the procedure, as well as an assessment of the need for intraoperative mapping techniques. Our findings emphasize the value of identifying functional pathways when operating within the parietal lobe, particularly when operating in or around languageor visual-associated pathways.
Conclusions
Fig. 3. Bar graph showing the extent of resection (x axis) by surgical side. For both left- and right-sided lesions, volumetric extent of resection analysis revealed comparatively aggressive resections, although less so for tumors infiltrating the somatosensory cortex, that is, Areas 1+ and 2+.
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The current study frames the risks of parietal glioma resection in the modern neurosurgical era. In contrast to previous authors, we found that parietal lobe syndromes are infrequently associated with parietal gliomas, yet language and visual deficits are surprisingly prevalent. Based on our parietal glioma classification system, tumors in Areas 1 and 3 are associated with higher rates of permanent language and visual deficits, respectively, suggesting that diffusion tensor imaging tractography and/or more extensive cortical/subcortical language mapping may be beneficial in parietal lobe glioma resections. Interestingly, our observed rate of permanent language deficits following parietal glioma resection (8.4%) is not only 5-fold greater than our previously reported rate after intraoperative language mapping for dominant hemisphere gliomas, 1185
N. Sanai, J. Martino, and M. S. Berger but is also associated with right parietal lesions in 20% of such cases. Taken together, these observations underline the value of intraoperative cortical and subcortical mapping techniques for parietal lobe gliomas, including language pathways within the nondominant hemisphere. Disclosure The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper. Author contributions to the study and manuscript preparation include the following. Conception and design: Berger, Martino. Acquisition of data: Sanai, Martino. Analysis and interpretation of data: Berger, Sanai. Drafting the article: Berger, Sanai. Critically revising the article: all authors. Reviewed submitted version of man uscript: all authors. Approved the final version of the manuscript on behalf of all authors: Berger. Statistical analysis: Sanai. References 1. Duffau H, Denvil D, Lopes M, Gasparini F, Cohen L, Capelle L, et al: Intraoperative mapping of the cortical areas involved in multiplication and subtraction: an electrostimulation study in a patient with a left parietal glioma. J Neurol Neurosurg Psychiatry 73:733–738, 2002 2. Duffau H, Leroy M, Gatignol P: Cortico-subcortical organization of language networks in the right hemisphere: an electrostimulation study in left-handers. Neuropsychologia 46: 3197–3209, 2008 3. Kurimoto M, Asahi T, Shibata T, Takahashi C, Nagai S, Hayashi N, et al: Safe removal of glioblastoma near the angular gyrus by awake surgery preserving calculation ability— case report. Neurol Med Chir (Tokyo) 46:46–50, 2006 4. McGirt MJ, Mukherjee D, Chaichana KL, Than KD, Weingart JD, Quinones-Hinojosa A: Association of surgically acquired
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motor and language deficits on overall survival after resection of glioblastoma multiforme. Neurosurgery 65:463–470, 2009 5. Nakano M, Tanaka S, Arai H, Ebato M, Ueno H: [A case of selective short-term memory disturbance due to a glioma in the left temporo-parietal lobe.] No To Shinkei 45:465–471, 1993 (Jpn) 6. Petrovich NM, Holodny AI, Brennan CW, Gutin PH: Isolated translocation of Wernicke’s area to the right hemisphere in a 62-year-man with a temporo-parietal glioma. AJNR Am J Neuroradiol 25:130–133, 2004 7. Russell SM, Elliott R, Forshaw D, Kelly PJ, Golfinos JG: Resection of parietal lobe gliomas: incidence and evolution of neurological deficits in 28 consecutive patients correlated to the location and morphological characteristics of the tumor. J Neurosurg 103:1010–1017, 2005 8. Sanai N, Mirzadeh Z, Berger MS: Functional outcome after language mapping for glioma resection. N Engl J Med 358: 18–27, 2008 9. Scarone P, Gatignol P, Guillaume S, Denvil D, Capelle L, Duffau H: Agraphia after awake surgery for brain tumor: new insights into the anatomo-functional network of writing. Surg Neurol 72:223–241, 2009 10. Zangwill OL: Agraphia due to a left parietal glioma in a lefthanded man. Brain 77:510–520, 1954 Manuscript submitted July 25, 2011. Accepted February 22, 2012. Current affiliation for Dr. Sanai: Department of Neurological Surgery, Barrow Neurological Institute, Phoenix, Arizona. Please include this information when citing this paper: published online March 23, 2012; DOI: 10.3171/2012.2.JNS111228. Address correspondence to: Mitchel S. Berger, M.D., Department of Neurological Surgery, University of California, San Francisco, 505 Parnassus Avenue, M779, San Francisco, California 94143. email:
[email protected].
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