Abstract
Background: To avoid permanent neurologic deficits and preserve brain function, intraoperative electrical stimulation mapping (IESM) is essential for surgical resection. Case Report: A 59-year-old right-handed woman with ovarian cancer who had undergone stereotactic radiotherapy for brain metastasis two years before, was introduced due to progressive left upper paresis. Magnetic resonance imaging showed a recurrence of the lesion. We performed awake surgery using IESM. Thus, the sensorimotor site was elicited on the precentral and postcentral gyrus. However, IESM elicited no disturbance of motor function on the surface of the posterior part of the precentral gyrus. We made a safe corticotomy on it, and performed the resection of recurrent BM. Preserving the motor and sensory function, we achieved the resection of BM. After surgery, she experienced a significant improvement in motor function. Conclusion: IESM is a useful tool to make a safe approach via the precentral gyrus avoiding permanent sensorimotor deficits.
- Motor function
- awake surgery
- brain metastasis
- intraoperative electrical stimulation mapping
- subcortical metastasis
- precentral gyrus
Brain metastasis (BM) from systemic cancer is the most common neoplasm among intracranial brain tumors. Stereotactic radiosurgery (SRS) is an effective and routinely used treatment modality for brain metastasis, achieving high local tumor control (LTC) rates and typically avoiding the neurocognitive toxicities associated with whole-brain radiation therapy. Based on a recent systematic review, the reported one-year LTC rates vary from 71% to >90% (1). However, among the long-term survivors, thanks to advancements in chemotherapy, a few patients previously treated with SRS and fractionated stereotactic radiotherapy (fSRT) experienced recurrence, radiation necrosis, and cyst formation in the long follow-up after SRS/fSRT (2-7). In such cases with recurrence in previously irradiated fields, it is controversial how these lesions should be treated.
To avoid permanent neurologic deficits and preserve brain function in and near the eloquent area, intraoperative electrical stimulation mapping (IESM) is necessary for infiltrating glioma. However, awake surgery for BM is adapted to limited cases because most BMs are cortically located and have much clearer border lines than infiltrating gliomas. Here, we present a successful surgical case of subcortical BM in the precentral gyrus (PrCG), preserving the sensorimotor function by using IESM.
Case Report
A 59-year-old right-handed woman with ovarian cancer was introduced to our department due to progressive left upper paresis. Two years ago, she underwent fSRT with 28 Gy in five fractions for BM located in the PrCG (Figure 1A). She was administrated bevacizumab (a humanized antibody inhibiting the vascular endothelial growth factor) because of radiation necrosis, as judged by radiological findings, and the lesion was shrunk (Figure 1B). After that, she presented with progressive left upper paresis, and repeated magnetic resonance imaging (MRI) revealed a continuous regrowth of the lesion. MRI revealed an enhancing lesion with perifocal edema in the PrCG, which invaded the postcentral gyrus (Figure 1C and D). This patient was evaluated by a multidisciplinary team, including neurosurgeons, neuroradiologists, and radiation oncologists in our hospital, to determine the most appropriate therapy. Due to the progressing symptoms and the amount of moderate edema on T2-weighted MRI, surgical resection instead of stereotactic radiosurgery or radiotherapy was recommended. Eventually, we decided to perform surgical resection using IESM with awake surgery. Results of the preoperative motor function revealed a mild disturbance in the upper extremity. The patient underwent awake surgery with IESM to identify and preserve the cortical and subcortical eloquent structures. This method, including the electrical parameters and the intraoperative clinical tasks, has been extensively described in previous studies (8-10). After opening the dura mater, the patient was woken up. The tumor was delineated using ultrasonography and a neuro-navigation system (Brain Lab, Munich, Germany) (Figure 2A, tag: A-F). Starting cortical mapping using an intensity of 3.2 mA, transient sensory disturbances were elicited in the primary sensory area of the face and finger (Figure 2, no. 1-5), and transient motor disturbances were elicited in the primary motor area of the face (Figure 2, no. 6). No other motor disturbances were induced on the surface of the PrCG by IESM. After completion of this cortical mapping, the lesion resection was initiated. Since the opening of the central sulcus was very difficult because the adhesions were very tight to dissect, we made a safe corticotomy on the posterior part of the PrCG, where she was able to move her upper extremity and speak normally. After the demarcated tumor was exposed, we resected the tumor and dissected the surrounding gliosis. The muscular contraction of the upper extremity was reproducibly elicited at the anterior part of the tumor cavity by subcortical stimulation (Figure 2B, no. 49, 50). This muscular contraction was normalized after stopping the stimulation. As this tumor had infiltrated the region underneath the primary sensory area (no. 4, 5), we intentionally left the tumor just beneath the primary sensory area to preserve the somatosensory function. The intraoperative frozen section revealed the recurrence of cancer. At the final stage of the awake condition, she could move her upper extremity and speak normally.
Preoperative images. (A) Magnetic resonance imaging (MRI) of the brain showing brain metastasis before stereotactic radiotherapy (SRT). (B) MRI showing a shrinkage, 12 months after SRT. (C) and (D) MRI showing a left frontal lesion suggesting a recurrent brain metastasis with perifocal edema on enhanced images and T2-weighted axial image.
Intraoperative pictures. Intraoperative photograph on the surface of the exposed operative field. The tumor boundaries identified using ultrasonography and neuro-navigation were marked by alphabets (A-F). The eloquent cortical sites identified using electrical stimulations were marked by numbers as follows: 1: sensory area of face, 2-5: sensory area of finger, and 6: motor area of face. Upper right: intraoperative photograph on the surface without any marks. Intraoperative photograph after the resection. The eloquent subcortical sites identified using electrical stimulations were marked by numbers as follows: 49, 50: finger movement. Upper right: intraoperative photograph of the exposed recurrent brain metastasis.
The postoperative functional outcome was assessed by the same neurosurgeon. The postoperative course was uneventful. She recovered from motor disturbance gradually. Postoperative MRI revealed a small remnant beneath the postcentral gyrus (Figure 3A and B). Neuropathological examination revealed viable cancer cells compatible with ovarian cancer. Again, a multidisciplinary team determined the additional Gamma Knife SRS for the remnant of the lesion three weeks after surgery. Eventually, she returned to a normal life with an improvement of motor disturbances. MRI 15 months after surgery revealed no recurrence (Figure 3C).
Preoperative and postoperative images. Magnetic resonance imaging of the brain on enhanced images [(A) before surgery, (B) the next day after surgery, and (C) 15 months later after surgery].
Discussion
SRS is an effective, routinely used treatment modality for BM, achieving high LTC rates, and typically avoiding the neurocognitive toxicities associated with whole-brain radiation therapy. Based on a recent systematic review, the reported one-year LTC rates vary from 71% to >90% (1). A few patients previously treated with SRS/fSRT experienced a recurrence, radiation necrosis, and cyst formation in the long follow-up after SRS/fSRT (2-7).
The treatment options for recurrent BM after SRS/fSRT are whole-brain radiation therapy, re-irradiation using SRS/fSRT, and surgical resection. Re-irradiation for recurrent BM after SR/fSRT is limited due to frequent radiation necrosis and local tumor control, in the case of recurrent BM with progressing neurological symptoms and spreading perifocal edema.
For large BM, surgical intervention under image-guided assistance and intraoperative neurophysiological monitoring has become the gold standard of modern neurosurgery (11). On the other hand, surgical intervention of BM in and near the eloquent area is still under discussion. In our previous study, we reported awake surgery for cavernous angioma located in the eloquent area. Using IESM by awake surgery can optimize the resection for the subcortical located cavernous angioma with a safety corridor through the normal brain (8).
Recently, several studies reported that intraoperative brain mapping and neurophysiological monitoring for BM located in the Rolandic region might contribute to the safe maximum resection and the preservation of the sensorimotor function (11, 12). Spena et al. reported the approach to the purely subcortical brain tumor including the BM, glioma, and cavernous angioma with the aid of awake intraoperative electrical stimulation mapping. The main distance of the tumors from the cortical surface was 18.2 mm. Cortical and subcortical electrical stimulation was fundamental to obtain the proper surgical corridor to the lesion. Transient postoperative morbidity was 79.5%, but all patients had recovered to preoperative status.
Conclusion
In this case, cortical IESM under intraoperative sensorimotor evaluation was very useful to decide the ideal corridor on the surface of PrCG. After surgery, the patient had a significant recovery from motor disturbance. Thus, we propose to consider awake surgery for subcortically located BM beneath the PrCG to optimize the extent of resection while preserving the motor function.
Footnotes
Conflicts of Interest
The Authors have no conflicts of interest to declare in relation to this study.
Authors’ Contributions
RM, FS, and MK performed the surgery. TM and FN analyzed the clinical course. All Authors discussed the clinical results, critically revised the report, commented on drafts of the manuscript and approved the final manuscript. IN and HN supervised the findings of this case.
- Received November 16, 2021.
- Revision received December 4, 2021.
- Accepted December 5, 2021.
- Copyright © 2022 International Institute of Anticancer Research (Dr. George J. Delinasios), All rights reserved.
