Brain Tumor Res Treat 2022;10(3):164-171 / pISSN 2288-2405 / eISSN 2288-2413

REVIEW ARTICLE [Link]

Recent Update on Neurosurgical Management

of Brain Metastasis
Jihwan Yoo1 , Hun Ho Park1 , Seok-Gu Kang2 , Jong Hee Chang2
Department of Neurosurgery, Gangnam Severance Hospital, Yonsei University College of Medicine, Seoul, Korea
1

Department of Neurosurgery, Severance Hospital, Yonsei University College of Medicine, Seoul, Korea
2

Brain metastasis (BM), classified as a secondary brain tumor, is the most common malignant central
nervous system tumor whose median overall survival is approximately 6 months. However, the survival
rate of patients with BMs has increased with recent advancements in immunotherapy and targeted
therapy. This means that clinicians should take a more active position in the treatment paradigm that
passively treats BMs. Because patients with BM are treated in a variety of clinical settings, treatment
planning requires a more sophisticated decision-making process than that for other primary malignan-
Received June 9, 2022 cies. Therefore, an accurate prognostic prediction is essential, for which a graded prognostic as-
Revised June 22, 2022 sessment that reflects next-generation sequencing can be helpful. It is also essential to understand the
Accepted June 25, 2022 indications for various treatment modalities, such as surgical resection, stereotactic radiosurgery, and
Correspondence whole-brain radiotherapy and consider their advantages and disadvantages when choosing a treat-
Jong Hee Chang ment plan. Surgical resection serves a limited auxiliary function in BM, but it can be an essential thera-
Department of Neurosurgery, peutic approach for increasing the survival rate of specific patients; therefore, this must be thoroughly
Brain Tumor Center, Severance Hospital, recognized during the treatment process. The ultimate goal of surgical resection is maximal safe resec-
Yonsei University College of Medicine,
tion; to this end, neuronavigation, intraoperative neuro-electrophysiologic assessment including evoked
50-1 Yonsei-ro, Seodaemun-gu,
Seoul 03722, Korea
potential, and the use of fluorescent materials could be helpful. In this review, we summarize the con-
Tel: +82-2-2228-2156 siderations for neurosurgical treatment in a rapidly changing treatment environment.
Fax: +82-2-393-9979
E-mail: changjh@[Link] Keywords 
Brain neoplasms; Neurosurgery; Neoplasm grading; Evoked potentials; Fluorescein.

INTRODUCTION and the role of neurosurgery in BM was first demonstrated in

a randomized controlled study conducted by Patchell et al. [8].
Metastatic brain tumors are the most common type of ma- For single BM lesions, a study randomized between a radiation-
lignant brain tumors in adults [1-3]. The incidence of brain only group and the surgery with radiation group showed a me-
metastasis (BM) has recently increased [4,5]. This is because dian survival of 15 weeks in the former and 40 weeks in the
of the advancement of cancer therapies, prolonged patient latter, indicating a significant survival benefit [8]. Bindal et al.
survival, and strengthening of screening protocols [4]. Al- [6] showed a statistically significant survival benefit when all
though the exact occurrence of BMs varies slightly in the lit- tumors were surgically removed in multiple BM cases com-
erature, it has recently been reported as 10%–40% and up to pared to those with residual tumors with a median survival
25% in autopsy studies [2,3,6,7]. BM requires aggressive treat- similar to that of patients with a single metastasis.
ment because it not only causes convulsions, paralysis, and Owing to the nature of the disease, BM can be caused by
speech impairment but can also affect patient survival. Even diverse carcinomas and presents different clinical situations
in palliative settings, it is crucial to address these symptoms, for each patient. Therefore, building a personalized treatment
plan is crucial, and physicians must consider the individual
This is an Open Access article distributed under the terms of the Creative Commons
Attribution Non-Commercial License ([Link] aspects during this process. These factors are represented by
which permits unrestricted non-commercial use, distribution, and reproduction in any clinical variables such as patient age, performance status, BM
medium, provided the original work is properly cited.
Copyright © 2022 The Korean Brain Tumor Society, The Korean Society for Neuro-
number and size, neurological symptoms, extracranial metas-
Oncology, and The Korean Society for Pediatric Neuro-Oncology tases, and genetic alterations [9]. Surgical resection, radio-

164
 J Yoo et al.

therapy such as stereotactic radiosurgery (SRS) and whole- ical situations [12]. Steady efforts have been made to develop
brain radiotherapy (WBRT), and systemic therapies including a prognostic prediction system (Table 1).
targeted therapy and immunotherapeutic agents, are used to The original work of the prognostic prediction system is a
treat BM [10,11]. This review summarizes considerations for recursive partitioning analysis (RPA) of the Radiation Oncol-
the surgical resection of BM, selection of treatment modali- ogy Treatment Group (RTOG) published by Gaspar et al. [13],
ties, and surgical tips. and 1,200 patients included in three clinical trials from 1979
to 1993 were analyzed. According to the RPA tree, age, Kar-
PREOPERATIVE PROGNOSIS nofsky performance score (KPS), systemic disease status, and
ASSESSMENT the presence of extracranial metastasis (ECM) reportedly af-
fect prognosis. In this study, patients with KPS of 70 or high-
Predicting prognosis is among the most important aspects er, controlled systemic disease, age <65 years, and no ECM
of BM treatment [9]. For neurosurgeons, the option of surgi- were classified as Class I; those with a KPS <70 as Class III;
cal resection includes general anesthesia; therefore, there must and other applicable patients as Class II. This system can eas-
be a clear benefit. Surgical resection is generally recommend- ily stratify patients using simple variables to predict progno-
ed for patients with an expected survival period of at least sis, but it is not currently used and remains a legacy because it
three months and should be chosen according to diverse clin- is not disease-specific, and current systemic therapies are not

Table 1. Graded prognostic assessments by cancer type

GPA scoring criteria
0 0.5 1.0 1.5 2.0
Lung cancer (NSCLC)
Age (yr) ≥70 <70 NA
KPS ≤70 80 90–100
ECM Present Absent
No. of BM >4 1–4
Gene status EGFR(-) and ALK(-) EGFR(+) or ALK(+)
Melanoma
Age (yr) ≥70 <70
KPS ≤70 80 90–100
ECM Present Absent
No. of BM >4 2–4 1
Gene status BRAF(-) or NA BRAF(+)
Renal cell carcinoma
KPS <80 80 90–100
ECM Present Absent
No. of BM >4 1–4
Hgb ≤11 11.1–12.5 >12.5
Gastrointestinal cancer
KPS <80 80 90–100
Age (yr) ≥60 <60
ECM Present Absent
No. of BM >3 2–3 1
Breast cancer
Age (yr) ≥60 <60
KPS ≤60 70–80 90-100
ECM Present Absent
No. of BM >1 1
Subtype Basal Luminal A HER2, luminal B
GPA, graded prognostic assessment; NSCLC, non-small cell lung cancer; KPS, Karnofsky performance score; BM, brain metastasis; EGFR, epi-
dermal growth factor receptor; ALK, anaplastic lymphoma kinase; ECM, extracranial metastasis; Hgb, hemoglobin; HER2, human epidermal
growth factor receptor-2

165
Neurosurgical Update for BM

reflected [9]. easy to become confused. However, the decision flow of the
Sperduto et al. [9] retrospectively analyzed 3,940 patients two systems is entirely distinct, so it is essential to fully com-
with newly diagnosed BM and published diagnosis-specific prehend it.
graded prognostic assessment (GPA) scores. Following this, Since surgical treatment can bring rapid resolution of the
specific GPAs for each cancer type were announced in the mass effect in tumors larger than 3–4 cm, it has the advantage
following order: breast cancer (breast-GPA) [14], lung cancer of being able to drastically reduce the steroid requirement and
(lung-molGPA) [15], melanoma (melanoma-molGPA) [16], minimize radiation necrosis that may occur after radiation
renal cell carcinoma (renal-GPA) [17], and gastrointestinal [5]. However, SRS can be applied to relatively small tumors
cancer (GI-GPA) [18]. Prognostic factors were evaluated us- and has the advantage of being delivered on an outpatient ba-
ing weights through multiple Cox regression analysis and sis or during a short hospital stay without requiring general
RPA methods, and the largest change was that genetic altera- anesthesia [5]. In addition, although WBRT appears effective
tions were included [14]. Genes associated with prognostic in almost all tumors, the neurocognitive decline that may oc-
factors differ among cancer types and include non-small cell cur after treatment has recently attracted attention [24,25]. A
lung cancer (epidermal growth factor [EGFR] or anaplastic large meta-analysis by Tallet et al. [26] reported decreases in
lymphoma kinase [ALK] alteration), breast cancer (estrogen neurocognitive function of 31%–57% within 3 months and
receptor [ER], progesterone receptor [PR], human epidermal 48%–89% in 1 year. This study reported that radiation expo-
growth factor receptor 2 [HER2]), and melanoma (BRAF) [14- sure to hippocampal lesions and the temporal lobe could re-
16]. This shift is attributed to the development of effective tar- duce a patient’s intelligence quotient and capacity to generate
geted therapies for specific gene abnormalities for each carci- new memories. To avoid this cognitive decline, hippocampal
noma, which has a substantial impact on patient prognosis. preservation or prophylactic administration of memantine
Immunotherapy has recently become popular and is widely may be used [27,28].
applied, especially for lung cancer and melanoma. Predictive
factors in immunotherapy can also be included as prognostic INNOVATIVE NEUROSURGICAL
factors in the future [19,20]. This prognostic prediction sys- TECHNIQUE
tem will be updated continuously. Therefore, neurosurgeons
should apply these changes with sensitivity when treating pa- Although the role of surgical treatment in BM treatment is
tients or designing clinical studies. limited, it appears to have a clear survival benefit in patients
with good performance status and single or oligometastases
TREATMENT MODALITY CHOICE [12]. In addition, since performance status is one of the most
important prognostic factors in patients with BM, the most
As mentioned above, combined with systemic chemother- important goal of surgical treatment is maximal safe resection
apy, localized therapies for BM include surgical resection, without neurological deficits. To achieve this goal, various re-
SRS, and WBRT [12]. The most important factors in deter- cently developed neurosurgical modalities can be used.
mining the treatment method are the number of BM and per- First, the positional relationship between metastatic brain
formance status. In a single metastasis situation, if the tumor tumors and the functional tract should be investigated using
is accessible and the patient has RPA Class I or II, surgical neuronavigation and diffusion tensor imaging tractography
treatment and adjuvant WBRT or adjuvant SRS are recom- [29]. The corticospinal tract (CST), which can affect motor
mended [12,21]. In cases of RPA Class III, SRS or WBRT function, is a representative tract requiring preservation (Fig. 1).
without surgical treatment is recommended [12,22,23]. If the In addition, recent language tracts are related to paraphasia,
tumor location is not accessible, SRS is recommended for RPA word recognition, and conditional associative tasks such as the
Class I or II, and WBRT is preferred for RPA Class III [12]. superior longitudinal fasciculus I, II, III, and uncinate fascicu-
In cases of multiple BM, treatment methods are largely clas- lus, which can also affect language function [30]. It is recom-
sified based on BM number (n>4), and surgical treatment is mended that we fully understand the three-dimensional ana-
recommended only when the tumor causes a mass effect and tomical relationship of the language tract during surgery and
is located in an accessible lesion [12,21]. SRS or WBRT is rec- carefully remove the tumor. Tumors invading the temporal
ommended if the patient’s performance is unsatisfactory and stem could affect the visual pathway and cause symptoms
the BM does not cause a mass effect. In some cases, SRS fol- such as hemianopia and quadrantanopia, so this should be
lowed by WBRT can be considered [12]. Due to the similarity sufficiently discussed with patients before surgery. One con-
between clinical variables used to determine treatment mo- sideration of neuronavigation during surgery is that accuracy
dality and prognostic prediction systems such as GPA, it is can change intraoperatively due to brain shifting, shallow an-

166 Brain Tumor Res Treat 2022;10(3):164-171

 J Yoo et al.

A B
Fig. 1. Example of application of neuronavigation and diffusion tensor imaging (DTI) tractography. A: Neuronavigation showing the anatomi-
cal relationship between the tumor and the corticospinal tract (CST). B: Three-dimensional DTI tractography showing an intuitive perspec-
tive of the CST.

esthesia, or brain swelling [31]. Therefore, it is necessary to between the monopolar stimulator and the CST is approxi-
compare the depth of the cerebral vein or the brain’s surface, mately 5 mm. If muscle movement is detected at a lower than
which can be landmarks, to evaluate and maintain accuracy expected current, the CST may be located closer to that ob-
during surgery. Furthermore, by setting a rescue point during served during navigation. This method will further reduce
the surgery, when shaking occurs, accuracy can be increased postoperative complications and contribute to maintaining
through re-registration to protect the surgeon from naviga- patient performance status.
tion errors [32]. In addition to the above methods, to increase resection ex-
Since the occurrence of neurological symptoms after sur- tent, staining materials that can differentiate between tumor
gery could impair the performance status of patients with and normal tissue, called fluorescence-guided surgery, are used
BM, particular attention is needed. Numerous types of sur- (Fig. 3A and B). In particular, sodium fluorescein is highly ac-
veillance devices can preserve patient functionality, including cumulated in enhancing lesions where the blood-brain bar-
motor evoked potentials (EPs), somatosensory EPs, visual rier is disrupted, distinguishing it from the normal parenchy-
EPs, and brainstem auditory EPs [33-36]. EPs can be used to ma under a yellow 560 nm surgical microscope filter, which
compare neurologic deficits after surgery versus before tumor enables tumor visualization [45,46]. It is usually used at a con-
removal; however, it has disadvantages in that it is difficult to centration of 5 mg/kg to stain tumors and is administered
predict the functional tract before tumor removal and diffi- through an intravenous injection after completion of the pro-
cult to measure the change in EP in real-time [33]. For simul- cedure under general anesthesia [46]. During resection, the
taneous monitoring, subcortical stimulation (SCS) mapping operator can view the tumor in real-time at high resolution
can also be used in asleep and awake surgery [37,38]. Since using a microscope. In the course of BM surgery using sodium
the use of SCS during brain surgery was reported by Duffau fluorescein, there was a strong correlation between the stained
et al. [39,40], it has been widely applied to various patients, area and enhancement on magnetic resonance imaging with
such as glioma patients, and the intraoperative procedure a reported sensitivity of 91% and specificity of 100% [46]. In
used for SCS has been described in detail elsewhere. SCS is a fact, 5-aminolevulinic acid, which is widely used in glioma
simple method of depolarizing the CST using a monopolar surgery, is also not widely used because it is expensive and has
stimulator to detect muscle movement with proven safety distinct detection rates for different primary cancer types (Fig.
[40,41]. Therefore, SCS-assisted BM resection could help pre- 3C and D). In a prospective study of 157 BMs, fluorescence was
serve function postoperatively (Fig. 2). Multichannel electro- observed in only 104 patients (66%), and the fluorescence pat-
myography recordings can increase the sensitivity of detect- tern was inconsistent. In particular, fluorescence was observed
ing muscle movements [42]. Recent studies suggested that the in 73% of breast cancer cases, but fluorescence was observed
current strength (mA) and the distance between the CST (mm) in only 33% of melanoma cases, and there was a statistically
correspond almost 1:1 [43,44]. For example, if stimulation is significant difference between carcinomas, resulting in incon-
sensed at 5 mA before tumor removal, the predicted distance sistency [47]. Additionally, in approximately two-thirds of

167
Neurosurgical Update for BM

cases, histological analysis of biopsies obtained from residual rounding tissues. However, most BMs do not have clear bound-
fluorescent areas during BM resection revealed false-positive aries with the surrounding normal parenchyma, and some
results [48]. cases show an invasive growth pattern [48-50]. Therefore, af-
The BM was previously thought to be distinct from the sur- ter gross total resection (GTR) has been achieved, the extent

B C
Fig. 2. Subcortical stimulation (SCS) during tumor resection. A: Sample monopolar stimulator for SCS. B: Application of SCS after tumor re-
section to estimate the distance to the corticospinal tract. C: Recording of muscle depolarization caused by SCS.

A B

C D
Fig. 3. Tumor resection using sodium fluorescein (A and B). A: Tumor and normal parenchyma under white light. B: Tumor and normal pa-
renchyma under a yellow 560 nm filter. The tumor, where the blood-brain barrier was disrupted, is well stained by sodium fluorescein. Tumor
resection using 5-aminolevulinic acid (5-ALA) (C and D). C: Tumor and normal parenchyma under white light. D: Tumor and normal paren-
chyma under a blue 400 nm filter. The tumor is well-stained with 5-ALA showing a strong red wavelength. CSF, cerebrospinal fluid.

168 Brain Tumor Res Treat 2022;10(3):164-171

 J Yoo et al.

of resection can be increased by additional removal of ap- In the rapidly developing neurosurgical armamentarium, the
proximately 5 mm; this method has been named microscop- application of fluorescein, neuro-electrophysiological surveil-
ic GTR (MTR) or supramarginal resection [51,52]. This meth- lance, and neuronavigation systems is expected to make a sig-
od is applicable to BM that occurs in non-eloquent areas and nificant contribution to maximal safe resection. Consequent-
can be implemented with methods such as functional brain ly, successful surgical resection may prolong cancer patient
mapping using SCS [52]. Yoo et al. [51] observed a local re- survival and provide opportunities for them to benefit from
currence rate of 23.3% in the MTR group and 43.1% in the novel therapies.
GTR group and reported a clear local control effect. The use
of this strategy for BM in the eloquent area and its contribu- Ethics Statement
Not applicable
tion to overall survival are unclear; therefore, this should be
investigated in greater depth in future research. Availability of Data and Material
Data sharing not applicable to this article as no datasets were generated
during the study.
NOVEL OPTIONS FOR BM
ORCID iDs
A novel technique called laser interstitial thermal therapy Jihwan Yoo [Link]
(LITT) was recently reported for its clinical utility since it was Hun Ho Park [Link]
first applied to BM in 2010 [53-55]. Briefly, LITT is a localized Seok-Gu Kang [Link]
Jong Hee Chang [Link]
minimally invasive method that attempts to kill cancer cells by
placing a stereotactically placed laser probe on the tumor and Author Contributions
delivering high thermal energy [55]. It is widely applied in BM, Conceptualization: Jihwan Yoo, Jong Hee Chang. Supervision: Jong Hee
Chang, Seok-Gu Kang. Resources: Hun Ho Park, Seok-Gu Kang, Jong Hee
with a short recovery term and a relatively simple procedure
Chang. Visualization: Jihwan Yoo. Writing—original draft: Jihwan Yoo.
[54]. This is preferred for patients with deeply seated tumors, Writing—review & editing: Jihwan Yoo, Hun Ho Park, Jong Hee Chang.
patients with expected high morbidity, a thin scalp, and low-
performance status, meaning that they are not surgical can- Conflicts of Interest
The authors have no potential conflicts of interest to disclose.
didates, and it can be applied as an adjuvant therapy in radio-
resistant tumors [54]. Funding Statement
In addition, some groups are trying neoadjuvant SRS, not- None
ing that WBRT or adjuvant SRS, which is performed after sur-
Acknowledgments
gical resection, reports rates of about 7.5%–14% leptomenin-
The authors would like to thank Editage ([Link]) for English
geal seeding (LMS) in BM [56]. Conceptually, neoadjuvant language editing.
GKS before surgery is used to reduce viable tumor cells, so
that even microtumor cells that are invisible during surgery REFERENCES
overflowing into the surrounding arachnoid space are not ex- 1. Artzi M, Bressler I, Ben Bashat D. Differentiation between glioblasto-
pected to lead to colonization. Asher et al. [56] reported a lo- ma, brain metastasis and subtypes using radiomics analysis. J Magn
cal control rate of 86%, a distant control rate of 38%, and LMS Reson Imaging 2019;50:519-28.
2. Nayak L, Lee EQ, Wen PY. Epidemiology of brain metastases. Curr On-
of 0% in a study of 47 patients. Thus, it may be an alternative col Rep 2012;14:48-54.
to adjuvant GKS or adjuvant WBRT in radio-resistant tumors 3. Stelzer KJ. Epidemiology and prognosis of brain metastases. Surg Neu-
such as melanoma and renal cell carcinoma, but caution is re- rol Int 2013;4(Suppl 4):S192-202.
4. Fecci PE, Champion CD, Hoj J, McKernan CM, Goodwin CR, Kirkpat-
quired for application as no survival benefit has been observed rick JP, et al. The evolving modern management of brain metastasis.
in large-scale clinical studies. Clin Cancer Res 2019;25:6570-80.
5. Suh JH. Stereotactic radiosurgery for the management of brain metas-
tases. N Engl J Med 2010;362:1119-27.
CONCLUSION 6. Bindal RK, Sawaya R, Leavens ME, Lee JJ. Surgical treatment of multi-
ple brain metastases. J Neurosurg 1993;79:210-6.
BM is clearly a desperate situation for cancer patients; how- 7. Walker AE, Robins M, Weinfeld FD. Epidemiology of brain tumors: the
ever, with the development of systemic treatment options, national survey of intracranial neoplasms. Neurology 1985;35:219-26.
8. Patchell RA, Tibbs PA, Walsh JW, Dempsey RJ, Maruyama Y, Kryscio
more aggressive treatment is recommended. In particular, RJ, et al. A randomized trial of surgery in the treatment of single metas-
the surgical treatment of BM remains important because it is tases to the brain. N Engl J Med 1990;322:494-500.
expected to alleviate the patient’s symptoms by immediately 9. Sperduto PW, Kased N, Roberge D, Xu Z, Shanley R, Luo X, et al. Sum-
mary report on the graded prognostic assessment: an accurate and fac-
eliminating the mass effect. For surgical success, neurosur- ile diagnosis-specific tool to estimate survival for patients with brain
geons must decide which patients are appropriate candidates. metastases. J Clin Oncol 2012;30:419-25.

169
Neurosurgical Update for BM

10. Narita Y, Sato S, Kayama T. Review of the diagnosis and treatment of rent applications of diffusion tensor imaging and tractography in intra-
brain metastases. Jpn J Clin Oncol 2022;52:3-7. cranial tumor resection. Front Oncol 2019;9:426.
11. Valiente M, Ahluwalia MS, Boire A, Brastianos PK, Goldberg SB, Lee 30. Hervey-Jumper SL, Berger MS. Insular glioma surgery: an evolution of
EQ, et al. The evolving landscape of brain metastasis. Trends Cancer thought and practice. J Neurosurg 2019;130:9-16.
2018;4:176-96. 31. Nimsky C, Ganslandt O, Hastreiter P, Fahlbusch R. Intraoperative com-
12. Hatiboglu MA, Akdur K, Sawaya R. Neurosurgical management of pa- pensation for brain shift. Surg Neurol 2001;56:357-64; discussion 364-5.
tients with brain metastasis. Neurosurg Rev 2020;43:483-95. 32. Catapano G, Sgulò FG, Acurio Padilla PE, Spennato P, Di Nuzzo G,
13. Gaspar L, Scott C, Rotman M, Asbell S, Phillips T, Wasserman T, et al. Boniello V, et al. Palatal position of patient tracker for magnetic neuro-
Recursive partitioning analysis (RPA) of prognostic factors in three Ra- navigation system: technical note. World Neurosurg 2018;116:105-9.
diation Therapy Oncology Group (RTOG) brain metastases trials. Int 33. Krieg SM, Schäffner M, Shiban E, Droese D, Obermüller T, Gempt J, et
J Radiat Oncol Biol Phys 1997;37:745-51. al. Reliability of intraoperative neurophysiological monitoring using
14. Sperduto PW, Kased N, Roberge D, Xu Z, Shanley R, Luo X, et al. Effect motor evoked potentials during resection of metastases in motor-elo-
of tumor subtype on survival and the graded prognostic assessment quent brain regions: clinical article. J Neurosurg 2013;118:1269-78.
for patients with breast cancer and brain metastases. Int J Radiat Oncol 34. Zuo F, Hu K, Kong J, Zhang Y, Wan J. Surgical management of brain me-
Biol Phys 2012;82:2111-7. tastases in the perirolandic region. Front Oncol 2020;10:572644.
15. Sperduto PW, Yang TJ, Beal K, Pan H, Brown PD, Bangdiwala A, et al. 35. Gutzwiller EM, Cabrilo I, Radovanovic I, Schaller K, Boëx C. Intraop-
Estimating survival in patients with lung cancer and brain metastases: erative monitoring with visual evoked potentials for brain surgeries. J
an update of the graded prognostic assessment for lung cancer using Neurosurg 2019;130:654-60.
molecular markers (Lung-molGPA). JAMA Oncol 2017;3:827-31. 36. Zileli M, Idiman F, Hiçdönmez T, Ovül I, Tunçbay E. A comparative
16. Sperduto PW, Jiang W, Brown PD, Braunstein S, Sneed P, Wattson DA, study of brain-stem auditory evoked potentials and blink reflexes in
et al. Estimating survival in melanoma patients with brain metastases: posterior fossa tumor patients. J Neurosurg 1988;69:660-8.
an update of the graded prognostic assessment for melanoma using 37. Sayyahmelli S, Aydin I, Wheeler B, Baskaya MK. Mapping of the inter-
molecular markers (Melanoma-molGPA). Int J Radiat Oncol Biol Phys nal capsule with subcortical stimulation for gross-total resection of a
2017;99:812-6. thalamic metastatic tumor. Neurosurg Focus 2018;45(VideoSuppl2):V7.
17. Sperduto PW, Deegan BJ, Li J, Jethwa KR, Brown PD, Lockney N, et al. 38. Han SJ, Morshed RA, Troncon I, Jordan KM, Henry RG, Hervey-Jumper
Estimating survival for renal cell carcinoma patients with brain metas- SL, et al. Subcortical stimulation mapping of descending motor pathways
tases: an update of the Renal Graded Prognostic Assessment tool. Neu- for perirolandic gliomas: assessment of morbidity and functional out-
ro Oncol 2018;20:1652-60. come in 702 cases. J Neurosurg 2018;131:201-8.
18. Sperduto PW, Fang P, Li J, Breen W, Brown PD, Cagney D, et al. Esti- 39. Duffau H, Peggy Gatignol ST, Mandonnet E, Capelle L, Taillandier L.
mating survival in patients with gastrointestinal cancers and brain me- Intraoperative subcortical stimulation mapping of language pathways
tastases: an update of the graded prognostic assessment for gastrointes- in a consecutive series of 115 patients with Grade II glioma in the left
tinal cancers (GI-GPA). Clin Transl Radiat Oncol 2019;18:39-45. dominant hemisphere. J Neurosurg 2008;109:461-71.
19. To KKW, Fong W, Cho WCS. Immunotherapy in treating EGFR-mu- 40. Duffau H. Intraoperative direct subcortical stimulation for identifica-
tant lung cancer: current challenges and new strategies. Front Oncol tion of the internal capsule, combined with an image-guided stereotac-
2021;11:635007. tic system during surgery for basal ganglia lesions. Surg Neurol 2000;
20. Dimitriou F, Long GV, Menzies AM. Novel adjuvant options for cuta- 53:250-4.
neous melanoma. Ann Oncol 2021;32:854-65. 41. Raabe A, Beck J, Schucht P, Seidel K. Continuous dynamic mapping of
21. Carapella CM, Gorgoglione N, Oppido PA. The role of surgical resec- the corticospinal tract during surgery of motor eloquent brain tumors:
tion in patients with brain metastases. Curr Opin Oncol 2018;30:390-5. evaluation of a new method. J Neurosurg 2014;120:1015-24.
22. Hatiboglu MA, Chang EL, Suki D, Sawaya R, Wildrick DM, Weinberg 42. Yingling CD, Ojemann S, Dodson B, Harrington MJ, Berger MS. Iden-
JS. Outcomes and prognostic factors for patients with brainstem me- tification of motor pathways during tumor surgery facilitated by mul-
tastases undergoing stereotactic radiosurgery. Neurosurgery 2011;69: tichannel electromyographic recording. J Neurosurg 1999;91:922-7.
796-806. 43. Nossek E, Korn A, Shahar T, Kanner AA, Yaffe H, Marcovici D, et al.
23. Li B, Yu J, Suntharalingam M, Kennedy AS, Amin PP, Chen Z, et al. Intraoperative mapping and monitoring of the corticospinal tracts with
Comparison of three treatment options for single brain metastasis from neurophysiological assessment and 3-dimensional ultrasonography-
lung cancer. Int J Cancer 2000;90:37-45. based navigation. J Neurosurg 2011;114:738-46.
24. Crossen JR, Garwood D, Glatstein E, Neuwelt EA. Neurobehavioral 44. Shiban E, Krieg SM, Haller B, Buchmann N, Obermueller T, Boeckh-
sequelae of cranial irradiation in adults: a review of radiation-induced Behrens T, et al. Intraoperative subcortical motor evoked potential
encephalopathy. J Clin Oncol 1994;12:627-42. stimulation: how close is the corticospinal tract? J Neurosurg 2015;123:
25. Meyers CA, Brown PD. Role and relevance of neurocognitive assess- 711-20.
ment in clinical trials of patients with CNS tumors. J Clin Oncol 2006; 45. Okuda T, Kataoka K, Yabuuchi T, Yugami H, Kato A. Fluorescence-
24:1305-9. guided surgery of metastatic brain tumors using fluorescein sodium. J
26. Tallet AV, Azria D, Barlesi F, Spano JP, Carpentier AF, Gonçalves A, et Clin Neurosci 2010;17:118-21.
al. Neurocognitive function impairment after whole brain radiothera- 46. Hamamcıoğlu MK, Akçakaya MO, Göker B, Kasımcan MÖ, Kırış T.
py for brain metastases: actual assessment. Radiat Oncol 2012;7:77. The use of the YELLOW 560 nm surgical microscope filter for sodium
27. Gondi V, Deshmukh S, Brown PD, Wefel JS, Tome W, Armstrong T, et fluorescein-guided resection of brain tumors: our preliminary results in
al. NRG Oncology CC001: A phase III trial of hippocampal avoidance a series of 28 patients. Clin Neurol Neurosurg 2016;143:39-45.
(HA) in addition to whole-brain radiotherapy (WBRT) plus meman- 47. Marhold F, Mercea PA, Scheichel F, Berghoff AS, Heicappell P, Kiesel B,
tine to preserve neurocognitive function (NCF) in patients with brain et al. Detailed analysis of 5-aminolevulinic acid induced fluorescence
metastases (BM) [abstract]. J Clin Oncol 2019;37(15 Suppl):2009. in different brain metastases at two specialized neurosurgical centers:
28. Brown PD, Gondi V, Pugh S, Tome WA, Wefel JS, Armstrong TS, et al. experience in 157 cases. J Neurosurg 2020;133:1032-43.
Hippocampal avoidance during whole-brain radiotherapy plus me- 48. Kamp MA, Grosser P, Felsberg J, Slotty PJ, Steiger HJ, Reifenberger G,
mantine for patients with brain metastases: phase III trial NRG oncol- et al. 5-Aminolevulinic acid (5-ALA)-induced fluorescence in intrace-
ogy CC001. J Clin Oncol 2020;38:1019-29. rebral metastases: a retrospective study. Acta Neurochir (Wien) 2012;
29. Costabile JD, Alaswad E, D’Souza S, Thompson JA, Ormond DR. Cur- 154:223-8.

170 Brain Tumor Res Treat 2022;10(3):164-171

 J Yoo et al.

49. Baumert BG, Rutten I, Dehing-Oberije C, Twijnstra A, Dirx MJ, De- 53. Patel P, Patel NV, Danish SF. Intracranial MR-guided laser-induced
bougnoux-Huppertz RM, et al. A pathology-based substrate for target thermal therapy: single-center experience with the Visualase thermal
definition in radiosurgery of brain metastases. Int J Radiat Oncol Biol therapy system. J Neurosurg 2016;125:853-60.
Phys 2006;66:187-94. 54. Kamath AA, Friedman DD, Hacker CD, Smyth MD, Limbrick DD Jr,
50. Neves S, Mazal PR, Wanschitz J, Rudnay AC, Drlicek M, Czech T, et al. Kim AH, et al. MRI-guided interstitial laser ablation for intracranial
Pseudogliomatous growth pattern of anaplastic small cell carcinomas lesions: a large single-institution experience of 133 cases. Stereotact
metastatic to the brain. Clin Neuropathol 2001;20:38-42. Funct Neurosurg 2017;95:417-28.
51. Yoo H, Kim YZ, Nam BH, Shin SH, Yang HS, Lee JS, et al. Reduced lo- 55. Missios S, Bekelis K, Barnett GH. Renaissance of laser interstitial ther-
cal recurrence of a single brain metastasis through microscopic total mal ablation. Neurosurg Focus 2015;38:E13.
resection. J Neurosurg 2009;110:730-6. 56. Asher AL, Burri SH, Wiggins WF, Kelly RP, Boltes MO, Mehrlich M,
52. Kamp MA, Dibué M, Niemann L, Reichelt DC, Felsberg J, Steiger HJ, et al. A new treatment paradigm: neoadjuvant radiosurgery before
et al. Proof of principle: supramarginal resection of cerebral metastases surgical resection of brain metastases with analysis of local tumor re-
in eloquent brain areas. Acta Neurochir (Wien) 2012;154:1981-6. currence. Int J Radiat Oncol Biol Phys 2014;88:899-906.

171