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CLINICAL ARTICLE J Neurosurg 127:790–797, 2017 Surgical benefits of combined awake craniotomy and intraoperative
CLINICAL ARTICLE J Neurosurg 127:790–797, 2017 Surgical benefits of combined awake craniotomy and intraoperative

CLINICAL ARTICLE

J Neurosurg 127:790–797, 2017

Surgical benefits of combined awake craniotomy and intraoperative magnetic resonance imaging for gliomas associated with eloquent areas

Kazuya Motomura, MD, PhD, 1 Atsushi Natsume, MD, PhD, 1 Kentaro Iijima, MD, 1 Shunichiro Kuramitsu, MD, PhD, 1 Masazumi Fujii, MD, PhD, 2 Takashi Yamamoto, MD, 1 Satoshi Maesawa, MD, PhD, 3 Junko Sugiura, ST, 4 and Toshihiko Wakabayashi, MD, PhD 1

1 Department of Neurosurgery, Nagoya University School of Medicine, Nagoya; 2 Department of Neurosurgery, Fukushima Medical University, Fukushima; 3 Brain and Mind Research Center, Nagoya University Graduate School of Medicine; and 4 Department of Rehabilitation, Nagoya University Hospital, Nagoya, Japan

OBJECTIVE Maximum extent of resection (EOR) for lower-grade and high-grade gliomas can increase survival rates of patients. However, these infiltrative gliomas are often observed near or within eloquent regions of the brain. Awake sur- gery is of known benefit for the treatment of gliomas associated with eloquent regions in that brain function can be pre- served. On the other hand, intraoperative MRI (iMRI) has been successfully used to maximize the resection of tumors, which can detect small amounts of residual tumors. Therefore, the authors assessed the value of combining awake craniotomy and iMRI for the resection of brain tumors in eloquent areas of the brain. METHODS The authors retrospectively reviewed the records of 33 consecutive patients with glial tumors in the eloquent brain areas who underwent awake surgery using iMRI. Volumetric analysis of MRI studies was performed. The pre-, intra-, and postoperative tumor volumes were measured in all cases using MRI studies obtained before, during, and after tumor resection. RESULTS Intraoperative MRI was performed to check for the presence of residual tumor during awake surgery in a total of 25 patients. Initial iMRI confirmed no further tumor resection in 9 patients (36%) because all observable tumors had already been removed. In contrast, intraoperative confirmation of residual tumor during awake surgery led to further tumor resection in 16 cases (64%) and eventually an EOR of more than 90% in 8 of 16 cases (50%). Furthermore, EOR benefiting from iMRI by more than 15% was found in 7 of 16 cases (43.8%). Interestingly, the increase in EOR as a result of iMRI for tumors associated mainly with the insular lobe was significantly greater, at 15.1%, than it was for the other tumors, which was 8.0% (p = 0.001). CONCLUSIONS This study revealed that combining awake surgery with iMRI was associated with a favorable surgical outcome for intrinsic brain tumors associated with eloquent areas. In particular, these benefits were noted for patients with tumors with complex anatomy, such as those associated with the insular lobe.

https://thejns.org/doi/abs/10.3171/2016.9.JNS16152

KEY WORDS awake craniotomy; intraoperative magnetic resonance imaging; glioma; eloquent area; extent of resection; volumetric analysis; oncology

T he ideal treatment strategy for both lower-grade and high-grade gliomas has recently been reported to be maximal tumor resection as the initial therapeutic

option. 11,16,24 A large number of studies based on objec- tive evaluation of the extent of resection (EOR) in cases of gliomas showed that a total resection, or maximum EOR, significantly increased not only the progression-free sur- vival but also the overall survival (OS). 3,11,15,24,26,29 Regard-

ing lower-grade gliomas in particular, one evidence-based clinical practice guideline recommends resection over ob- servation to improve OS for patients, a recommendation based on high levels of evidence. 1 However, these infiltra- tive gliomas are often observed near or within eloquent regions of the brain, 8,25 which means that their removal in- creases the risk of neurological damage, including motor, language, and cognitive dysfunction. Therefore, the gold-

ABBREVIATIONS EOR = extent of resection; iMRI = intraoperative MRI; OS = overall survival. SUBMITTED January 19, 2016. ACCEPTED September 13, 2016. INCLUDE WHEN CITING Published online January 6, 2017; DOI: 10.3171/2016.9.JNS16152.

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standard treatment for gliomas associated with eloquent regions is awake surgery with direct electrocortical stim- ulation to preserve brain function. 10,22 The goal of awake surgery is to achieve the maximum degree of tumor resec- tion while determining the functional tumor boundary by using both cortical and subcortical mapping. 7,10,12 Intraoperative MRI (iMRI) provides information about EOR and imaging data sets, incorporating anatomical changes that occur as a result of surgical retraction, dural opening, brain shift, gravity, and loss of CSF. 19,30 iMRI can be an important tool allowing neurosurgeons to maximize the EOR of gliomas by overcoming the effect of intraop- erative brain shifting. In addition, iMRI can detect small amounts of residual tumors, which allows surgeons to maximize EOR while minimizing postoperative neuro- logical deficits. 18 Thus, by combining awake craniotomy, using cortical and subcortical stimulation, with iMRI, functional and anatomical brain information can be obtained and used to avoid neurological complications. In this study, we aimed to investigate the significance of combining awake craniotomy and iMRI for the resections of brain tumors located in eloquent areas of the brain.

Methods

Patient Population We retrospectively reviewed the records of 33 consecu- tive patients with glial tumors located in eloquent areas of the brain who underwent awake surgery at Nagoya Uni- versity Hospital from December 2012 through July 2014. All patients had tumors that were anatomically associ- ated with eloquent brain regions including areas involving motor, language, and/or cognitive function, as shown on preoperative MRI. When possible, we tried to use intra- operative MRI (iMRI) to evaluate the EOR and maximize tumor resection during awake craniotomy. 13,27 The diagno- sis of brain tumor was established by a histological exami- nation based on the World Health Organization (WHO) guidelines 16,17 independently by at least two expert neu- ropathologists. Grade II and III gliomas were defined as lower-grade gliomas, as previously reported. 31 The study was approved by the institutional review board at Nagoya University Hospital and complied with all provisions of the Declaration of Helsinki.

Preoperative Evaluation The presenting neurological symptoms and preopera- tive neurological examination findings were assessed at admission before the awake surgery. Handedness was assessed using a standardized ques- tionnaire (Edinburgh Handedness Inventory). 21 Hemi- spheric language dominance was determined according to functional MRI findings or WADA testing. Functional MRI was performed using a MAGNETOM Verio (Sie- mens) 3.0-T scanner with a 32-channel head coil. WADA testing, performed as previously described, 32 was conduct- ed by injecting propofol into the internal carotid artery. In addition, neurocognitive status and language func- tion were assessed by speech therapists and occupational therapists using Standard Language Test of Aphasia, the

Benefits of iMRI and awake surgery for gliomas in eloquent areas

third edition of the Wechsler Adult Intelligence Scale, and the Wechsler Memory Scale–Revised 1 week before and after the awake craniotomy. Preoperative brain images, including 3D T1-weighted images, conventional MRI images (T1- and T2-weighted images), and diffusion-weighted images, were acquired using a 3.0-T scanner (Trio, Siemens). Images were coreg- istered and fused using the automatic image fusion soft- ware included in Brainlab iPlan Cranial 2.6 and 3.0. 20 According to these preoperative findings, we determined the final target for tumor resection and aimed to achieve gross-total removal of the tumor, despite the difficulty of excising tumors located in eloquent areas.

Intraoperative Mapping All patients underwent surgery using an asleep-awake- asleep technique so that intraoperative brain mapping could be performed using direct brain stimulation. 10 A wide craniotomy was performed, and intraoperative neu- ronavigation was used to delineate the margin of the tu- mor. Furthermore, somatosensory evoked potentials were evaluated using a strip electrode (6 contacts) to determine the location of the central sulcus. Electrocorticograms were recorded using strip electrodes to detect the appear- ance of the afterdischarge during direct brain stimulation and tumor resection. The awake surgery technique allowed us to use intra- operative functional mapping, particularly language, cor- tical, and subcortical mapping, by using direct electrical stimulation. We used a bipolar stimulator with a 2-mm diameter and a 5-mm interelectrode distance (Unique Medical) to deliver a biphasic current (pulse frequency 60 Hz; single pulse phase duration 0.5 msec; amplitude 2–8 mA) to the brains of these awake patients. A Neuro- master MEE-1200 system (Nihon Kohden) was used for intraoperative neurophysiological monitoring during the procedure. First, cortical mapping was performed after opening the dura mater. We used counting tasks and object-nam- ing tasks presented to patients on a monitor to identify the cortical language sites affected by electrical stimulations. Speech therapists evaluated and analyzed the type of lan- guage disturbance, such as speech arrest, anomia, dysar- thria, anarthria, speech slowness, initiation troubles, per- severation, and paraphasia. After evaluation of language disturbances, each of the eloquent areas was marked using number tags on the brain surface. After cortical mapping was completed, the lesion re- section was started by using a subpial excision technique. We removed the tumor to the level of the white matter, while frequently checking the patient’s response using subcortical stimulation. Thus, subcortical mapping en- abled us to determine the functional boundary between tumor and white matter.

Intraoperative MRI We performed iMRI using a 0.4-T vertical field MR scanner (Aperto Inspire, Hitachi) installed in the operat- ing room of the Brain Theater of Nagoya University Hos- pital just after tumor resection during awake craniotomy.

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In the present study, the intraoperative imaging proto- col included T1- and T2-weighted imaging and, if neces- sary, T1-weighted imaging with injection of contrast me- dium. Initial iMRI was performed based on the surgeon’s judgment that most targeted lesions were completely re- moved according to functional boundaries by using awake brain mapping. If remaining resectable tumor was found, we removed the additional tumor, and iMRI investigation was repeated to ensure that the surgical goal was achieved based on the preoperative plans.

Volumetric Analysis Volumetric analysis of MR images was performed on a 3D basis using the cranial planning software included in the Brainlab iPlan Cranial 2.6 and 3.0. 20 The pre-, in- tra-, and postoperative tumor volumes were measured in all patients using contrast-enhanced T1-weighted or T2- weighted MR images obtained before, during, and after tumor resection. The EOR was calculated as follows: (pre- operative tumor volume - postoperative tumor volume)/ preoperative tumor volume. 29 The increase in EOR as a result of iMRI was calculated as follows: (final EOR - EOR on iMRI).

Statistical Analysis Statistical analysis was performed using the statistical software SPSS for Windows, version 22.0 (SPSS Inc.). The t-test and the Mann-Whitney U-test were used to test for association between clinical variables and EOR of the tu- mor. A significance level of p = 0.05 was assumed.

Results

Clinical Parameters Between December 2012 and July 2014, 33 consecu- tive patients with glial tumors associated with the elo- quent brain areas who underwent awake surgery were enrolled in the current study. Their clinical characteristics are summarized in Table 1. Histologically, there were 26 lower-grade diffuse gliomas, including 19 WHO Grade II gliomas (9 diffuse astrocytomas, 7 oligoastrocytomas, 2 oligodendrogliomas, and 1 pleomorphic xanthoastrocyto- ma), 7 WHO Grade III gliomas (2 anaplastic astrocytomas and 5 anaplastic oligodendrogliomas), and 4 high-grade gliomas (glioblastoma). This study group comprised 25 men and 8 women aged 28–67 years (median 41 years). The tumor was located in the left hemisphere in 30 cases (90.9%) and in the right hemisphere in 3 cases (9.1%). The majority of the tumors were located in the left frontal lobe (n = 15, 45.5%), followed by the insular lobe plus the tem- poral or frontal lobe (n = 11, 33.3%), the parietal lobe (n = 5, 15.2%), the temporal lobe (n = 1, 3.0%), and the occipital lobe (n = 1, 3.0%). The median tumor volume, measured on MRI at preoperative diagnosis, was 46.1 cm 3 (range 0.6–196.4 cm 3 ). Final EOR 90% was achieved in 15 pa- tients (45.5%), and 18 patients (54.5%) had an EOR < 90%. Operative time was calculated from starting the skin incision to finishing the wound closure, including the time for awake functional mapping, tumor removal, iMRI, and

792 J Neurosurg Volume 127 • October 2017

TABLE 1. Clinical characteristics

Parameter

No. of Pts (n = 33)

Percentage

Age (yrs)

Median

41

Range

28–67

Sex

Male

25

75.8

Female

8

24.2

Histological type

Diffuse astrocytoma

9

27.2

Oligodendroglioma

2

6.1

Oligoastrocytoma

7

21.2

Anaplastic astrocytoma

2

6.1

Anaplastic oligodendroglioma

5

15.2

Glioblastoma

4

12.1

Pleomorphic xanthoastrocytoma

1

3.0

Gliosis

3

9.1

Side of lesion

Left

30

90.9

Right

3

9.1

Tumor location

Frontal

15

45.5

Insular mainly

11

33.3

Parietal

5

15.2

Temporal

1

3.0

Occipital

1

3.0

iMRI

Performed

25

75.8

Not performed

8

24.2

Tumor vol (cm 3 )

Median

46.1

Range

0.6–196.4

Final EOR

≥90%

15

45.5

<90%

18

54.5

Insular mainly = insular plus temporal and/or frontal; Pt = patient.

further resection of residual tumor. The mean total opera- tive time was 7.8 hours (range 4.4–12.0 hours; Table 2). Total operative time exceeded 8 hours in 9 patients, which included 7 cases of insular tumor, 1 of frontal tumor, and 1 of parietal tumor. The mean iMRI scanning time was 26.8 minutes (range 20–36 minutes; Table 2).

Neurological and Neuropsychological Outcomes In the postoperative period, 10 patients (30%) had new transient speech disturbance and 4 patients (12%) devel- oped permanent speech disorders. Three of 4 patients with permanent speech disorders already had aphasia or apraxia of speech preoperatively. Four patients (12%) had transient motor disorders, and none had permanent motor disturbance (Table 3). One patient (3%) experienced post- operative hemorrhage and 2 patients (6%) showed seman- tic paraphasia during the postoperative course (Table 3).

Benefits of iMRI and awake surgery for gliomas in eloquent areas

TABLE 2. Clinical detailed data of 25 patients who underwent iMRI during the awake craniotomy

Pt

Age

Tumor

Tumor

Total Op

Op Time to 1st iMRI (hrs)

Scanning Time for iMRI (mins)

Op Time After iMRI (hrs)

No.

(yrs)

Sex

Type

Location

Time (hrs)

1

44

M

OA

Frontal

7

4.6

30

1.7

2

32

M

OG

Insula mainly

9.2

6.6

20

1.9

3

40

F

OA

Frontal

6.7

4.1

32

1.4

4

44

F

AO

Frontal

4.4

5.4

25

1.7

6

43

M

OA

Insula mainly

7.9

6.1

35

1.2

7

46

M

DA

Insula mainly

7.5

5

20

1.5

8

45

M

Gliosis

Frontal

5.5

3.3

20

1.7

11

48

M

GBM

Frontal

6.8

4.4

25

1.8

13

54

M

AO

Frontal

7.8

3.6

32

3.1

14

38

M

Gliosis

Frontal

6.3

3.9

30

1.3

15

67

M

AA

Insula mainly

9

6.8

25

1.7

16

42

F

OA

Parietal

5.8

3.9

35

1.2

18

64

M

Gliosis

Frontal

7.6

4.8

30

1.9

19

37

F

DA

Frontal

7.1

4.6

20

1.7

21

41

M

OA

Frontal

6.1

3.4

20

2.1

22

63

M

DA

Insula mainly

9.8

7.1

25

2

24

72

M

DA

Insula mainly

10.1

7.7

36

1.8

25

28

M

PXA

Parietal

9.5

7.6

30

1.4

26

37

F

GBM

Insula mainly

11.3

8.1

20

2.4

27

36

F

DA

Insula mainly

10.7

7.7

20

1.9

29

29

M

AA

Insula mainly

6.6

4.1

35

1.3

30

56

F

DA

Temporal

4.7

3.2

35

0.9

31

43

M

AO

Frontal

9.3

6.4

24

1.9

32

67

F

GBM

Insula mainly

12

6.9

22

1.5

33

66

M

AO

Frontal

7.3

5.5

25

1.4

AA = anaplastic astrocytoma; AO = anaplastic oligodendroglioma; DA = diffuse astrocytoma; GBM = glioblastoma; OA = oligoastrocytoma; OG = oligodendroglioma; PXA = pleomorphic xanthoastrocytoma.

Results of neuropsychological assessment are also listed in Supplementary Table 1. Preoperative functional MRI allowed us to localize the Broca and Wernicke cortical areas in all patients.

TABLE 3. Summary of preoperative and postoperative neurological deficits

Deficit or Complication

No. of Pts

Preoperative deficit

Aphasia

2

Apraxia of speech

1

Postoperative deficit

Transient speech disturbance

10

Transient motor disturbance

3

Permanent speech disturbance

4

Permanent motor disturbance

0

Postoperative complication

Postoperative hemorrhage

1

Semantic paraphasia

2

Effect of iMRI on Awake Surgery in Patients Intraoperative MRI was performed to check for the presence of residual tumor during awake surgery in a total of 25 patients. If residual tumor was found using iMRI, further tumor resection was performed, unless there was a risk of damaging eloquent brain regions (Pa- tient 32, Fig. 1). Of the remaining 8 patients, we aborted awake surgery midstream in 3 cases because the disturbance of con- sciousness persisted to the end. In 5 patients, iMRI could not be performed because of the patient’s position (e.g., lateral position). Initial iMRI confirmed no further tumor resection in 9 patients (36%) because all observable tumors had al- ready been removed. In such cases, the mean final EOR of these patients was 92.8% (Table 4). Interestingly, these cases were characterized by the presence of frontal tu- mors (55.6%). In contrast, intraoperative confirmation of residual tumor during awake surgery led to further tumor resection in 16 cases (64%) and eventual EOR of more than 90% in 8 of 16 cases (50%) (Table 5). Furthermore, EOR benefiting from iMRI by more than 15% was found in 7 of 16 cases (43.8%). Thus, the use of iMRI increased EOR of the tumor in patients undergoing awake surgery.

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K. Motomura et al. FIG. 1. Tumor volumes on the pre, intra-, and postoperative MRI in

FIG. 1. Tumor volumes on the pre, intra-, and postoperative MRI in Patient 32. Intraoperative MRI revealing a residual tumor (red- outlined areas). Eventual EOR was 97.6%. Figure is available in color online only.

Benefits of Combined iMRI and Awake Craniotomy for Patients With Tumors Associated With the Insular Lobe Next, we sought to determine which cases had benefit- ed most from the use of iMRI during awake surgery. We focused on the 25 patients who underwent iMRI during awake craniotomy (Tables 4 and 5). These cases consisted of frontal tumors (12 cases), insular tumors (10 cases), pa- rietal tumors (2 cases), and temporal tumor (1 case). No- tably, the increase in EOR as a result of iMRI for tumors associated mainly with the insular lobe was significantly greater, at 15.1%, than the increase in EOR for the other tumors, which was 8.0% (p = 0.001) (Table 6).

Discussion

To preserve brain function of structures located in the eloquent areas, functional brain mapping during awake craniotomy has been increasingly performed at several in- stitutions, and a greater need for the procedure has been emphasized. 6,7,10,11,22 This is because both anatomical and functional variability of cognitive functions, including lan- guage function, has been shown even in healthy human beings. 33 This variation in cognitive functional areas in- creases in cases of intrinsic brain tumors, including glio- mas, which invade the brain itself. In such cases, normal cerebral functions might shift to other regions due to brain plasticity, especially in slow-growing tumors such as low- er-grade gliomas. 5 Therefore, “tailor-made awake surgery” is essential to detect cortical and subcortical functional or- ganization for each brain tumor patient. Based on the cor- tical-subcortical functional boundaries, tumors associated with eloquent areas should be resected during awake cra-

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niotomy. 11 By using awake craniotomy, brain tumor treat- ment can be safe, practical, and effective at the outcome stage. 28 A recent study revealed a 3.4% rate of permanent severe neurological deficits in patients after resections with intraoperative stimulation mapping. 4 Even when using awake brain mapping, a small amount of tumor was sometimes left around the tumor cavity in the complex anatomical brain structures such as deep re- gions close to the basal ganglia. Furthermore, there were some advantages to tumor removal under iMRI guidance, including the ability to define tumor targets and lesion margins and identify normal brain anatomical structures,

TABLE 4. Clinical results of 9 patients who needed no further resection after checking iMRI during the awake craniotomy

Pt

Age

Tumor

Tumor

Tumor Vol (cm 3 )

Final

No.

(yrs)

Sex

Type

Location

Initial

Postop

EOR (%)

4

44

F

AO

Frontal

32.1

2.2

93.2

7

46

M

DA

Insular mainly

65.2

0.8

98.7

11

48

M

GBM

Frontal

31.3

2.1

93.2

13

54

M

AO

Frontal

38.9

3.9

90.1

16

42

F

OA

Parietal

1.2

0.2

87.7

18

64

M

Gliosis

Frontal

85.1

0

100

25

28

M

PXA

Parietal

0.6

0

100

30

56

F

DA

Temporal

5.6

0.3

94.4

33

66

M

AO

Frontal

69.7

15.4

77.9

Mean final EOR (%)

 

92.8

Benefits of iMRI and awake surgery for gliomas in eloquent areas

TABLE 5. Clinical results of 16 patients who underwent further resection after iMRI was checked during the awake craniotomy

Pt

Age

Tumor

Tumor

Increased Rate of EOR Due to iMRI (%)

No.

(yrs)

Sex

Type

Location

Initial

Intraop

Postop

on iMRI

Final

1

44

M

OA

Frontal

19

1.5

0

92

100

8

2

32

M

OG

Insular mainly

67.8

41.6

33.4

38.6

50.7

12.1

3

40

F

OA

Frontal

46.1

2.9

2.7

93.6

94.2

0.6

6

43

M

OA

Insular mainly

105.7

25.5

9.6

75.8

90.9

15.1*

8

45

M

Gliosis

Frontal

6.8

1.6

0.7

77.2

90.3

13.2

14

38

M

Gliosis

Frontal

8.8

1.6

0

81.4

100

18.6*

15

67

M

AA

Insular mainly

107.6

80.5

49.5

25.2

54

28.7*

19

37

F

DA

Frontal

86.1

45.4

43.6

47.3

49.3

2

21

41

M

OA

Frontal

8.8

0.9

0.4

89.6

95.6

6

22

63

M

DA

Insular mainly

85.1

21.4

8.5

74.9

90

15.1*

24

72

M

DA

Insular mainly

24.9

12

3.4

51.8

86.2

34.3*

26

37

F

GBM

Insular mainly

118.7

32.6

18.4

72.5

84.5

12

27

36

F

DA

Insular mainly

61.6

30

16.5

51.2

73.3

22.1*

29

29

M

AA

Insular mainly

196.4

147.9

137.9

24.7

29.8

5.1

31

43

M

AO

Frontal

101.9

39.9

26.2

60.9

74.3

13.4

32

67

F

GBM

Insular mainly

31.2

15.8

0.8

50.6

97.6

47*

Tumor Vol (cm 3 )

EOR (%)

* Shows that the increased rate of EOR benefited from iMRI more than 15%.

even in the dynamic changes of CSF during tumor resec- tion. In addition, the utilities of iMRI were to detect unan- ticipated residual disease, to update intraoperative neuro- navigation registration accounting for brain shift, and to exclude the presence of any intraoperative complications including hemorrhagic events. The use of iMRI was significantly beneficial in detect- ing the residual tumor to achieve a more complete resec- tion of brain tumors close to the eloquent areas. In the present study, just after the iMRI, in 9 cases (36%) we ac- complished maximal resection of the target tumor without need for further removal (Table 4). However, in 16 cases (64%) the EOR increased using further resection thanks to iMRI findings (Table 5). Of these 16, 9 (56.3%) were tumors in areas associated with the insular lobe. Insular gliomas are surgically challenging tumors be- cause of their complex anatomy and the adjacent cortices and white matter tracts associated with language func- tions, and because of the vascular branch and important perforating arteries such as the lenticulostriate artery and long insular artery. The insula is very close to perisylvian language areas, Broca’s and Wernicke’s areas, the primary motor and sensory areas of the lower portion of the face, and the white matter pathways traversing these regions.

Thus, brain tumors located in the insular region had long been considered inoperable, often operated on only for bi- opsy purposes. Berger et al. and Duffau et al., who are expert glioma surgeons, have demonstrated that it is cru- cial to perform functional mapping prior to the removal of insular glioma because of the critical nature of both insu- lar and peri-insular structures. 2,9,14,23 Although they used functional brain mapping without iMRI, insular tumors present a surgical challenge without the help of structural and functional imaging. Using iMRI for such challenging tumors with compli- cated structures provides rewarding surgical outcomes and can assist neurosurgeons with intraoperative surgical planning. In the present study, we have compared the clini- cal data of insular and other tumors in patients who un- derwent further resection after using iMRI during awake craniotomy (Table 6). Statistically, the benefit associated with the combination of iMRI and the awake craniotomy was shown in patients whose tumors were located near the insular lobe (Table 6). This finding suggests that iMRI can detect the small amount of remnant tumor after awake brain mapping to define the functional boundary of the tu- mor using direct cortical and subcortical stimulation. The combination of the complementary functions of iMRI and

TABLE 6. Comparison of clinical data between insular and the other tumors in patients who underwent further resection after iMRI was checked during the awake craniotomy

Tumor

No. of

Mean Initial Tumor Vol (cm 3 )

Median EOR (%)

Increased Rate of EOR Due to iMRI (%)

p

Location

Pts

on iMRI (%)

Final

Value

Insular mainly

10

88.87

51.2

84.5

15.1

0.001

Other

15

39.64

81.4

94.2

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awake surgery will enable treatment of insular tumors due to the highly functional nature of the insula and surround- ing brain as well as the insula’s difficult access with the hidden surface underlying the frontal and temporal oper- culum.

Conclusions

In summary, this study demonstrated that in cases of intrinsic brain tumors, including lower- and high-grade gliomas associated with eloquent areas of the brain, the combination of awake craniotomy and iMRI was associat- ed with a favorable surgical outcome. These benefits were, in particular, noted for patients with tumors with complex anatomy, such as those associated with the insular lobe. Our results are limited compared with those of a pro- spective clinical trial, as retrospective studies can be in- fluenced by unrecognized biases. However, this study pro- vides essential information about the treatment of gliomas associated with eloquent areas of the brain. The collection of evidence for combined awake craniotomy and iMRI will help further treatment of this disease and hopefully create a novel surgical strategy.

Acknowledgments

We would like to thank Ms. Maki Tobinaga, Mr. Daisuke Hara, and Mr. Yasuyuki Matsui (Department of Rehabilitation, Nagoya University Hospital, Nagoya, Japan) for their wonderful technical assistance. Dr. Motomura was supported by grants from a Grant-in-Aid (B) for Scientific Research from the Ministry of Health, Labor, and Welfare, Japan.

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Disclosures

The authors report no conflict of interest concerning the materi-

Benefits of iMRI and awake surgery for gliomas in eloquent areas

als or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Motomura, Natsume, Wakabayashi. Acquisition of data: Motomura, Iijima, Kuramitsu, Fujii, Yama- moto, Maesawa, Sugiura. Analysis and interpretation of data:

Motomura. Drafting the article: Motomura. Critically revising the article: Motomura, Natsume. Statistical analysis: Motomura. Study supervision: Motomura, Natsume, Wakabayashi.

Supplemental Information

Online-Only Content

Supplemental material is available with the online version of the article. Supplementary Table 1. https://thejns.org/doi/suppl/10.3171/

Correspondence

Kazuya Motomura, Department of Neurosurgery, Nagoya Uni- versity School of Medicine, 65 Tsurumai-cho, Showa-ku, Nagoya 466-8550, Japan. email: kmotomura@med.nagoya-u.ac.jp.

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