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Cortico-cortical evoked potential by single-pulse electrical stimulation is a generally safe procedure

Kobayashi, Katsuya Matsumoto, Riki Usami, Kiyohide Matsuhashi, Masao Shimotake, Akihiro Kikuchi, Takayuki Yoshida, Kazumichi Kunieda, Takeharu Miyamoto, Susumu Takahashi, Ryosuke Ikeda, Akio 神戸大学

2021.05.01

概要

Objective Cortico-cortical evoked potential (CCEP) by single-pulse electrical stimulation (SPES) is useful to investigate effective connectivity and cortical excitability. We aimed to clarify the safety of CCEPs. Methods We retrospectively analyzed 29 consecutive patients with intractable partial epilepsy undergoing chronic subdural grid implantation and CCEP recording. Repetitive SPES (1 Hz) was systematically applied to a pair of adjacent electrodes over almost all electrodes. We evaluated the incidences of afterdischarges (ADs) and clinical seizures. Results Out of 1283 electrode pairs, ADs and clinical seizures were observed in 12 and 5 pairs (0.94% and 0.39%, per electrode pair) in 7 and 3 patients (23.3% and 10.0%, per patient), respectively. Of the 18–82 pairs per patient, ADs and clinical seizures were induced in 0–4 and 0–3 pairs, respectively. Stimulating 4 SOZ (seizure onset zone) (2.5%) and 8 non-SOZ pairs (0.75%) resulted in ADs. We observed clinical seizures in stimulating 4 SOZ (2.5%) and 1 non-SOZ pair (0.09%). The incidence of clinical seizures varied significantly between SOZ and non-SOZ stimulations (p = 0.001), while the difference in AD incidence tended towards significance (p = 0.058). Conclusion Although caution should be taken in stimulating SOZ, CCEP is a safe procedure for presurgical evaluation. Significance CCEP is safe under the established protocol.

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参考文献

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Figure Legends

Figure 1: A representative ECoG of stimulus-induced clinical seizure

(Patient 3)

A: Ictal ECoG induced by SPES on the pair of electrodes on the precentral

gyrus (C19-C20). Repetitive spikes appeared on the B plate, followed by

paroxysmal fast occurring on the C plate (shown in the magenta frames).

The patient showed a habitual seizure characterized by right foot twitches.

The recording band-pass filter was 0.08-600 Hz and the filter for display is

10

1.6-50 Hz.

11

B: Configuration of implanted SDG electrodes. SOZs defined by the initial

12

ictal ECoG changes in the spontaneous seizure are shown as red circles.

13

Abbreviations: ECoG = electrocorticogram; SPES = single-pulse electrical

14

stimulation; SDG = subdural grid; SOZ = seizure-onset zone.

15

16

Figure 2: A representative ECoG of stimulus-induced clinical seizure

17

(Patient 25)

18

A: In this patient (Patient 25), SOZ was not conventionally identified because

19

spontaneous seizure did not occur despite AED reduction. One electrode

20

pair of SPESs (A12-A17) induced a habitual seizure that included

21

hyperventilation and right face twitches. This finally evolved to focal to

22

bilateral tonic-clonic seizure. Clear ictal ECoG changes are highlighted by the

33

Kobayashi et al 34

frames in magenta. The surgical removal of the areas including the pair that

induced the seizure and showed the earliest ECoG changes during the

induced seizure led to seizure freedom for more than 2 years. The recording

band-pass filter was 0.08-300 Hz and the filter for display is 1.6-50 Hz.

B: Configuration of implanted SDG electrodes. Probable SOZs, defined by

this stimulus-induced clinical seizure, are shown as orange circles.

Abbreviations: SOZ = seizure-onset zone; SPES = single-pulse electrical

stimulation; AC-PC line = anterior commissure – posterior commissure line;

VAC line = line vertical to the AC-PC line through the AC; Rt = right; AED =

10

antiepileptic drug; ECoG = electrocorticogram; SDG = subdural grid.

34

Kobayashi et al. 35

Table 1: Patient profile

Patient

1 (1st SDG)

1 (2nd SDG)

10

11

12

13

14

15

16

17

18

19

20

21

22

23

24

25

26

27

28

29

Total

Total except

for Patient 17

Age and

gender

23F

23F

23M

40M

22M

44M

24M

17F

29M

34M

38F

28F

55M

41F

52M

Epilepsy

Etiology

Rt FLE

Rt FLE

Rt OLE

Lt F-PLE

Lt F-TLE

Rt FLE

Lt FLE

Lt TLE

Lt TLE

Rt P-TLE

Lt TLE

Rt PLE

Lt TLE

Lt TLE

Lt TLE

27F

27F

39M

45M

61M

30F

28F

39M

29M

21M

16F

41M

16M

39F

23F

Rt TLE

Rt PLE

Lt FLE

Lt FLE

Lt PLE

Rt TLE

Lt TLE

Rt TLE

Rt FLE

Lt TLE

Lt FLE

Lt TLE

Rt F-T-PLE

Lt FLE

Lt PLE

FCD IA

FCD IA

FCD IIA

Mixed oligoastrocytoma

Gliosis (F), FCD IA (T)

Mixed oligoastrocytoma, FCD IA

FCD IB

FCD IB

HS, FCD IA

Posttraumatic change (P), HS (T), Scar (T)

FCD IIA

Low grade neuroepithelial tumor

Diffuse astrocytoma

FCD IA

Arteriovenous malformation, Gliosis,

Inflammatory infiltration

FCD IA

FCD IIB

FCD IIB

FCD IA

Oligoastrocytoma

FCD IIA, Mild gliosis

Non-neoplastic brain tissue

HS, FCD IA

FCD IA

HS, FCD IA

Dysmorphic neuroepithelial tumor

HS, FCD IA

FCD IC

FCD IIB

FCD IIB

Implanted SDG

electrodes

52

44

52

56

66

48

100

60

102

82

88

48

56

102

110

Total SPES

pairs

27

24

18

22

36

26

50

34

51

55

44

28

27

49

38

SPES pairs for SOZ stim

(ADs and clinical seizures)

5 (3 clinical seizures)

10

4 (2 ADs)

4 (1 AD)

10

SPES pairs for non-SOZ stim

(ADs and clinical seizures)

24

21

16

17 (1 AD)

29 (1 clinical seizure)

24

40

28

47 (1 AD)

46

41

25

23 (3 ADs)

45

28 (1 AD)

76

72

108

104

106

102

106

90

100

82

92

92

162

68

84

40

36

54

50

58

40

55

48

58

53

55

47

82

36

42

1283

1229

n.a.

5 (1 AD)

12

6 (1 clinical seizure)

12

38

29

n.a.

47

50 (1 AD)

38

50

45

50

41

49

35 (1 AD)

78

27

36

162

(4 ADs and 4 clinical seizures)

1067

(8 ADs and 1 clinical seizure)

SPES, single-pulse electrical stimulation; SOZ, seizure onset zone; stim, stimulation; AD, afterdischarge; SDG, subdural grid; FLE, frontal lobe

epilepsy; OLE, occipital lobe epilepsy; PLE, parietal lobe epilepsy; TLE, temporal lobe epilepsy; FCD, focal cortical dysplasia; HS, hippocampal

sclerosis; n.a., not available

35

Kobayashi et al. 36

Table 2: EEG characteristics of stimulus-induced clinical seizures and ADs

Patient

Event

Clinical seizure

Clinical seizure

Clinical seizure

25

Clinical seizure

Clinical seizure

AD

AD

12

AD

21

AD

AD

AD

12

AD

12

AD

12

AD

14

AD

19

AD

26

AD

Stimulus site

(anatomical

location)

SOZ

(PCL)

SOZ

(PrCG)

SOZ

(PrCG)

SOZ

(PrCG)

non-SOZ

(Ento)

SOZ

(Ento)

SOZ

(Ento)

SOZ

(Ento)

SOZ

(Ento)

non-SOZ

(PrCG)

non-SOZ

(IFG)

non-SOZ

(IFG)

non-SOZ

(FuG)

non-SOZ

(ITG)

non-SOZ

(Ento)

non-SOZ

(FuG)

non-SOZ

(ITG)

Involvement of

adjacent electrode

(<2 cm)

Involvement of

remote electrode

(>5 cm or other lobes)

Involvement

of SOZ

180

Involvement of

near electrode

(2-5 cm)

Consistency of

propagation pattern with

spontaneous seizure

Consistent

51

Consistent

15

241

Consistent

10

142

(no spontaneous seizure)

12

104

Consistent

10

50

44

14

10

28

61

10

34

10

94

10

45

Inconsistent: narrower

distribution

Inconsistent: narrower

distribution

Inconsistent: narrower

distribution

Inconsistent: narrower

distribution

Inconsistent: narrower

distribution

Inconsistent: narrower

distribution

Inconsistent: different

locations

Consistent

10

10

80

10

34

10

519

Stimulus

intensity (mA)

Duration of EEG

changes (sec)

12

Inconsistent: different

locations

Inconsistent: partial

overlap

Inconsistent: different

locations

Inconsistent: partial

overlap

AD, afterdischarge; SOZ, seizure onset zone; PCL, paracentral lobule; PrCG, precentral gyrus; Ento, entorhinal cortex; IFG, inferior frontal gyrus;

FuG, fusiform gyrus; ITG, inferior temporal gyrus

36

...

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