Abstract
Purpose: The mechanism underlying sulcal hyperintensity observed on
fluid-attenuated inversion recovery magnetic resonance imaging (MRI) (sulcal FLAIR
hyperintensity [S-FLAIR-HI]) without apparent abnormalities in the cerebrospinal fluid
(CSF) is believed to involve alterations in regional hemodynamics, including venous
congestion caused by mass effect, leading to a pathological increase in the blood
pool-to-CSF ratio. While S-FLAIR-HI is observed in chronic subdural hematoma (CSDH), its
exact incidence, mechanism of occurrence, and relationship with seizures remain unclear.
Methods: Clinical data and MRI findings, including FLAIR and 1.5-Tesla
pseudo-continuous arterial spin labeling perfusion imaging performed within 1 day before
surgery in 34 patients with CSDH, were retrospectively reviewed. The focus was on the
laterality of arterial transit artifact(s) in the sulcus (sulcal ATA [S-ATA]), which are
intravascular signals that increase with a delay in arterial transit time, and
(peri-)ictal hyperperfusion linked to seizure activity by neurovascular coupling.
Results: S-FLAIR-HI was observed in 12 (35.3%) of the 34 patients with
CSDH, 11 of whom exhibited an increase in S-ATA on the ipsilateral side. Increased S-ATA
levels were also observed in 10 of the 22 patients without S-FLAIR-HI. However, none of
the 12 patients with S-FLAIR-HI developed seizures. In addition, 2 patients who exhibited
perioperative seizures did not undergo S-FLAIR-HI.
Discussion:
S-FLAIR-HI, observed preoperatively in approximately one-third of patients with CSDH, is a
nonspecific finding caused by alterations in regional hemodynamics. Furthermore, there is
no evidence supporting the direct involvement of S-FLAIR-HI in the development of
seizures.
Introduction
Sulcal hyperintensity on magnetic resonance imaging (MRI) with fluid-attenuated inversion
recovery sequences (FLAIR) (sulcal FLAIR hyperintensity [S-FLAIR-HI]) is a condition in
which the cerebrospinal fluid (CSF) is not suppressed in the cortical sulcus. S-FLAIR-HI is
most commonly caused by CSF abnormalities, such as subarachnoid hemorrhage, meningitis, and
CSF dissemination in malignancies[1, 2]. However, S-FLAIR-HI has also been observed in the
absence of apparent CSF abnormalities[1,2,3,4]. The primary mechanism is believed to involve
alterations in regional hemodynamics, including venous congestion due to mass effect of the
lesion and venous (sinus) thrombosis. This causes a pathological increase in the blood
pool-to-CSF ratio within the sulcus, resulting in water signals being unsuppressed on
FLAIR images[1].
Although S-FLAIR-HI is also observed in the cerebral hemisphere directly below the chronic
subdural hematoma (CSDH)[5,6,7], its exact incidence and
mechanism remain unknown. The main reason behind this is that computed tomography (CT) is
used in the diagnosis and surgical management of CSDH as a general rule. Perioperative MRI
is rarely applied[7].
Arterial spin labeling (ASL) perfusion MRI is a non-invasive method to evaluate cerebral
blood flow (CBF) by labeling the spin of the cervical arterial blood with a magnetic field.
Due to the effect of the blood flow velocity, more specifically, the arterial transit time
(ATT), imaging using multiple post-labeling delays (PLDs) has the advantage of enabling the
evaluation of intracranial hemodynamics[8,9,10,11,12,13]. We have previously reported on 3 CSDH patients with
S-FLAIR-HI, using 3-Tesla (T) pseudo-continuous labeling (3-T pCASL) with dual PLDs of 1.5
and 2.5 s. In these patients, ASL signal intensity decreased in the region where S-FLAIR-HI
was observed at a PLD of 1.5 s, but increased later at a PLD of 2.5 s, i.e., ATT was
delayed[7]. This suggests that alterations in
regional hemodynamics due to mass effect may be involved in the development of the MRI
finding in patients with CSDH.
In the present study, we focused on the fact that 1.5-T ASL has an inferior image
resolution as a perfusion image compared to 3-T pCASL, and that correct CBF cannot be
evaluated at a slower PLD, such as 2.5 s, due to rapid T1 decay. However, 1.5-T ASL also has
the characteristic to easily enhance arterial transit artifact (ATA) with delayed ATT[14,15,16,17,18,19,20,21,22,23,24,25,26], which are intravascular ASL signals in the
subarachnoid space. We retrospectively reviewed clinical data and MRI findings of 34
patients with CSDH who underwent MRI, including both FLAIR and 1.5-T pCASL with triple PLDs
of 1.5, 1.75, and 2.0 s[15,16,17,18,19,20,21,22,23,24,25,26] within 1 day before surgery. We investigated the incidence of
S-FLAIR-HI in CSDH patients, and whether alterations in regional hemodynamics, mainly
delayed ATT, were involved in its pathogenesis.
Regarding the clinical significance of S-FLAIR-HI in CSDH, a few investigations have
addressed its association with seizure development. Neshige et al.[5] reported that in 60 patients with CSDH, S-FLAIR-HI was observed in only
5 (12.5%) of 40 patients who did not develop seizures during the perioperative period, while
it was observed in 9 (45%) of 20 patients who developed seizures. Oshida et al.[6] reported a case in which 123I-single-photon
emission computed tomography, performed 2 days after a generalized convulsive seizure that
occurred 9 days after surgery, exhibited a transient decrease in benzodiazepine receptors in
the region where S-FLAIR-HI was observed. We also reported that in 3 patients with seizures
that developed during the perioperative period, S-FLAIR-HI was found on the side that
matched the seizure symptoms, electroencephalographic (EEG) abnormalities, and peri-ictal
ASL hyperperfusion linked to seizure activity by neurovascular coupling[12, 15, 16, 18,19,20,21,22,23,24,25,26,27] captured using 3-T pCASL[7]. In the present study, we describe the chronological changes in the
clinical, EEG, and MRI findings, including 1.5-T pCASL with triple PLDs, in 2 patients who
developed seizures, and discuss the relationship between S-FLAIR-HI and the development of
seizures.
Methods
Patients
Between April 2022 and December 2024, 102 patients underwent 107 evacuations for CSDH
through a single burr-hole opening on the parietal bone at our hospital. CT was used in
both pre- and postoperative evaluations of all patients. In this cohort of 102 patients,
we investigated 34 patients who underwent 1.5-T MRI, including both FLAIR and pCASL within
1 day before surgery, in addition to CT scan, taken for clinical purposes, depending on
the patient’s conditions and the discretion of the attending physicians.
The cohort of 34 patients consisted 18 females and 16 males, with a mean age of 78.9
years (range 62 to 102 years). Twenty-six patients had unilateral CSDH, including 6
patients with bilateral CSDH in whom only one side was operated on since there was almost
no mass effect prevalent on the other side. The remaining 8 patients had bilateral CSDH.
Clinical symptoms included weakness of the upper and lower limbs in 25 patients, cognitive
decline in 7 patients, and headache in 1 patient. Only 1 patient (Patient 1) developed
seizures immediately before surgery. Patient 2, who developed weakness in the upper and
lower limbs, developed seizures 2 months before and 7 days after surgery. Surgery was
performed on 33 patients based on findings that the above symptoms were due to mass effect
of the CSDH; however, in Patient 1, surgery was performed to control seizures.
Ethical approval was obtained from the Institutional Review Board of Hachisuga Hospital
(No. 22-1); the requirement for written informed consent was waived due to the
retrospective study design.
MRI
MRI was performed on all patients using a 1.5-T scanner (ECHELON OVAL V6, FUJIFILM
Medical Co., Ltd., Tokyo, Japan) equipped with a 15-channel receive-only head coil for
signal reception.
The parameters for FLAIR were as follows: repetition time (TR), 10000 ms; echo time (TE),
120 ms; inversion time, 2300 ms; echo train length, 19; echo space, 12 ms; field of view,
240 mm; matrix, 512 × 512; slice thickness, 5.0 mm; slice interval, 6 mm; and slice
number, 23.
PCASL was performed as part of a routine MRI examination using a three-dimensional
gradient and spin-echo sequence with background suppression for perfusion imaging of the
entire brain, as previously described[15,16,17,18,19,20,21,22,23,24,25,26]. The acquisition parameters were as follows: phase
encoding in the z-direction, 28; TR, 4291 ms; TE, 17.4 ms; field of view, 250 mm;
matrix,128 × 128; slice thickness, 6 mm; reconstruction interval, 3 mm; and number of
slices, 48. The labeling duration was 1.5 s. Three PLDs (1.5, 1.75, and 2.0 s) were
selected. The ASL acquisition times for each PLD were 3 min and 1 s.
The obtained ASL images were pseudo-colorized and superimposed onto anatomical MRI,
including FLAIR and diffusion-weighted images (DWI), using Synapse Vincent (FUJIFILM
Medical Co., Ltd., Tokyo, Japan), as previously described[15,16,17,18,19,20,21,22,23,24,25,26].
ASL findings were evaluated through visual inspection by board-certified neurosurgeons
(S.I. and T.S.) experienced in ASL interpretation and blinded to the clinical data, as
described in our previous reports[22,23,24,25]. No differences were observed in the independent
assessments.
Results
(Table 1)
Table 1 Relationship between findings of sulcal FLAIR hyperintensity (S-FLAIR-HI) and
increased sulcal arterial transit artifact (S-ATA) in 34 patients with chronic subdural
hematoma (CSDH)
|
Unilateral CSDH
26 |
Bilateral CSDH
8 |
Total
34 |
S-FLAIR-HI
(+) |
9
→Increased S-ATA
(+): 9 |
3
→ Increased S-ATA
(+): 2
ND:
1 |
12
→ Increased S-ATA
(+): 11
ND:
1 |
S-FLAIR-HI
(-) |
17
→ Increased S-ATA
(+): 9**
(-): 7
ND: 1* |
5
→ Increased S-ATA
(+): 1
ND:
4 |
22
→ Increased S-ATA
(+): 10
(-): 7
ND: 5 |
Number indicates number of the patients.Abbreviations: FLAIR, fluid-attenuated
inversion recovery; ND, not determined;*, including Patient 1; **, including Patient
2.
S-FLAIR-HI was observed in 12 (35.3%) of 34 patients with CSDH, of whom 9 had unilateral
CSDH, in the cerebral hemisphere directly below the CSDH (Fig. 1A). Not all sulci compressed by CSDH exhibited high signals, and S-FLAIR-HI
tended to become more evident toward the vertex. The remaining three patients had bilateral
CSDH, two of whom had S-FLAIR-HI on the side with the larger hematoma size, and one had
S-FLAIR-HI bilaterally. Of these 12 patients, 8 patients presented upper and lower limb
weakness, 4 patients had cognitive decline, and none presented seizures.
Of the 22 patients who did not have S-FLAIR-HI, 17 patients had unilateral CSDH and 5
patients had bilateral CSDH. Sixteen patients presented with upper and lower limb weakness,
3 patients with cognitive impairment, and 1 patient with headache. Patient 1, who presented
with seizure, did not undergo S-FLAIR-HI. Patient 2, who presented with seizures 2 months
before and 7 days after surgery, did not have S-FLAIR-HI before surgery, but developed
S-FLAIR-HI on the 9th day after surgery. The clinical courses of these 2 patients are
described in detail later.
On the ASL of the 12 patients with S-FLAIR-HI, in all 9 patients with unilateral CSDH,
laterality was observed between the ASL signals in the sulcus; more specifically, the sulcal
ATA (S-ATA), and the signal intensity of the ipsilateral S-ATA was higher than that of the
contralateral S-ATA at a PLD of 1.5 s (Fig. 1B).
The signal intensity of this S-ATA was attenuated at a PLD of 1.75 s (Fig. 1C); however, the laterality remained at a PLD of 2.0 s (Fig. 1D), and was judged to be increased S-ATA on the
side of the CSDH. However, there was no tendency for the S-ATA signal intensity to be higher
in sulci with high S-FLAIR-HI signals. Of the 3 patients with bilateral CSDH who exhibited
S-FLAIR-HI, increased S-ATA was evident on the ipsilateral side in 2 patients with
unilateral S-FLAIR-HI; however, in 1 patient with bilateral S-FLAIR-HI, the laterality of
S-ATA could not be determined. In other words, 11 of the 12 patients with S-FLAIR-HI
observed had increased S-ATA levels on the ipsilateral side, and in 1 patient with bilateral
CSDH, the result was undetermined.
Among the 17 patients with unilateral CSDH who did not exhibit S-FLAIR-HI, ipsilateral
increased S-ATA was observed in 9 patients, including Patient 2 (Table 1, **), but not in 7 patients. The remaining patient
(Patient 1), who developed seizures immediately prior to surgery, had peri-ictal ASL
hyperperfusion in the cortex directly below the CSDH, making it impossible to evaluate S-ATA
laterality (Table 1, *).This is discussed in
more detail later in this paper. Of the 5 patients with bilateral CSDH, 1 patient had
increased S-ATA on the side with a larger hematoma size, but the laterality of the S-ATA
could not be determined in 4 patients. In summary, of the 22 patients without S-FLAIR-HI, 10
patients had increased ipsilateral S-ATA levels and 7 patients did not. In the remaining 5
patients, increased S-ATA could not be determined.
Here we present the chronological changes in clinical, EEG, and MRI findings, including
1.5-T pCASL with triple PLDs, in Patient 1, who developed seizures 25 days before and
immediately before surgery, and in Patient 2, who developed seizures 2 months before surgery
and 7 days after surgery.
Patient 1
A 90-year-old woman was transferred to our hospital after developing her first seizure, a
focal to bilateral tonic-clonic seizure (FBTCS), 25 days before the surgery (Day 1). On
arrival, she experienced a generalized convulsive seizure with right conjugate deviation,
which was resolved by intravenous administration of 5 mg diazepam (DZP). CT scan revealed
a thin CSDH on the left side (Fig. 2A). ASL at a
PLD of 1.5 s performed 30 min after admission demonstrated peri-ictal hyperperfusion in
the left hemisphere, except for parts of the frontal and parietal lobes and the occipital
lobe (Fig. 2B, white arrows). ASL signals in the
bilateral thalami also increased. Perfusion in the contralateral temporo-occipital lobes
also increased, most likely due to the effect of FBTCS (Fig. 2B, white dotted arrows). This hyperperfusion was attenuated at a PLD of
1.75 s, and signals remained in the interhemispheric fissure of the left frontal lobe and
in the bilateral thalami (Fig. 2C), but almost
disappeared at a PLD of 2.0 s. The presence or absence of increased S-ATA levels could not
be determined due to the influence of peri-ictal hyperperfusion. DWI revealed a faint,
high signal intensity in the left parietal lobe and pulvinar (Fig. 2D, yellow arrows). FLAIR imaging was not performed due to the
situation being an emergency.
Since mass effect of the left CSDH was minimal, conservative treatment was selected, and
2 mg perampanel (PER) was administered intravenously, followed by oral administration of 1
mg PER. The patient was in a restless state with electrolyte abnormality (Na 119 mEq/L, K
2.5 mEq/L, Cl 178 mEq/L), and was transferred to the Nephrology Department on Day 2.
Electrolyte abnormality was diagnosed due to long-term use of 50 mg mefruside, a
thiazide-like diuretic. This diuretic was discontinued, and saline loading was
administered. As a result, electrolyte abnormality was nearly resolved, and the patient
was discharged on Day 15. The size of the hematoma remained almost unchanged, and the
patient was still observed to have CSDH.
However, on Day 25, the day before surgery, a second seizure occurred, and a total of 10
mg DZP was used to stop the seizure. Four and a half hours later, EEG showed 1.6 Hz
rhythmic delta activities+ S with a maximum amplitude at O1 and P3 (Fig. 2E), and the patient was diagnosed as being in
the ictal-interictal continuum based on the American Clinical Neurophysiology Society’s
Standardized Critical Care EEG Terminology 2021 version (ACNS2021)[28].
MRI was performed 5.5 h after the seizure. The size of the left CSDH remained virtually
unchanged from that of Day 1, and no S-FLAIR-HI was observed (Fig. 2F). ASL at a PLD of 1.5 s revealed prominent hyperperfusion
in the left temporal, parietal, and occipital lobes and the left thalamus (Fig. 2G). The hyperperfusion was attenuated at a PLD
of 1.75 s; however, the increased signal in the left parietal and occipital lobes remained
at a PLD of 2.0 s (Fig. 2H). DWI showed faint,
high signals in the cortex of the left temporal, parietal, and occipital lobes and in the
left pulvinar (Fig. 2I), where ASL
hyperperfusion was observed. In addition, some of the hematoma contents exhibited high
signal intensity, suggesting fresh bleeding into the hematoma cavity.
Convulsive seizure in the right upper extremity continued, requiring continuous infusion
of midazolam (MDZ) and intravenous administration of levetiracetam to achieve control.
Although mass effect of the CSDH was not significant, surgery was performed on Day 26 to
control the seizure. Although clots were observed within the hematoma cavity, the
intraoperative findings did not show any significant changes compared to those of usual
CSDH surgery. However, continuous MDZ infusion was necessary to control the seizure even
after surgery. On Day 28 (the second day after surgery), EEG revealed a decreased
frequency and amplitude of paroxysmal activities (Fig.
2J); however, the patient developed pneumonia with pleural effusion, and her
respiratory condition worsened. Controlled respiration was performed with endotracheal
intubation; however, the patient’s respiratory condition did not improve. The patient
experienced a drop in blood pressure and oliguria, and died on Day 29.
Patient 2
A 91-year-old woman with dementia and diabetes mellitus was admitted to a facility with a
modified Rankin Scale score of 3; however, her blood glucose control with insulin was
poor. Approximately 2 months before surgery, she experienced her first seizure, FBTCS with
right conjugate deviation, and was transferred to our hospital (Day 1). Even after
intravenous administration of DZP (total 20 mg) and PER (2 mg), her seizure continued, and
a continuous intravenous infusion of MDZ was required. Despite an increase in the amount
of insulin administered at the facility before being transported, the patient’s blood
glucose level remained at 287 mg/dL. CT scan revealed thin CSDHs on both sides with a
left-dominant pattern. EEG showed drug-induced fast waves on the right hemisphere.
Activities on the left hemisphere were extremely low, but low-voltage fast wave
activities, which minimally evolved in frequency and amplitude, were observed with the
maximal amplitude at O1 (Fig. 3A, red arrows)
and minimal amplitude at O2 and Pz (Fig. 3A,
blue lines). Based on the ACNS2021, the patient was diagnosed as having electrographic
seizures.
Respiratory depression was observed due to the effects of MDZ, and MRI was performed on
Day 2. S-FLAIR-HI was not detected (Fig. 3B).
ASL at a PLD of 1.5 s revealed hyperperfusion in the left hemisphere immediately below the
CSDH (Fig. 3C), which persisted even at a PLD of
2.0 s (Fig. 3D). No signal changes were observed
on DWI. Thereafter, no seizures occurred with the oral administration of 1 mg PER, blood
glucose levels were well controlled with insulin administration, and the patient returned
to the facility on Day 28.
However, two months later, right hemiparesis developed, and the patient was transferred
to our hospital again (Day 1’). FLAIR revealed that the sulci were compressed by increased
mass effect of the left CSDH. However, S-FLAIR-HI was not observed (Fig. 3E). On ASL at a PLD of 1.5, the S-ATA of the left hemisphere
was slightly elevated compared to that of the right hemisphere (Fig. 3F), and this laterality persisted at a PLD of 2.0 s (Fig. 3G). There was no change in the DWI signal. On
Day 2’, surgery was performed, and the right hemiparesis improved.
On postoperative day 7 (Day 9’), however, hyperglycemia (289 mg/dL) recurred, and the
patient developed right facial spasms, which stopped with the administration of 10 mg DZP.
EEG revealed attenuated background activities on the left hemisphere, but there were no
paroxysmal discharges. FLAIR revealed a decrease in mass effect of the CSDH, whereas
S-FLAIR-HI appeared (Fig. 3H). ASL at a PLD of
1.5 s revealed hyperperfusion in the cortex directly below the hematoma (Fig. 3I). This hyperperfusion was attenuated at a
PLD of 1.75 s; however, the hyperperfusion in the fronto-temporal lobes, where S-FLAIR-HI
was the strongest, remained intense at a PLD of 2.0 s (Fig. 3J). Due to this hyperperfusion, the laterality of the S-ATA could not be
determined. No signal changes were observed on DWI.
The PER dose was increased from 1 mg to 2 mg. On Day 19’, S-FLAIR-HI virtually
disappeared (Fig. 3K). In addition, increased
S-ATA levels were observed on the same side on the ASL at a PLD of 1.5 s (Fig. 3L), as well as at a PLD of 2.0 s (Fig. 3M). The patient returned to the facility on
Day 30’ when blood glucose control was easier to maintain.
Discussion
Previous reports addressing S-FLAIR-HI in CSDH included many cases in which MRI was
performed only after the development of various postoperative complications including
seizures, and S-FLAIR-HI was detected[5,6,7]. Therefore,
there were cases in which S-FLAIR-HI was not observed preoperatively, but developed
postoperatively, such as Patient 2 in this study. The occurrence of postoperative S-FLAIR-HI
cannot be ruled out as a mechanism by which the CSF in the sulci becomes abnormal, such as
the occurrence of subarachnoid hemorrhage or changes in vascular permeability that cause
protein leakage into the CSF[1] due to surgery.
Therefore, in the present study, we reviewed the data of 34 patients in whom MRI was
performed within 1 day before surgery, of which a one-third of the patients showed
S-FLAIR-HI.
In this study, 1.5-T pCASL revealed increased S-ATA on the ipsilateral side in 11 of the 12
patients in whom S-FLAIR-HI was observed, and in 10 of the 22 patients in whom S-FLAIR-HI
was not observed. Therefore, increased S-ATA levels were observed in 21 of 34 patients
(61.8%). All 34 patients, except for Patient 1, were determined as having clinical symptoms
due to mass effect of the CSDH, and surgery was performed. The results of this study
indicate that, in many CSDH cases, prolonged ATT occurs preoperatively due to the mass
effect. In other words, the occurrence of S-FLAIR-HI in CSDH supports the previous concept
that it is a nonspecific finding that causes a pathological increase in the blood
pool-to-CSF ratio within the sulcus due to alterations in regional hemodynamics[1]. However, not all sulci compressed by the CSDH
exhibited FLAIR hyperintensity, and there was no tendency for the ATA signal intensity to be
higher in sulci exhibiting FLAIR hyperintensity. Therefore, we believe that the occurrence
of S-FLAIR-HI involves complex factors, including the relationship between the original
width of the sulci and the density of blood vessels.
In the present study, none of the 12 patients with S-FLAIR-HI developed seizures. In
contrast, the side exhibiting EEG abnormalities and peri-ictal ASL hyperperfusion was
ipsilateral to the CSDH in Patients 1 and 2, as described in the previous reports[5,6,7]. In particular, peri-ictal ASL hyperperfusion was
distributed in the cortex directly below the CSDH, suggesting that the CSDH may be involved
in seizure development. However, since neither patient exhibited S-FLAIR-HI, we were unable
to conclude that S-FLAIR-HI was directly involved in the development of seizures. The
possible reason why the result of this study differs from those of the previous
investigation[5,6,7] is that, as mentioned above, many of
those studies included cases in which the presence of S-FLAIR-HI was first observed after
surgery. In fact, in Patient 2, ictogenesis of S-FLAIR-HI could have been suspected at 9
days after surgery, when only the cortex with the newly developed S-FLAIR-HI below the CSDH
was shown to have peri-ictal ASL hyperperfusion. However, in the present case, S-FLAIR-HI
was not observed preoperatively.
In Patient 1, electrolyte abnormality (mainly hyponatremia) and bleeding into the CSDH
cavity were observed during the first and second seizures, respectively. In Patient 2,
hyperglycemia was observed for both seizures. These are the causative factors for
situation-related and acute symptomatic seizures[22,
25, 29,30,31]. Therefore,
we believe that in both patients, seizures were caused by these conditions and acute
lesions, in addition to CSDH. Furthermore, the distribution of peri-ictal ASL hyperperfusion
differed slightly between the first and second seizure episodes in both patients. This is
due to the complex involvement of multiple factors in seizures of CSDH patients, differing
from focal epilepsy, which arises from a single focus around the area of structural
abnormality and exhibits the same blood flow distribution each time[20].
The present study has several limitations. First, ASL cannot be used to quantify CBF;
therefore, we visually assessed CBF based on the abnormal distribution of CBF, primarily
laterality. In particular, because increased S-ATA was judged based on laterality, increased
S-ATA could not be determined in five of eight patients with bilateral CSDH. However, when
examining 26 patients with unilateral CSDH, increased S-ATA levels were observed more
frequently in 18 patients (69.2%), further emphasizing the results of this study. Second, as
in Patient 2, it is desirable to observe chronological changes in S-FLAIR-HI and increased
S-ASL with postoperative MRI; however, in many patients with a good postoperative course,
postoperative evaluation was performed only with CT scans, and sufficient MRI data was not
be available. Third, this was a retrospective study with a small number of patients (n =
34). In the future, re-evaluation with a larger number of patients, including postoperative
MRI, is necessary.
Conclusion
Although further investigation with a larger number of patients is required, our results
support the previous concept that S-FLAIR-HI, encountered in approximately one-third of
patients with CSDH immediately before surgery, is a nonspecific finding caused by
alterations in regional hemodynamics, including increased S-ATA levels with prolonged ATT
due to mass effect of CSDH. Furthermore, there is no evidence to support the direct
involvement of S-FLAIR-HI in the development of seizures.
Acknowledgments
We would like to thank Ryoji Shiraki and colleagues at Hachisuga Hospital, for supporting
our study. We would also like to thank Editage for the English language editing.
Conflict of Interest Disclosure
The authors declare that they have no conflicts of interest to disclose.
References
- [1] Taoka T, Yuh WTC, White ML, Quets JP, Maley JE,
Ueda T. Sulcal hyperintensity on fluid-attenuated inversion recovery mr images in patients
without apparent cerebrospinal fluid abnormality. AJR Am J Roentgenol 2001; 176: 519–524.
PMID:11159107, https://doi.org/10.2214/ajr.176.2.1760519
- [2] Stuckey SL, Goh TD, Heffernan T, Rowan D.
Hyperintensity in the subarachnoid space on FLAIR MRI. AJR Am J Roentgenol 2007; 189:
913–921. PMID:17885065, https://doi.org/10.2214/AJR.07.2424
- [3] Yazdani M, Stalcup ST, Chatterjee AR, Matheus MG.
Sulcal FLAIR hyperintensity after CSF removal in two patients with intracranial
hypertension. Eur J Radiol Open 2019; 6: 33–35. PMID:30619917,
https://doi.org/10.1016/j.ejro.2018.12.005
- [4] de Oliveira EP, Tsehmaister-Abitbul V, Kontolemos
M, Glikstein R, Torres C. Reversible sulcal FLAIR hyperintensity on MRI in a migraine
patient with aura. Radiol Case Rep 2020; 15: 174–176. PMID:31890062,
https://doi.org/10.1016/j.radcr.2019.10.029
- [5] Neshige S, Sekihara Y, Ishii N, Sato M, Ota S,
Kuriyama M. Clinical and radiological studies of seizure in chronic subdural hematoma—case
control study—. Rinsho Shinkeigaku 2014; 54: 869–875. PMID:25420559,
https://doi.org/10.5692/clinicalneurol.54.869
- [6] Oshida S, Akamatsu Y, Matsumoto Y, Ishigame S,
Ogasawara Y, Aso K, Kashimura H. A case of chronic subdural hematoma demonstrating the
epileptic focus at the area with sulcal hyperintensity on fluid-attenuated inversion
recovery image. Radiol Case Rep 2019; 14: 1109–1112. PMID:31338136,
https://doi.org/10.1016/j.radcr.2019.06.021
- [7] Tashiro K, Haga S, Tanaka S, Tokunaga S, Inoue D,
Shimogawa T, Mukae N, Shono T, Yoshimoto K, Morioka T. Sulcal hyperintensity on magnetic
resonance imaging with fluid-attenuated inversion recovery sequence in patients with
chronic subdural hematoma. Interdiscip Neurosurg 2022; 29: 101571.
https://doi.org/10.1016/j.inat.2022.101571
- [8] Haga S, Morioka T, Shimogawa T, Akiyama T, Murao
K, Kanazawa Y, Sayama T, Arakawa S. Arterial spin labeling perfusion magnetic resonance
image with dual postlabeling delay: A correlative study with acetazolamide loading
123I-Iodoanphetamine single-photon emission computed tomography. J Stroke Cerebrovasc Dis
2016; 25: 1–6. PMID:26387043,
https://doi.org/10.1016/j.jstrokecerebrovasdis.2015.08.025
- [9] Haga S, Morioka T, Kameda K, Takahara K, Amano T,
Tomohara S, Takaki H, Tsurusaki Y, Arihiro S. Subtraction of arterial spin-labeling
magnetic resonance perfusion images acquired at dual post-labeling delay: potential for
evaluating cerebral hyperperfusion syndrome following carotid endarterectomy. J Clin
Neurosci 2019; 63: 77–83. PMID:30738738,
https://doi.org/10.1016/j.jocn.2019.01.044
- [10] Akiyama T, Morioka T, Shimogawa T, Haga S, Sayama
T, Kanazawa Y, Murao K, Arakawa S. Arterial spin-labeling magnetic resonance imaging with
dual post-labeling delay in internal carotid artery steno-occlusion: validation with
digital subtraction angiography. J Stroke Cerebrovasc Dis 2016; 25: 2099–2108.
PMID:27339943, https://doi.org/10.1016/j.jstrokecerebrovasdis.2016.06.005
- [11] Shimogawa T, Morioka T, Akiyama T, Haga S,
Arakawa S, Sayama T. Sequential changes of arterial spin-labeling perfusion MR images with
dual postlabeling delay following reconstructive surgery for giant internal carotid artery
aneurysm. Surg Neurol Int 2017; 8: 222. PMID:28966828,
https://doi.org/10.4103/sni.sni_73_17
- [12] Takahara K, Morioka T, Shimogawa T, Haga S,
Kameda K, Arihiro S, Sakata A, Mukae N, Iihara K. Hemodynamic state of periictal
hyperperfusion revealed by arterial spin-labeling perfusion MR images with dual
postlabeling delay. eNeurologicalSci 2018; 12: 5–18. PMID:30229134,
https://doi.org/10.1016/j.ensci.2018.06.001
- [13] Tokunaga S, Morioka T, Shirozu N, Tsurusaki Y,
Arihiro S, Shimogawa T, Mizoguchi M, Haga S. Arterial spin-labeling perfusion MR images
with dual postlabeling delay reveals hemodynamic changes in dural arteriovenous fistulas
following endovascular surgery. Interdiscip Neurosurg 2020; 21: 100733.
https://doi.org/10.1016/j.inat.2020.100733
- [14] Jaganmohan D, Pan S, Kesavadas C, Thomas B. A
pictorial review of brain arterial spin labelling artefacts and their potential remedies
in clinical studies. Neuroradiol J 2021; 34: 154–168. PMID:33283653,
https://doi.org/10.1177/1971400920977031
- [15] Oketani H, Morioka T, Inoha S, Shimogawa T, Mukae
N, Yasukouchi H, Kinoshita Y, Yoshimoto K. Comparison between 1.5-Tesla pseudocontinuous
and pulsed arterial spin labeling in visualizing peri-ictal hyperperfusion: A case report.
Epilepsy & Seizure 2023; 15: 17–25.
https://doi.org/10.3805/eands.15.17
- [16] Oketani H, Morioka T, Inoha S, Akiyama T,
Shimogawa T, Mukae N, Yoshimoto K. Hemodynamics of ictal hyperperfusion in an epileptic
patient with dual pathology revealed by arterial spin labeling perfusion image with triple
postlabeling delays. Epilepsy & Seizure 2023; 15: 26–34.
https://doi.org/10.3805/eands.15.26
- [17] Oketani H, Morioka T, Inoha S, Miki K, Shimogawa
T, Mukae N, Sakata A, Shigeto H, Yoshimoto K. Arterial spin labeling MR perfusion image in
differentiating metabolic encephalopathy from non-convulsive status epilepticus in a
patient with generalized periodic discharges with triphasic morphology. Epilepsy &
Seizure 2023; 15: 59–66. https://doi.org/10.3805/eands.15.59
- [18] Oketani H, Morioka T, Inoha S, Miki K, Shimogawa
T, Mukae N, Sakata A, Shigeto H, Yoshimoto K. Detection of slightly increased signals in
temporal lobe on periictal arterial spin labeling perfusion image for initial suspicion of
temporal lobe epilepsy. Epilepsy & Seizure 2023; 15: 67–74.
https://doi.org/10.3805/eands.15.67
- [19] Oketani H, Morioka T, Inoha S, Mugita F, Mukae N,
Shimogawa T, Sakata A, Shigeto H, Yoshimoto K. Periictal hyperperfusion in the perituberal
cortex revealed by arterial spin labeling perfusion images in a patient with tuberous
sclerosis complex. Epilepsy & Seizure 2023; 15: 75–81.
https://doi.org/10.3805/eands.15.75
- [20] Mugita F, Morioka T, Inoha S, Akiyama T,
Shimogawa T, Mukae N, Sakata A, Shigeto H, Yoshimoto K. Crossed cerebellar hyperperfusion
during periictal and ictal periods revealed by 1.5-Tesla arterial spin labeling magnetic
resonance perfusion images. Epilepsy & Seizure 2023; 15: 95–103.
https://doi.org/10.3805/eands.15.95
- [21] Mugita F, Morioka T, Inoha S, Akiyama T, Maehara
N, Shimogawa T, Mukae N, Sakata A, Shigeto H, Yoshimoto K. Absence of periictal
hyperperfusion on arterial spin labeling perfusion images in a patient with posttraumatic
epilepsy and underdevelopment of ipsilateral internal carotid and middle cerebral
arteries. Epilepsy & Seizure 2024; 16: 1–11.
https://doi.org/10.3805/eands.16.1
- [22] Morioka T, Inoha S, Mugita F, Oketani H,
Shimogawa T, Mukae N, Maehara N, Akiyama T, Miki K, Karashima S, Sakata A, Shigeto H,
Yoshimoto K. Addition of 1.5-Tesla arterial spin labeling magnetic resonance perfusion
imaging to routine electroencephalography in pathophysiological diagnosis of first-onset
generalized convulsive seizures in patients with dementia at neurological emergency.
Epilepsy & Seizure 2024; 16: 29–43.
https://doi.org/10.3805/eands.16.29
- [23] Morioka T, Mugita F, Inoha S, Akiyama T, Miki K,
Shimogawa T, Mukae N, Sakata A, Shigeto H, Yoshimoto K. Usefulness and limitation of
addition of 1.5-Tesla arterial spin labeling magnetic resonance perfusion imaging to
routine electroencephalography in pathophysiological diagnosis of post-intracerebral
hemorrhage epilepsy at neurological emergency. Epilepsy & Seizure 2024; 16: 78–94.
https://doi.org/10.3805/eands.16.78
- [24] Morioka T, Mugita F, Inoha S, Akiyama T, Haruyama
H, Karashima S, Shimogawa T, Mukae N, Sakata A, Shigeto H, Yoshimoto K. Ictal 1.5-Tesla MR
imaging with arterial spin labeling perfusion imaging in three patients with
electrographic seizures diagnosed with routine electroencephalography based on the ACNS
Critical Care EEG Terminology 2021. Epilepsy & Seizure 2025; 17: A000162.
https://doi.org/10.3805/eands.A000162
- [25] Morioka T, Mugita F, Inoha S, Shimogawa T, Mukae
N, Akiyama T, Haruyama H, Karashima S, Sakata A, Shigeto H, Yoshimoto K. Time to detect
periictal hyperperfusion following short acute symptomatic seizures using 1.5-Tesla
arterial spin labeling magnetic resonance perfusion imaging. Epilepsy & Seizure 2025;
17: A000163. https://doi.org/10.3805/eands.A000163
- [26] Morioka T, Mugita F, Inoha S, Kinoshita Y,
Akiyama T, Shimogawa T, Mukae N, Sakata A, Shigeto H, Yoshimoto K. Detection of subtle
periictal hyperperfusion with 1.5-Tesla arterial spin labeling perfusion imaging in a
patient with congenital unilateral perisylvian syndrome in a neurological emergency.
Epilepsy & Seizure 2025; 17: A000164.
https://doi.org/10.3805/eands.A000164
- [27] Shimogawa T, Morioka T, Sayama T, Haga S,
Kanazawa Y, Murao K, Arakawa S, Sakata A, Iihara K. The initial use of arterial spin
labeling perfusion and diffusion-weighted magnetic resonance images in the diagnosis of
nonconvulsive partial status epileptics. Epilepsy Res 2017; 129: 162–173. PMID:28092848,
https://doi.org/10.1016/j.eplepsyres.2016.12.008
- [28] Hirsch LJ, Fong MWK, Leitinger M, LaRoche SM,
Beniczky S, Abend NS, Lee JW, Wusthoff CJ, Hahn CD, Westover MB, Gerard EE, Herman ST,
Haider HA, Osman G, Rodriguez-Ruiz A, Maciel CB, Gilmore EJ, Fernandez A, Rosenthal ES,
Claassen J, Husain AM, Yoo JY, So EL, Kaplan PW, Nuwer MR, van Putten M, Sutter R,
Drislane FW, Trinka E, Gaspard N. American Clinical Neurophysiology Society’s Standardized
Critical Care EEG Terminology: 2021 Version. J Clin Neurophysiol 2021; 38: 1–29.
PMID:33475321, https://doi.org/10.1097/WNP.0000000000000806
- [29] Thomas P, Beaumanoir A, Genton P, Dolisi C,
Chatel M. ‘De novo’ absence status of late onset. Neurology 1992; 42: 104–110.
PMID:1734289, https://doi.org/10.1212/WNL.42.1.104
- [30] Thomas P, Zifkin B, Migneco O, Lebrun C, Darcourt
J, Andermann F. Nonconvulsive status epilepticus of frontal origin. Neurology 1999; 52:
1174–1183. PMID:10214739, https://doi.org/10.1212/WNL.52.6.1174
- [31] Wu CJ. Acute confusional state in type 2 diabetic
patient: non‐convulsive status epilepticus. Geriatr Gerontol Int 2009; 9: 89–91.
PMID:19260985, https://doi.org/10.1111/j.1447-0594.2008.00508.x
