Functional Neuroimaging Strategy in Temporal Lobe Epilepsy: A Comparative Study of 18FDG-PETand 77mTc-HMPAO-SPECT Philippe Ryvlin, MD," Bernard Philippon,; Luc Cinotti, MD,* Jean C Froment, MD,$ Diclier Le Bars, PhD," and Franpis Mauguiere, MD, PhD"

We performed W'nTc-hexamethylpropyleneamineoxime-single-photonemission computed tomography (SPECT) and "F-fluorodeoxyglucose-positron emission tomography (PET) in 20 epileptic patients with well-lateralized temporal electroencephalographic focus, normal computed tomographic scan, and brain magnetic resonance imaging (MRI) either normal (n = 10) or showing nonspecific changes in the epileptogenic temporal lobe (n = 10). In patients with a normal MRl, PET exhibited focal hypometabolism in SO%, whereas SPECT showed corresponding hypoperfusion in only 2 0 9 . In patients with an abnormal MRI, PET and SPECT yielded 100% and 90% sensitivity, respectively. The metabolic and regional cerebral blood flow disturbances were topographically concordant with electroencephalographic and MRI findings in all these patients. Only patients with a large and pronounced hypometabolism on PET images exhibited hypoperfusion on SPECT. Spatial resolution appeared to be the critical factor responsible for the higher sensitivity of PET. However, this superiority of PET did not prove clinically useful in patients whose SPECT was abnormal, particularly when brain MRI showed nonspecific changes in the epileptogenic temporal lobe. Ryvlin P, Philippon B, Cinotti L, Froment JC, Le Bars D, Mauguiere F. Functional neuroimaging strategy in temporal lobe epilepsy: a comparative study of 18FDG-PET and """Tc-HMPAO-SPECT. Ann Neurol 199.?;31:650-656

Positron emission tomography (PET) and singlephoton emission computed tomography (SPECT) have proved helpful for lateralizing the epileptogenic focus and for deciding on a surgical treatment in patients with refractory temporal lobe epilepsy (TLE) El-31. These two neuroimaging techniques investigate closely related functions in epilepsy, usually using "F-fluorodeoxyglucose ("FFDG) and "'""Tc-hexamethylpropyleneamineoxime (""'"Tc-HMPAO) as tracers for cerebral glucose metabolism [ii]and blood flow [5-7), respectively. "FDG-PET is characterized by a higher spatial resolution and a more reliable quantification, but a poorer temporal resolution than """TcHMPAO-SPECT [S]. Because SPECT can use a conventional gamma camera, it is less expensive and more widely available than PET [ 2 , 91. Thus, it has been questioned whether PET offers any clinically relevant information in addition to that provided by SPECT [ 10, 111. The rwo methods were compared in the same population of epileptic patients in only one previous study [12). In this series of 10 patients, the rate of

detection of abnormalities was higher for PET than for SPECT, suggesting that at least in some patients, PET might demonstrate abnormalities not detected o n SPECT. In patients with an abnormal SPECT, additional information might theoretically be provided by PET images due to their higher spatial resolution, but to our knowledge this issue has never been adclressed. Because MRI changes were found to correlate with the degree of PET and SPECT abnormalities in patients with TLE [ 13, 141, one should also consider magnetic resonance imaging (MRI) data when comparing PET and SPECT sensitivity. T o better assess the clinical usefulness of PET in patients with epilepsy, we compared "FDG-PET and "3"Tc-HMPAO-SPEC'~ in 2 0 patients with TLE, with and without nonspecific MRI abnormalities.

From the *CERMEP, a n J the Ikpartments of ?Nuclear Medicine and iNeuro-K't~iioIogy, Neurological Hospiral, Lyon, France.

Address correspondence r o Dr Mauguien:, CERMEP, Hopital Neurologique, 59 Bd Pinel, 69003 Lyori, Irance.

Materials and Methods SzbjeL ts The pertinent clinical data concerning our 2 0 patients are summarized in Table 1 All were wlecccd from larger popu-

Received Jul 8, 1991, and in revised form Sep 18 arid Dec 4 . Accepted for publication Dec 12, 1'991.

650

Copyright 9 1902 by the American Neurological Association

Tdle I , Patietit Summap Epilepsy Patient No. 1

2 3 4 5 6 7

8

9 10

11 12 13 14 15

16 1-

18 10 20 ~

~~~~~~~~~~~~~

Sex

Age (yr) Cause

F M F M F F M M F F M M F F M F M F F F

59 20 20 21 21 37 25 14 37 16 46 52 37

27 35

29 59 22 29 30

Duration (yr) Per Month

...

... P N anoxia Feb convulsion ...

... Feb convulsion

... Feb convulsion

P N anoxid ... Feb convulsion Feb convulsion Feb convulsion ~

~

~

55 14 18 17 15 3 I5 12 25 4 21 15 25 25 8 18 12 6

19 25

EEG Abnormalities

Seizures

1-5 1-5 >10 1-5 1-5 >10 1-5 6-10 1-5 >10 1-5 1-5 > 10 1-5 > 10 >10 1-5 1-5 6-10 >10

PatternJ

Spikeb Ictal

G G, V, OMS 0, OMS, H 0

-

0, v

G 0 G, V V, H V, OMS G, H 0 G, 0 G, 0 0 0 G, H G, 0 V, H G

+

+ +

+

+ + +

+ + +

+

+

+

-

+

-

+

+ +

+ +

-

+ +

+

+ + + +

+

+ +

-

+ -

+ -

MRI Changes

Site

Type

RT LT RT LT RT LT LT LT RT LT LT RT RT RT LT RT LT LT RT LT

A

Site

+ Hyp

... ...

RT LT RT LT RT LT LT LT RT LT ... ... ... ... ... ... ... ...

...

...

.._

...

HYP

A

+

Hyp

HYP HYP HYP HYP HYP HYP A

... ... ... ... ... ...

~

"All patterns included initial l o s s of awareness. hInterictal spikes or spike and wave complexes. EEG = electroencephalojiram, MRI = magnetic resonance imaging; G = gestural automatism; RT = right temporal; A = major atrophy of the temporal pole; Hyp = nonspecific hyperintense signal on T2-weighted images; V = vegetative disorder; OMS = other motor symptoms; LT = left temporal; PN = perinatal; O = oroalimentary automatism; H = hallucination; Feb = febrile.

lation of 55 patients who suffered from refractory complex partial seizures of temporal lobe origin according to clinical and scalp electroencephalographic (EEG) data, and whose computed tomographic (CT) scans were normal. All had a definite lateralized EEG focus, with unilateral focal slow waves and spikes, spike and wave complexes, or ictal discharges observed on several standard scalp EEG recordings. Selection was performed on the basis of MRI data, including axial and coronal T2-weighted images (TR 2,000 msec; TE 60 and 120 msec), and coronal T1-weighted images (TR 500 msec; TE 21 msec). Group 1 included all 10 patients with TLE referred to us whose MRI displayed a nonspecific hyperintense T2 signal (n = 7 ) , severe atrophy (n = l), or both these abnormalities (n = 2) in the epileptogenic temporal lobe. For comparison, we selected 10 of 37 patients with TLE with a normal MRI (Group 2). The two groups were matched with regard to age, gender, history of febrile convulsions or perinatal anoxia, duration of epilepsy, seizure frequency, and side of the EEG focus (see Table 2). Hippocampal volume measurement was not performed and discrete hippocampal asymmetry was not considered in this selection.

Table 2. Clinical Comparability of Patients W i t h and Without an Ablzormnl M R I

Sex ratio (M1F) Age (mean SD) (yr) Perinaral anoxia or febrile convulsions (%) Duration of epilepsy (mean ? SD) (yr) Seizure frequency per month ( 5 5 / > 5 ) (9) Side of the EEG focus (leftiright) (2)

*

MRI

=

Abnormal MRI (n = 10)

Normal MRI (n = 10)

07 27 i 14 40

0.7 38 ? 14 40

18

* 15

17

7

rt

60140

50150

60140

50/50

magnetic resonance imaging; EEG = electroencephalogram.

SPECT and PET Data Acquisition PET study and a second MRI scan were performed on the same day 1 to 12 months after SPECT study (mean F SD,

Ryvlin et al: PET and SPECT in TLE

651

Table 3. SPECT and P E T Detertzon Rate Reguyding M R I Findzngr Abnormal SPECT (%)

Abnormal PET (%)

20 90 55

100 90

McNernar Test of Symmetry v )

~~~~~~~

Normal MRI (n = 10) Abnormal MRI (n = 10) Total (n = 20) SPECT

=

single-photon emission computed romography; PET = positron emmion tomography; MRl

3.6 t 1.4 months). In all patients, MRI findings were unchanged compared with the first MRI scan, and the antiepileptic drug regimen was not modified during the study. """Tc-HMPAO-SPECT and "FDG-PET investigations are described in detail elsewhere {13, 141. In brief, both investigations were performed under EEG monitoring using an eight-channel bipolar montage [ 141. EEG was recorded during the 10 minutes preceding the injection of the tracer and throughout its accumulation in the brain. During that time, patients were lying with eyes closed and ears plugged. SPECT provided eight contiguous orbitomeatal slices, 12.5 mm thick, with an in-plane spatial resolution of 14 mm at full width half maximum (FWHM). These eight slices were used for visual analysis and then pooled in four 25-mm-thick slices for quantitation. PET scanning produced two sets of seven 9-mm-thick orbitomeatal slices spaced by 3 mm, with 6-mm shifts between sets. Spatial resolution in the plane was 7 mm at FWHM.

SPECT and PET Data Analysis SPECT and PET data were reported by two different investigators, each blinded to all the other dam. However, investigators were aware of ictal events occurring during the period of tracer accumulation. Detection of SPECT and PET abnormalities was based on visual analysis. We considered only latcralized regional cerebral blood flow (rCBF) or metabolic disturbances that appeared as an unequivocal asymmetry on at least two successive slices. We used regions of interest (ROIs) and asymmetry index (AI) to compare SPECT and PET regional activities in the interictal state. Two patients were excluded from this analysis because of an ictal study (Patient 1 ) or a technical problem that precluded metabolic quantitation of PET data (Patient 20). Due to the differences in the spatial resolution of SPECT and PET images and in the method used routinely when interpreting these data, ROIs were designed differently for the two investigations as detailed elsewhere C13, 141. We compared SPECT and PET sensitivity in the 20 patients of this study, as well as in the different MRI subgroups, using the McNemar test of symmetry [l5}. We then looked for a correlation between the regional asymmetry index of HMPAO activity and glucose metabolism using simple linear regression (n = 18).

Results EEG Monitoring During SPECT and PET Studies In Patient 1, the EEG showed a right temporal rhythmic slow wave discharge that started 1 minute after "'"Tc-HMPAO injection and lasted for 40 seconds. 652 Annals of Neurology Vol 31 N o 6 June 1992

c0.02 NS

80

io.01 -

magneric resonance im;tging.

Clinical correlation was impeded because the patient was lying quietly in a dark room with her eyes covered This patient frequently had staring spells and wds often not aware of them. No other ictal events werc recorded during the EEG monitoring of our patients

SPECT and PET Sensitiz'ity 1feYiri.s M R l F i r d i n g s SPECT and PET results are summarized in Table 3. Significant asymmetries were detected in 1 1 SPlECT studies ( 5 5 % ), including 1 0 of 19 performed interictally (53%) and the one carried out ictally (Patient I ) . All the interictal abnormahties corresponded t o teniporal hypoperfusion ipsilateral to the EEG focus, wlhich in 1 patient spread to thr: ipsilateral frontoparietal regions. The ictal SPECT study showed temporal hyperperfusion associated with ipsilateral frontoparietal hypoperfusion on the same side as the ictal discharges and the previously demonstrated EEG focus. The 11 patients whose SPECT was abnormal included 0 of the 10 patients with abnormal MRI scans (W?)and 2 of the 10 with normal MRI scans ( 2 0 ( 7 ) . PET study demonstrated focal hypometabolism in 18 patients (90% ), which was ipsilateral t o the EEG focus in all but 1 patient (Patient 14). lnterictal PET abnormalities consisted of various degrees of lateral temporal hypometabolism, involving the ipsilateral rnesial temporal structures in 6 patients and extencling to ipsilateral extratemporal regions in 7 (centroparietal in 5 , frontoparietal in 1, and thalamic in 1). In these iatter patients, hypometabolism was always more pronounced in the temporal lobe than in the other affecred regions. PET sensitivity was 1009 in patients with abnormal MRI scans (n = 10) and XOiX in those whose MRI scans were normal ( n = 10). Overall, PET study was significantly more sensitive than SPECT in the whole population of 20 patients @ < 0.01), as well as in the group with normal MRl scans ( p < 0.02). SPECT and PET detection rates were comparable in patients with abnormal MRI scans.

Relations Between Interictal SPECT and PET Abnormalities All SPECT abnormalities (11 = 1 0 ) were associated with topographically concordant but more extensive hypometabolism on PET study (see Fig 1 ). In fact,

Fig 1 . Patient 7 with loss of contact and oroalimentary automutisms as ictal symptoms and left temporal electroencephalographic abnormalities. Axial T2-weighted magnetic resonance image shows a left mesial temporal increased signal intensity (arrow) (ai; 12S-mm-thick orbitomeatal single-photon emission computed tomographic slices evidence left temporal hypopevfusion (arrows) ibi; 9-mm-thick orbitomeatalpositron emission tomographic slices display left temporoparietal hypometabolism including the mesial temporal cortex (arrows) (ri.

Fig 2. Patient 16 with loss of contact and oroalimentary automatisms as ictal symptoms and right temporal electroencephalographic abnormalities. Orbitomeatal single-photon emission tomogruphic slices 112.5 mm thzcki do not show signijicant asymmetry o f perfusion (a); Orbitomeatalpositron emission tomographic slices (9 mm thick) evidence right tempowpolar hjpometabolism (arrows).

Ryvlin et al: PET and SPECT in

TLE 653

when the anterior one-half of the lateral temporal cortex was metabolically impaired during the interictal state, SPECT study always showed corresponding rCBF disturbances. Conversely, when PET scanning was normal or exhibited hypometabolism confined to the anterior one-third of the temporal lobe, no significant asymmetry was observed on SPECT study (see Fig 2). Thus, there was a relationship between the extent of metabolic abnormalities and the detectability of hypoperfusion. Furthermore, there was a significant correlation between PET and SPECT regional asymmetry index in the temporal lobes ( p < 0.0001) with SPECT A1 lower than that of PET in most patients. PET and SPECT frontal A1 also correlated; however, this correlation proved to depend on the extreme values of an outlier (Patient 3) because it dropped after excluding this patient. The other regional AIs did not show any correlation between the two investigations.

Discussion Our study showed that PET study was significantly more sensitive than SPECT study, with detection rates of 905f and j5%, respectively. However, these two investigations exhibited very comparable hit rates in patients with a nonspecific MRI abnormality. O u r results confirmed those reported by Stefan and colleagues [ 121 suggesting the better diagnostic value of PET scanning compared with SPECT scanning. These authors have evaluated both methods in 10 patients with TLE, 7 of whom had a unilateral EEG focus and a normal C T scan. All these 7 patients exhibited focal hypometabolism on PET study, whereas only 3 showed corresponding unequivocal SPECT abnormalities. The difference between the sensitivities of SPECT and PET scanning in our study was probably due to the better spatial resolution of PET images compared with those of SPECT, rather than to the different type of function investigated. Indeed, glucose metabolism and cerebral blood flow-which correlates closely with """'Tc-HMPAO brain uptake {5-7]-were decreased in a comparable manner at the site of the epileptic focus { l G , 171. W e have also controlled for possible bias related to the fact that SPECT scanning was performed before PET scanning, that is, (1) MRI findings were stable over the period of the present study, (2) the drug regimen was not changed between the two investigations, (3) PET and SPECT studies were performed in different laboratories, by different teams, and separated by more than 1 month in most patients, resulting in minimal habituation-like effect regarding the level of anxiety, and (4)PET and SPECT studies were reported blindly with respect to each other, and the same visual criteria were used to detect significant asymmetry. The role of spatial resolution is further suggested by the fact that, in our series, the metabolic abnormalities that 654 Annals of Neurology

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were not detected by SPECT study were always found mildly intense and restricted to the most anterior part of the lateral temporal cortex. It could be argued that SPECT scanning would have proved comparable with PET scanning if performed during the ictal o r postictal phases. Indeed, ictal and postictal SPECT studies, using either "o'nTc-HMPAO or NININ'-trimethyl-N'-(2 hydroxy-i-methyl-5-'-''1iodobenzyl)-l,3-propanediamine 2 H C P (HIPDM ) were found more sensitive than interictal investigations {2, 3, 7, 181. However, the following limitations apply to this procedure: (1) Patients must undergo long-term monitoring and drug withdrawal (2, 3 , 9 , 181, (2) radioactive tracers must be stored at the monitoring unit [2, 3,9,IS], (3) due to rapid degradation, """'Tc-HMPAO must be reconstituted after the seizure is detected and should be injected into the patient within 5 minutes after seizure onset [2, 181, and (41 HIPDM is markedly more expensive than ""Tc-HMPAO and has limited availability {2, 6, 19-2 1). Consequently, ictal and postictal SPECT studies are not used routinely in most centers. Moreover, ictal and postictal SPECT abnormalities are not always easily interpreted and comparative interictal data are recommended [3, 181. Overall, the difference between PET and SPECT sensitivity demonstrated in our patients is likely to reflect primarily the intrinsic technical limitations of rotating gamma cameras and single-photon emitting radioligands compared with positron emission tomographs and emitting radionuclides. The probability that PET scanning would disclose an abnormality in the temporal lobe not detected by SPECT study was dependent on MRI findings. Patient.r with a N o m a / M R I S c m PET study was abnormal in 80';1 and SPECT study in only 20% of the 10 patients whose MRI scans were normal. In the series of Stefan and colleagues j12), only 2 patients had normal MRI scans; hoth showed focal hypometabolism on PET study and I had ipsilatera1 hyperperfusion on SPECT study. Concerning PET scanning, our results d o not differ from those of recent TLE series [l, 227. Conversely, we found SPECT sensitivity to be markedly lower than that reported by other authors, in patients with normal MRI scans 12, 23, 241. This discrepancy might be related to our conservative criteria for significant abnormalities (see Materials and Methods), which on the other hand increased the reliability of our SPECT findings. In fact, in our series, SPECT abnormalities correlated with EEG, MRI, and PET data in all patients, whereas many other studies showed significant discordance between SPECT and EEG lateralization {2, 24, 25). Although scalp EEG can be misleading [l], this is not likely to explain most of the discordant patients reported in the other series. The adequacy of our criteria is further supported by

the fact that patients with normal SPECT studies never showed extensive hypometabolism on PET images. Thus, PET study was particularly useful in patients with normal MRI scans because in 60% of patients it demonstrated an area of focal hypometabolism too small to be detected by SPECT scanning. The site of hypometabolism was discordant with that of the EEG focus in only 1 patient (Patient 14). This patient had normal MRI scan, a right temporal EEG focus, and left temporal pole hypometabolism. Interestingly, SPECT also suggested left temporal hypoperfusion, although it was not considered a significant abnormality according to our criteria. A second PET study eventually confirmed left temporal pole hypometabolism. PET lateralization has been more reliable than that of scalp-sphenoidal EEG when both were compared with depth-electrode recordings [ 11. Discrepancies between scalp EEG and PET data might also be due to bilateral epileptic foci. PET scanning abnormalities not detected by SPECT study and discordant with EEG data indicate the need for intracranial EEG studies, and are thus of particular interest. Patients with Nonspecific Hyperintense T2 Signal on M R I SPECT and PET studies yielded 70%' and 100% sensitivity, respectively, in patients with nonspecific MRI abnormalities. When abnormal, SPECT and PET studies always indicated the same lateralization as EEG and MRI. Most of the other series reported similar PET detection rates in patients with TLE with nonspecific MRI findings C22, 26, 27). Stefan and colleagues [12) found PET scanning to be abnormal in all 7 patients with TLE with a normal CT scan and a hyperintense T2 signal o n MRI, whereas only 4 patients showed unequivocal SPECT abnormalities. In our series, only 1 patient with an abnormal MR signal and focal hypometabolism on PET scanning had a normal SPECT study. PET scanning did not prove useful when MRI and SPECT study results were concordant. Even though PET scanning sometimes revealed mesial temporal and subcortical hypoactivity not detected by SPECT scanning, these abnormalities were always associated with more pronounced lateral temporal hypometabolism as reported in other series E28-303. A rational functional neuroimaging strategy in patients with TLE would be to consider patients with a normal MRI scan and a normal SPECT study as the best candidates for PET scanning. Those with a nonspecific abnormal magnetic resonance signal undetected on SPECT study might also be candidates for a PET metabolic study. Conversely, there is no evidence that patients with congruent scalp EEG, MRI and SPECT scans need PET study as a part of their presurgical evaluation. This strategy should be reevaluated

whenever significant improvements are made in MRI, SPECT, or PET instrumentation. This work was supported in part by agrant from the French National Fund for Health Care (CNAM). Philippe Ryvlin was granted by the National Institute for Health and Medical Research (INSERM). We are grateful to P. Landais, G. Galy, F. Lavenne, M. Chaze, and J. P. Serra for the collection of PET data, Drs L. Garcia-Larrea, H. Bastuji, and P. Garassus for EEG analysis, and P. Adeleine for sratisrical analysis. We also thank Drs M. Revol and C. Fischer for referring some of the patients to us.

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Functional neuroimaging strategy in temporal lobe epilepsy: a comparative study of 18FDG-PET and 99mTc-HMPAO-SPECT.

We performed 99mTc-hexamethylpropyleneamineoxime-single-photon emission computed tomography (SPECT) and 18F-fluorodeoxyglucose-positron emission tomog...
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