Epilepsy Research 38 (2000) 139 – 149 www.elsevier.com/locate/epilepsyres
Temporal lobe epilepsy with sensory aura: interictal glucose hypometabolism Gilbert Wunderlich a, Michael F. Schu¨ller a,b, Alois Ebner b, Hans Holthausen b, Ingrid Tuxhorn b, Otto W. Witte a, Ru¨diger J. Seitz a,* a
Neurologische Klinik, Heinrich-Heine-Uni6ersita¨t Du¨sseldorf, Moorenstraße 5, P.O. Box 101007, D-40001, Du¨sseldorf, Germany b Epilepsiezentrum Bethel, Bielefeld, Germany Received 30 January 1999; received in revised form 23 May 1999; accepted 16 July 1999
Abstract Patients with mesial temporal lobe epilepsy (mTLE) exhibit marked depressions of the regional cerebral glucose metabolism (rCMRGlu) in the mesiotemporal region. We hypothesised that patients with temporal lobe epilepsy (TLE) who have a bilateral somatosensory or acoustic ( = temporolateral/SII-) aura can be differentiated from mTLE by rCMRGlu depressions primarily involving temporo-perisylvian locations. We therefore used this ictal semiology as a clinical criterion to define a subgroup of such patients and measured the rCMRGlu in 16 patients with TLE as evident from interictal and ictal EEG-video monitoring. Clinically, they presented with medically refractory complex partial seizures and were subjected to presurgical evaluation. The pattern of the interictal rCMRGlu in the TLE patients was different from that observed in patients with mTLE and showed significant depressions ipsilateral to the epileptic focus in mesial temporal and lateral temporal regions but spared the thalamus. The neocortical metabolic depressions were spatially more extended in right than in left TLE patients. Magnetic resonance images (MRI) were either normal (n =5) or revealed unilateral or bilateral hippocampal atrophy/sclerosis (n= 7), or temporal or extratemporal focal cortical dysplasia (n= 4). The selected TLE patients presented here comprise a heterogeneous group showing most pronounced metabolic depressions in the lateral temporal cortex. Thus, our data suggest that non-invasive metabolic imaging can assist in identifying the neocortical symptomatogenic zone in putative temporoperisylvian lobe epilepsy. © 2000 Elsevier Science B.V. All rights reserved. Keywords: Positron emission tomography; Temporal lobe epilepsy; Regional cerebral glucose metabolism; Magnetic resonance imaging
1. Introduction * Corresponding author. Tel.: + 49-211-8118974; fax: +49211-8118485. E-mail address:
[email protected] (R.J. Seitz)
Mesial temporal lobe epilepsy (mTLE) is a clinically and electrophysiologically well defined syndrome (Wieser et al., 1993). Characteristically, seizures start with an epigastric aura, often to-
0920-1211/00/$ - see front matter © 2000 Elsevier Science B.V. All rights reserved. PII: S 0 9 2 0 - 1 2 1 1 ( 9 9 ) 0 0 0 8 3 - 2
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Table 1 Clinical and epidemiologic data of 16 patients with TLEa Left TLE
EEG findings Sex
Age (years)
Duration (years)
Interictal
%*
M
31
31
LT
60–70
LTP
2
F
18
14
LT
20–30
LT
3
F
39
36
LT
Rare
LT
4
M
27
14
LT
41
LT
5
M
33
20
LT/RTPO
70
LTPO
– 80/10%
M
34
29
LT
7
M
17
11
LT/LmT
Rare
95/B5%
MRI
Bilateral tingling in the face Sensation in vagina, thighs, upper body, arms Tingling in both lower legs, arms and tongue Cephalic sensation Sensation of cold in both feet ascending in both legs Tingling in both feet ascending in body and arms Tingling in both hands
MTAL
Surgery
Histology
Outcome
–
–
–
Cyst LmT
1/96
LMTS
Seizure free (2 years), one aura
LMTA
2/96
LTS
seizure free (2 years), still auras
dysplasia L amygdala Normal
5/96 –
Gangliocytoma –
Seizure free (2 years) –
LTP
LMTA
8/96
LTS
Seizure free**
LFT, LT
LMTS, white matter dysplasia LT
4/96
LMTS
Seizure free (2 years)
G. Wunderlich et al. / Epilepsy Research 38 (2000) 139–149
1
6
Aura Ictal
Table 1 (continued) Left TLE
EEG findings Sex
8
Age (years)
Duration (years)
Interictal
Aura %* 66/34%
MRI
Surgery
Histology
Outcome
–
–
RMTS
Still seizures
Ictal
23
13
LPO/LT
LPO, RT
Symmetrical Normal sensation in body, mouth, tongue
9 10 11
F F M
31 14 40
18 11 34
RmT/LmT RT/RP RT
RP RT, LT RT
Acoustic Acoustic Diffuse ascending tingling, alteration of perception Sensation of cold water on the back Sensation of cold in both feet Bilateral somatosensory Tingling in tongue, mouth, lips, fingers of both hands Tingling in the auditory neck
12
F
11
10
RT
95%
RFTP
13
F
17
7
RT/RTP
54/46%
RT
14
F
14
13.5
Central spikes Rare
RFT
15
F
44
37
RT/LT
RTP, RT
Right TLE
16
M
35
32
RT
92/8% 99/1% 100%
84/16%
70%
RFT
Normal Normal RMTS
11/94
R temporo- 12/94 parietal cortical dysplasia Posterior 8/96 hippocampal atrophy Normal
Focal cortical Reduced dysplasia seizure frequency RTS Seizure free (1.5 years)
R
RMTS
3/95
\LMTA/ MTS R temporal dysplasia
11/96
Reduced seizure frequency
G. Wunderlich et al. / Epilepsy Research 38 (2000) 139–149
F
Focal cortical Reduced dysplasia due seizure freto tuberous quency sclerosis
a
L= left, R = right, m =mesial, l =lateral, F =frontal, T = temporal, P =parietal, O = occipetal, MTA = mesiotemporal atrophy, MTS =mesiotemporal sclerosis, TS=temporal sclerosis. * Distribution of interictal spikes. ** Death unrelated to epilepsy 4 months after surgery. 141
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gether with other autonomic or psychic symptoms. This is followed by a complex partial seizure, which usually begins with arrest and stare, oral or complex automatisms, followed by posturing of one upper extremity. MRI and histology reveal ipsilateral hippocampal atrophy or sclerosis (Margerison and Corsellis, 1966; Bahtia et al., 1993; Cendes et al., 1993). Positron emission tomography (PET) using [18F]-2-deoxy-D-glucose (FDG) shows a typical pattern of metabolic
depressions involving the affected temporal lobe including the temporal neocortex, the ipsilateral thalamus, and to some extent the frontal cortex (Henry et al., 1990, 1993; Rausch et al., 1994; Arnold et al., 1996; Jokeit et al., 1997). Recently, extramesiotemporal temporal lobe epilepsy, which clinically is often characterised by bilateral sensory phenomena including tingling sensations in limbs and trunk as well as acoustic auras, has been proposed as a nosological entity
Fig. 1. Topography of significant rCMRGlu-depressions in left TLE (upper row). The rCMRGlu was depressed compared to normal controls in the anterior part of the ipsilateral temporal, the posterior temporolateral cortex, and in the left mesiotemporal region (see Table 2). In right TLE (lower row) the rCMRGlu was depressed in the anterior and posterior ipsilateral temporal cortex and in the mesiotemporal region (see Table 2). R = right, L = left.
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Table 2 Significant rCMRGlu-depressions in TLE patients** Anatomic region
Size (cm3)
Stereotactic coordinatesa (mm)
rCMRGlu [mmol/100 g/min (SD)]
x
y
z
Normals
Patients
Depression (%)
Left TLE L hippocampus L middle temporal gyrus L fusiform gyrus
0.31 1.43 0.94
−20 −52 −47
−21 −19 −42
−16 −10 −16
22.6 (3.9) 33.6 (4.6) 33.7 (2.5)
18.3 (3.1) 25.6 (4.0) 25.7 (2.3)
19 24 24
Right TLE R hippocampus R middle temporal gyrus R superior temporal gyrus R fusiform gyrus R mesial frontal gyrus
0.44 2.60 0.83 0.52 0.36
+29 +59 +64 +44 +10
−18 −22 −27 −57 +41
−16 −4 +11 −16 +14
23.4 31.0 28.5 29.7 32.8
18.9 21.5 18.9 20.5 23.4
19 30 34 31 29
(2.6) (5.8) (5.5) (3.9) (5.9)
(2.4) (6.5) (5.9) (3.6) (5.0)
a
Center of gravity according to Talairach and Tournoux (1988). ** Significant rCMRGlu depressions (PB0.02 uncorrected, PB0.01 corrected for image resolution) in left and right TLE compared with healthy control subjects.
separate from mTLE (Blume et al., 1992). In other cases, there may be complex-partial seizures with motionless stare and dystonic posturing of contralateral extremities as in patients with mTLE. Thus, in an individual patient a differentiation may not always be possible solely based on seizure semiology (O’Brian et al., 1996; Gil-Nagel and Risinger, 1996; Pacia et al., 1996). The perisylvian cortex contains the auditory cortex (Lauter et al., 1985; Sams et al., 1985) and a cortical area that is responsive to sensory stimuli termed the secondary somatosensory area (Lu¨ders et al., 1985; Burton et al., 1993). These cortical areas are usually not affected in mTLE, but are often involved in putative extramesiotemporal lobe epilepsy (Lesser et al., 1983; Blume et al., 1992). Because of the involved anatomical structures including the superior bank of the sylvian fissure, the term temporo-perisylvian epilepsy seems to be more appropriate than extramesiotemporal epilepsy. A focal seizure originating from the perisylvian cortex is likely to induce somatosensory or acoustic auras before other ictal signs occur. Thus, we used the initial ictal semiology of somatosensory or acoustic auras as a criterion to define a subgroup of patients different from mTLE (Lu¨ders and Awad, 1991). Although
Table 3 rCMRGlu depressions in the epileptic temporal lobe compared to the contralateral sidea Lateral
Mesial
Extratemporal
Left TLE 1b 2 3b 4c 5 6b 7b,c 8
xxxx xxx xx xxx xxxx xx xx xxxx
xx xx x x
Right TLE 9 10 11b 12c 13b 14 15b 16c
xxxx xxxx xxx xxxxx xxx xx xx xxx
x
x x
xx
x x
xx x xx
xx xx x
xx x
a xxxxx = 30–35%; xxxx = 25–30%; xxx = 20–25%; xx =15– 20%. x =10–15%; −=B10%. b MTA and MTS. c Cortical dysplasia.
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the pattern of interictal cerebral hypometabolism (Savic et al., 1997). Furthermore, we have shown that depressions of regional cerebral glucose metabolism (rCMRGlu) indicate the ictal symptomatogenic zone in patients with focal motor seizures (Seitz et al., 1996; Schlaug et al., 1997). We therefore mapped the rCMRGlu in TLE patients whose seizures were characterised by an initial bilateral somatosensory or acoustic aura. Patients with olfactory or visual auras were excluded. Our aim was to analyse, whether a typical metabolic pattern in these patients can be differentiated from that in patients with mTLE.
2. Patients and methods
2.1. Patients
Fig. 2. A: Comparison of significant rCMRGlu depressions in the lateral temporal cortex ( ) and in the mesial temporal area ( ) in TLE and mTLE. B: Proportion of mesial versus lateral rCMRGlu-depression (mesial/lateral ratio) in TLE and mTLE, respectively. Note the greater affection of mesiotemporal structures in mTLE. R = right, L = left.
the patterns of interictal hypometabolism in mTLE have been shown to be far more extensive than the epileptic focus involving anatomically connected areas and in part also representing neuronal loss (Henry et al., 1993; Arnold et al., 1996, Ryvlin et al., 1998), there is accumulating evidence that the seizure semiology is reflected by
Sixteen patients with TLE [9 females, 7 males, age 26.7910.8 (SD) years, manifestation age 6.594.6 years, 8 right-, 8 left-sided] were selected from 300 consecutive patients undergoing a presurgical evaluation program on the following criteria: all had an initial bilateral somatosensory (n= 14) or acoustic (n= 2) aura preceding the complex partial seizure (Table 1). All patients had seizures of unilateral temporal origin as demonstrated by continuous interictal and ictal EEGvideo monitoring with scalp and spheroidal electrodes (Table 1). None of the patients had epileptic (ictal) aphasia, olfactory or visual auras. Patients with a history of cerebral trauma and patients with evidence of another cerebral or systemic disease with possible cerebral involvement (e.g. diabetes mellitus) or a cerebral mass lesion were excluded. Also, patients who had undergone neurosurgical procedures prior to this study were excluded. All patients had a high resolution MRI, and a PET scan of the rCMRGlu. None of the patients had an epileptic seizure 24 h prior or during PET imaging. All patients were on anticonvulsive medication during the time of the PET scan including carbamazepine (800–1600 mg/d), valproate (1200–2100 mg/d), primidone (750– 1500 mg/d), gabapentine (900–2400 mg/d) and vigabatrine (2000–4000 mg/d). Ten of the 16 patients were operated after the PET scan.
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Twelve healthy, sex- and age-matched subjects without a history of neurological, psychiatric, or medical disorders served as controls for the PET study. Written informed consent was obtained in accordance with guidelines of the Declaration of Human Rights, Helsinki 1975, and the study approved by the Ethics Committee of the Heinrich Heine University, Du¨sseldorf.
2.2. EEG hyp 6ideo monitoring: All patients underwent intensive EEG-video monitoring using continuous 24-h surface EEG recordings with 44 channels including spheroidal electrodes, digitisation and off-line evaluation. For localisation of interictal spikes see Table 1. The ictal discharges at seizure onset were used for lateralisation and localisation of the epileptic focus as established in systematic EEG-studies on (m)TLE (Morris et al., 1989; Risinger et al., 1989).
2.3. MRI MRls were obtained using a 1.5-T Magnetom (Siemens). The imaging sequences provided axial and coronal T1-weighted (TR 2000 ms, TE 20 ms) and T2-weighted (TR 2000 ms, TE 80 ms) images with a slice thickness of 10 mm. In addition, MR images were recorded applying the 3D-FLASH sequence for high-resolution imaging with isotropic resolution of 1.3 mm. The MRls were read independently by an experienced radiologist and two of the authors (G.W., R.J.S)
2.4. PET The rCMRGlu was measured quantitatively using a SCX PC-4096/7WBPET-camera and FDG as described in detail previously. After determination of the global CMRGlu (Seitz et al., 1994) the mean FDG-PETimages of each patient group were analysed regionally pixel-by-pixel in comparison with the group of age-matched controls. Briefly, t-maps were set at a threshold of t = 2.552 each (P B0.02, uncorrected). To correct for multiple comparisons in the pixel-by-pixel analysis and accounting for the limited spatial resolution of the
145
PET images only clusters of at least 16 suprathreshold pixels were considered significant (Wunderlich et al., 1997). Then, significant rCMRGlu-depressions were localised using overlay on a spatially standardised MRI of a healthy subject and plotted into the stereotactic space of Talairach and Tournoux (1988). Furthermore, the volume of the significant rCMRGlu depressions in the mesial temporal region (hippocampus and parahippocampal gyrus) and in the lateral temporal neocortex (middle temporal gyrus) in these patients were compared to the mTLE-group of Arnold et al. (1996). For this purpose, a mesial/ lateral temporal ratio was calculated. In addition, the rCMRGlu of patients and controls was determined individually in anatomically oriented and homologous regions of interest (ROls) according to Schlaug et al. (1997).
3. Results The two patient groups (right- and left-sided TLE) had a similar mean age at the time of examination. The right-sided TLE patients were 25.89 13.2 (SD) years compared with 27.89 7.9 years of the left TLE patients. The mean age of seizure onset was similar being 5.49 4.4 years for the right TLE group and 6.89 4.8 years for the left TLE group. Thus, also the mean duration of epilepsy in the right TLE group (20.3 9 12.1) was not different from that of the left TLE group (21.09 9.7). Finally, the degree of the seizure disorder was comparable between the two groups of patients as both had a similar frequency of approximately 9.195.8 typical seizures during the 3 months before PET scanning. Only three of 16 patients had a history of febrile convulsions. EEG-video monitoring was lateralising in 15 out of 16 patients showing interictal slowing as well as ictal spikes mostly in the lateral temporal and in the mesial temporal region (Table 1). All patients had an initial bilateral sensory aura. Specifically, some reported of bilateral, sometimes ascending tingling or feeling of cold in upper and lower extremities and body, bilateral cephalic sensations including mouth and tongue, while two experienced an acoustic aura (Table 1). There-
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after, 13 of the patients had psychomotor seizures sometimes with secondary generalisation, while three had focal tonic-clonic seizures with occasional secondary generalisation. MRI was less uniform among the patients. It revealed hippocampal atrophy or sclerosis in seven patients. Four patients had cortical dysplasia involving the temporal, temporo-parietal or hemispheric region. The MRIs of five patients were considered normal (Table 1). Histology performed in those patients who underwent resective neurosurgery demonstrated hippocampal sclerosis in four cases, and global sclerosis of the temporal lobe in three patients. One patient had a gangliocytoma grade and two a focal cortical dysplasia that in one of them was related to tuberous sclerosis (Table 1). PET demonstrated that the mean global CMRGlu of the right TLE group [26.5 9 10.2 (SD) mmol/100 g/min] and of the left TLE patients (27.99 10.9 mmol/100 g/min) was virtually identical to that of the control subjects (27.09 9.9 mmol/100 g/min). However, in both patient groups there were significant depressions of the rCMRGlu pattern compared to the controls. In the group with left-sided TLE rCMRGlu-depressions were detected ipsilateral to the suspected epileptic focus in three adjacent slices of the anterior part of the left temporal and in one slice of the left posterior lateral temporal cortex. Also, there was a small area of reduced rCMRGlu in the left mesial temporal region (Table 2). In patients with right-sided TLE mean rCMRGlu-depressions were detected in the ipsilateral temporal cortex extending over six adjacent slices to parts of the inferior parietal cortex. Specifically, they were located in the lateral temporal cortex (anterior and posterior), and in the mesial temporal region (on one slice). In addition, there was a significant rCMRGlu depression in the mesial frontal cortex (Fig. 1, Table 2). Apart from the larger volume of significant rCMRGlu depressions in right TLE patients due to greater involvement of the lateral temporal cortex, the topography of interictal rCMRGlu-depressions was not different between the right- and the leftsided TLE patients as judged from the involved gyri.
We performed single case analysis by comparing the rCMRGlu in homologue anatomical regions on each side. It became evident that the greatest regional depressions of up to 35% were present in the lateral temporal cortex in each patient (Table 3). Only nine of 16 patients (56%) had a moderately depressed glucose metabolism in the ipsilateral mesial temporal region (up to 20% difference), while in 10 patients extratemporal areas with a 10%-rCMRGlu reduction compared to the contralateral side were detected (Table 3). However, the group-analysis did not show a significant hypometabolism compared to normal controls in the fronto-orbital cortex, the parietal cortex, the thalamus, the contralateral cerebral hemisphere or the cerebellum. In both groups no areas of increased metabolic activity were found. While the degree of the mean rCMRGlu depressions in the lateral and mesial temporal regions in patients of this study was similar to those with mTLE (Arnold et al., 1996), the volumes of significant rCMRGlu depressions were smaller in TLE compared to mTLE patients both in mesial and lateral temporal regions (Fig. 2A). However, there was a marked difference between these two groups, since the mesial temporal region was relatively less affected than the lateral temporal region in the TLE patients compared to the mTLE patients. This was evident from the striking lower ratio of mesial/lateral rCMRGlu depression in left and right TLE compared to left and right mTLE (Fig. 2B).
4. Discussion In the present study right-handed TLE patients with medically refractory complex partial seizures preceded by an initial bilateral sensory aura were investigated. They had been selected on the basis of somatosensory or acoustic auras that are likely to originate from the perisylvian cortex (Lauter et al., 1985; Lu¨ders et al., 1985; Sams et al., 1985; Burton et al., 1993). In this group of patients, the rCMRGlu was most severely depressed in the temporal neocortex (medial and superior temporal gyrus) on the side of the epileptic focus as
G. Wunderlich et al. / Epilepsy Research 38 (2000) 139–149
assessed by interictal or ictal EEG-video monitoring. Furthermore, a less severe hypometabolism was found in ipsilateral mesial temporal structures including the hippocampus. This metabolic pattern was markedly different from the topography of the interictal glucose hypometabolism in mTLE (Arnold et al., 1996). In mTLE metabolic depressions are most severe in the mesiotemporal region including the hippocampal formation. In the TLE patients here, the degree of metabolic depression in this region was similar to those with mTLE, but the spatial extent of mesiotemporal involvement was strikingly smaller in our TLE patients compared to mTLE patients (Fig. 2). Additionally, in mTLE there are remote depressions in the orbitofrontal cortex, in the ipsilateral posterior insula or in the ipsilateral thalamus, which were not present in these patients with TLE. This is in good accordance with a study of Hajek et al. (1993), who also reported a different metabolic pattern in mesiobasal and lateral temporal lobe epilepsy. In contrast to our study, they observed no mesial hypometabolism in patients with lateral origin, even when mesial sclerosis was detected on MRI. This is likely to be due to the region-based analysis used by those authors, while we performed pixel-by-pixel computations. In our series, however, single case analysis demonstrated a mesial temporal hypometabolism in 56% (9/16) of the patients, which was probably related to the presence of interictal spike activity also in the mesial temporal region as observed with spheroidal electrodes. The main area of hypometabolism both in group and individual analysis involved the temporal and perisylvian neocortex and was located adjacent to the acoustic (Lauter et al., 1985) and secondary somatosensory cortex (Burton et al., 1993). As both areas are known to have a bilateral representation (Whitsel et al., 1969; Robinson and Burton, 1980; Manzoni et al., 1989), this may explain the non-lateralised character of the initial aura. However, the rCMRGludepressions were strictly unilateral on the side of the epileptic focus. No transcallosal spread of the metabolic affection was observed. It is interesting
147
to note that in left TLE the temporo-parietal area (Wernicke’s area) was spared. In correspondence to this, these patients did not experience epileptic (ictal) aphasia in contrast to the metabolic pattern and ictal semiology in the study of mTLE (Arnold et al., 1996). In our group of TLE patients MRI revealed mesial temporal sclerosis/atrophy in seven patients. However, the MRI findings were heterogeneous and involved also global temporal sclerosis, white matter dysplasia and focal cortical dysplasia, or were normal. Interestingly, also in a selected group of patients classified as extramesiotemporal epilepsy, the MRI was normal or non-specific in 15 patients, while six exhibited different types of lesions including hippocampal atrophy, tumours, heterotopic grey matter, and cortical dysgenesis (Pacia et al., 1996). Despite the wide spectrum of structural abnormalities in our study, both groups of TLE patients had a clearly lateralised hypometabolism in the temporal neocortex ipsilateral to the lateralised EEG changes. This was also true for single cases, thus indicating homogeneity on an individual basis similar to the group data (Tables 2 and 3). Considering the different topography of interictal glucose metabolism in our investigated patients with TLE and mTLE, the rCMRGlu may support a differentiation between temporo-perisylvian epilepsy and mTLE supplementing clinical, electrophysiological, and structural differences. We suggest that the hypometabolism in the temporal neocortex represents the ictal symptomatogenic zone for the bilateral somatosensory/acoustic aura (Lu¨ders and Awad, 1991; Ebner, 1994). Similarly, a regional hypometabolism has been demonstrated as an indicator of the ictal symptomatogenic zone in frontal lobe epilepsy of adults and children (Chugani, 1994; Seitz et al., 1996; Schlaug et al., 1997). The additional area of hypometabolism in the mesial temporal lobe of our TLE patients may reflect spread of seizure activity along existing anatomical links from the temporal neocortex to the hippocampus and the amygdaloid complex (Whitlock and Nauta, 1956; Gloor 1972; Turner et al., 1980).
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Acknowledgements We thank Dr. A. Lumiani for carefully recording the MRls of the patients. We are grateful to the Institute of Nuclear Chemistry (INC), Research Centre, Ju¨lich for the production of FDG and to A. Wirrwar, Department of Nuclear Medicine, Heinrich-Heine-University Du¨sseldorf for expert technical support during the PET measurements. This study was supported by the Deutsche Forschungsgemeinschaft (Eb 2-1 and Wi 830).
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