crises fébriles et syndrome d'épilepsie mésio-temporale. une

HAL Id: tel-00769920https://tel.archives-ouvertes.fr/tel-00769920

Submitted on 4 Jan 2013

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Crises fébriles et syndrome d’épilepsie mésio-temporale.Une modélisation chez la souris de la théorie du double

chocSophie Hamelin

To cite this version:Sophie Hamelin. Crises fébriles et syndrome d’épilepsie mésio-temporale. Une modélisation chez lasouris de la théorie du double choc. Sciences agricoles. Université de Grenoble, 2012. Français. <NNT: 2012GRENV015>. <tel-00769920>

https://tel.archives-ouvertes.fr/tel-00769920

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Université Joseph Fourier / Université Pierre Mendès France /

Université Stendhal / Université de Savoie / Grenoble INP

THÈSE Pour obtenir le grade de

DOCTEUR DE L’UNIVERSITÉ DE GRENOBLE Spécialité : Neurosciences Neurobiologie

Arrêté ministériel : 7 août 2006

Présentée par

Sophie HAMELIN Thèse dirigée par le Dr Antoine DEPAULIS codirigée par le Pr Philippe KAHANE préparée au sein de l’équipe 9, Dynamique des réseaux synchrones épileptiques, dans l’institut des Neurosciences de Grenoble

Ecole Doctorale chimie et sciences du vivant (218)

CRISES FÉBRILES ET SYNDROME D’ÉPILEPSIE MÉSIO-TEMPORALE UNE MODÉLISATION CHEZ LA SOURIS DE LA THÉORIE DU DOUBLE CHOC

Thèse soutenue publiquement le 23 avril 2012 devant le jury composé de :

Pr Philippe KAHANE PU-PH, INSERM U836, Grenoble (Président)

Dr Stéphane AUVIN PH, INSERM U676, Paris (Rapporteur)

Dr Pierre SZEPETOWSKI DR2, INSERM U901, Marseille (Rapporteur)

Dr Fiona FRANCIS DR2, INSERM UMRS 83917, Paris (Membre)

Dr Antoine DEPAULIS DR2, INSERM U836, Grenoble (Directeur)

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Long-term effects of febrile status epilepticus:

What animalmodels can tell us?Sophie Hamelin, Philippe Kahane, andAntoine Depaulis

GrenobleNeurosciences Institute, Joseph Fourier University – Inserm –Grenoble University Hospital,

Grenoble, France

Febrile Seizures and Mesial

Temporal Lobe Epilepsy

Febrile seizures (FS) are the most common type of sei-

zure in childhood, occurring in 2–5% of children between

6 months and 5 years of age. FS are short-lasting in about

75% of children and are called ‘‘simple FS.’’ However, FS

may have a prolonged duration (>15 min), a focal onset

and/or unilateral postictal deficit, and/or recurrence within

24 h. These seizures are generally termed ‘‘complex FS.’’

In addition, complex FS can potentially result in long-term

effects such as mesial temporal lobe epilepsy (MTLE) or

hippocampal dysfunction. Observations by Falconer et al.

(1964) based on 100 patients who had undergone surgery

for intractable MTLE suggested that the presence of hip-

pocampal sclerosis was associated with a history of com-

plex FS in 30% of patients. Several recent studies have

supported this association and have suggested that com-

plex FS are an initial trauma triggering MTLE (French

et al., 1993).

Neuroimaging studies dealing with the consequences of

complex FS or febrile status epilepticus generally show

hippocampal swelling during the acute stage. Magnetic

resonance imaging (MRI) studies performed in children

with complex FS (48 h and 4–8 months postseizure) have

revealed an increase in hippocampal volume and prolon-

gation of T2 relaxation time. This suggests that complex

FS can result in acute hippocampal edema, which resolves

within several months (Scott et al., 2002, 2003). Although

many neuroimaging studies report acute hippocampal

damage and subsequent atrophy after complex FS, it is not

known whether these patients go on to develop MTLE.

The low frequency of the occurrence of complex FS and

the need of years long-term follow-up from a large cohort

make difficult prospective studies in humans. In particu-

lar, it is difficult from clinical studies to determine

whether early complex FS damage the hippocampus and

cause hippocampal sclerosis. In addition, the hypothesis

that children have complex FS because their hippocampus

was previously damaged as a result of prenatal or perinatal

insult and/or by genetic predisposition (Cendes et al.,

1995) is an important alternative.

Animal Models of Complex

Febrile Seizures

In order to better understand the impact of complex FS

on the developing brain and the effects of previous hippo-

campal damages on FS and their consequences, animals

models have recently been developed in which hyperther-

mic seizures (HS) are induced (Baram et al., 1997; Baram

& Shinnar, 2002). Experimental HS can be evoked in rat

or mouse pups at postnatal day 10 to 11 (P10–11), which

corresponds to the stage of hippocampal development in

children at the age of occurrence of FS. A regulated stream

of heated air (42 € 2!C) induces hyperthermia and sei-

zures are rapidly observed that are characterized by behav-

ioral arrest and facial automatisms concomitant with

amygdala or hippocampal discharges on electroencepha-

lography (EEG) (Baram et al., 1997). Such recurrent sei-

zures are observed for 25–30 min, and approximately

95% of animals survive. Hyperventilation and alkalosis

play an important role in the increased neuronal activity

that leads to seizures (Schuchmann et al., 2009). In addi-

tion, several studies have demonstrated the role of the

interleukin 1ß pathway in this neuronal excitability (Dube

et al., 2004). HS in young rodents result predominantly in

a transient alteration of neurons in the hippocampus and

amygdala as revealed by silver staining of neurons (Toth

et al., 1998). These changes are observed only when

prolonged seizures are observed during hyperthermia;

when HS are prevented by benzodiazepines or barbitu-

rates, few histologic changes are observed. Furthermore,

analyses have shown that neuronal loss and neurogenesis

Address correspondence to Antoine Depaulis, Grenoble – Institut desNeurosciences, Centre de recherche Inserm U 836-UJF-CEA-CHU,Equipe 9: Dynamique des R"seaux Synchrones "pileptiques, Universit"Joseph Fourier – Facult" de M"decine, Domaine de la Merci, 38706 LaTronche Cedex, France. E-mail: [email protected]

Wiley Periodicals, Inc.ª 2009 International League Against Epilepsy

Epilepsia, 50(Suppl. 12):27–28, 2009

doi: 10.1111/j.1528-1167.2009.02353.x

PROCEEDINGS: THE INNSBRUCKCOLLOQUIUMONSTATUS EPILEPTICUS

27

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! !

are limited, even in seizure-sensitive hippocampal areas

(Bender et al., 2003). However, sprouting of mossy fibers

associated with an enhanced sensitivity of the hippocam-

pus is observed: 100% of rats exposed to HS at P10 dis-

play convulsive seizures at the age of 3 months when they

are injected with kainate (5 mg/kg, i.p.), whereas only

25% of controls seize (Bender et al., 2003). Finally, using

long-term EEG recordings, it was found that 35% of rats

that were exposed to HS displayed spontaneous seizures

when adults and that hippocampal spikes were observed in

88% of them (Dube et al., 2006). Several hypotheses have

been raised to explain this enduring increase of hippocam-

pal excitability and, in particular, hyperpolarization-trig-

gered cationic current and cannabinoid receptors appear

critical (Dube et al., 2007).

Febrile Seizures and MTLE:

A Dual Pathology?

The observation of humans with a history of typical

MTLE syndrome, associated with cortical dysplasia or

other lesions in the same hemisphere, has led authors to

propose the concept of dual pathology (Bocti et al., 2003).

According to this concept, FS probably lead to hippocam-

pal sclerosis, especially in the presence of a preexisting

lesion. In animal models, the presence of a localized corti-

cal microgyrus induced in rats by a cryolesion at P1 aggra-

vated HS induced at P10 (Scantlebury et al., 2004).

Furthermore, such cortical dysplasia predisposed rats that

were exposed to HS to chronic limbic seizures together

with deficits of learning and memory without histologic

evidence of cell loss (Scantlebury et al., 2005).

Conclusion

Clinical and experimental studies on FS suggest that

febrile status epilepticus is not associated with massive

cell death in the limbic regions and may not be solely

responsible for hippocampal sclerosis, as observed in

MTLE. However, the interaction of these prolonged sei-

zures with existing dysplasia or lesions appears to increase

the risk of developing MTLE after complex FS. Animal

studies exploring the interactions between changes in

brain development and HS may increase our understand-

ing of the role of febrile status epilepticus in the initiation

of MTLE.

Acknowledgment

This work is supported by Inserm.

We confirm that we have read the Journal’s position on issues involved inethical publication and affirm that this report is consistent with thoseguidelines

Disclosure: The authors declare no conflicts of interest.

References

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98:265–270.Baram TZ, Shinnar S. (2002) Febrile seizures. Academic Press, San

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Mossy fiber plasticity and enhanced hippocampal excitability, with-out hippocampal cell loss or altered neurogenesis, in an animal modelof prolonged febrile seizures.Hippocampus 13:399–412.

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Schuchmann S, Vanhatalo S, Kaila K. (2009) Neurobiological and physi-ological mechanisms of fever-related epileptiform syndromes. BrainDev 31:378–382.

Scott RC, Gadian DG, King MD, Chong WK, Cox TC, Neville BG,Connelly A. (2002) Magnetic resonance imaging findings within5 days of status epilepticus in childhood. Brain 125:1951–1959.

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28

S. Hamelin et al.

Epilepsia, 50(Suppl. 12):27–28, 2009doi: 10.1111/j.1528-1167.2009.02353.x

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Table 1: The initial status epilepticus

Sham

n=7

HS

n=7

p

EEG amplitude (µV)

Left hippocampus 2685±440 2171±429 0.45

Right hippocampus (injected) 1571±217 1584±424 0.62

Spike (n/mn.) 63±13 31±13 0.07

HPD (n/hour) 0.62±0.09 0.66±0.17 1.00

Clonic seizure (n/ 15 hour) 1.43±0.9 0.86±0.9 0.81

!

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Fig 1

Intra-hippocampal and cortical electroencephalographic recording in HS induced in a

mice pup at P10. (A) The normothermic EEG background was composed of arrhythmic, low-

amplitude 3- to 5-Hz activity with superimposed 7- to 9-Hz activity. (B) The start of

hyperthermia induced an increase in the rhythmicity and amplitudes of the slow activity,

associated with asymmetrical pseudo-periodic high-voltage, slow sharp-waves (period 5-7

second). (C) Intermittent medium-amplitude rapid activity appeared, stopped by high-amplitude

hippocampal and cortical spikes associated with myoclonus (Arrow). (D) Focal left

hippocampal discharge (headland of arrow) followed by hindlimb convulsions. (E) Post-

hyperthermia depression associated with EEG burst suppression, characterized by rhythmic

bursts of high-amplitude, epileptic, fast activity punctuated by periods of profound flattening of

the EEG.

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A

B

C

D

E

Hipp. L

Hipp. R

Cortex

Hipp. L

Hipp. R

Cortex

Hipp.L

Hipp. R

Cortex

Hipp. L

Hipp. R

Cortex

Hipp. L

Hipp. R

Cortex

1s.

100µV.

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Fig 2

Hippocampal and cortical local field potential activities during HPDs

(A) HS accelerated hippocampal epileptogenesis (Sham: open circles, n=14; HS: black

diamonds, n=17). Results are presented as mean days±SEM before reaching each stage (Mann-

Whitney, *p<0.05; **p<0.01). (B) Mean HPD duration (p=0.26) and recurrence (p=0.65) were

not different between groups (Sham: white n=11; HS: black n=19). (C) Example of

simultaneous LFP recording of injected hippocampus and cortex during a spontaneous HPD

occurring in a freely-moving mouse. (D) One sample T-statistics of normalized power in the

time–frequency plane (Left, n=84 HPDs from 5 Sham mice; Right, n=60 HPDs from 3 HS

mice; threshold: p<0.05 FWE). It was possible to derive a standard pattern of power by

rescaling the time axis of the time–frequency representation (temporal linear scaling was used to

realign start and end of HPDs; white lines). (E) Two sample T-statistics of normalized power in

the time–frequency plane (HS-Sham; threshold: p<0.05 FWE). HS mice displayed less powerful

increased in low frequency during HPD (blue area) and hippocampal post-HPD depression was

significantly less important (red area).

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1 mV1 s

Inj Hipp

CortexD

E

A B

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3

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1

Stage

*

*

*

*

*

DPI

32 427 372

(s)47

42

37

32

7

2

*p1j+

HPD Duration HPD Recurrence

322

97

72

47

2

1 mV1 s

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72

322

2

72

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2

72

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2

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2

72

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2

72

322

2

42

32

42

32

8

6

8

6

2

32

/32

2

4

-4

Inj H

ipp

Cort

ex

Inj Hipp

Cortex

JU/Ujco"r>2027"HYG

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Fig 3

HS increased GCD and hypertrophy but not neuronal cell loss. Sham group was represented

in white and HS group in black. (A) HS did not increase the pyramidal cell loss represented by

the length of remaining Ammon’s horn at 21 days post-injection (DPI) (Sham n= 11, HS n= 17;

Mann-Whitney p=0.28). (B) HS did not influence the neuronal cell loss in the hilus, CA1 and

CA3, at 21 DPI. (Sham n=8; HS n=7 mice, Mann-Whitney p=1.00, 0.53 and 0.71 for CA1, CA3

and hilus, respectively). (C) HS increased the mean area of dentate gyrus in the injected

hippocampus at 21 DPI (Sham n=12, HS n=17, Mann-Whitney p=0.01). (D) HS increased the

percentage of GCD significantly at 21 and 35 DPI. (10, 21, 35 and 60 DPI, n= 4, 4, 12, 7, 4 in

Sham, n=4, 4, 17, 5 in HS respectively, two-ways ANOVA for days interaction p=0.02, for

group interaction, p=0.009, Bonferroni post-tests p<0.01 21 and 35 DPI) (E) HS increased the

granular cells hypertrophy in the injected hippocampus. (Sham n=7, HS n=7 Mann-Whitney,

p=0.04). (F) Coronal sections of the hippocampus stained with cresyl violet. A progressive

dispersion of the granule cells is observed. Note the neuronal loss in CA1, CA3, and the hilus.

Scale bar, 250 µm.

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6

4

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Fig 4

Western-blots and immuno-staining for reelin in Sham and HS mice at P70, before the KA

injection. (A) A Cajal-Retzius cell in the stratum molecular of HS mice, stained with both reelin

and calretinin. Morphological analysis of these cells showed no increase of reelin

immunopositivity as a visible stained process, feature also seen in sham group. Scale bar: 5 µm

(B) Western-Blot: We observed the 3 known isoforms of reelin detected by the G10 antibody

(400, 310 and 180 kDa). However, in both Sham and HS mice, we saw no significant increase

or decrease in the expression of all of this 3 isoforms (Mann-Whitney Sham n=7 and HS=11).

(C, D) Reelin and Calretinin immunostaining showed no modification in HS group vs. Sham

group. Scale bar: 50 µm, stratum lacunosum and molecular. (E) Cells count in the stratum

molecular and stratum lacunosum showing no difference between groups (Mann-Whitney Sham

n=5, HS n=5).

!

! !

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! !

A B

C D

Calretinin Reelin

Dapi Merge

Calretinin Reelin

Dapi Merge

Calretinin Reelin

Dapi Merge

Sham HS

Sham HS

400 kDa310 kDa

180 kDa

GADPH 37 kDa

Reelin

400 310 180

DO/GADPH0.3

0.2

0.1

0

Calretinin Reelin Merge

Cells/mm75

60

45

30

15

0

!

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! !

Sham HS

GFAP NeuN

DAPI Merge

GFAPNeuN

MergeDAPI

GADPH

GFAP

37 kDa

50 kDa

Sham HS

DO/GADPH1

0

0.5

A

B

GFAP

Western-blots and immuno-staining for GFAP in Sham and HS mice at P70, before the KA injection.

(A) GFAP and NeuN immuno-staining in dentate gyrus, in sham and HS mice

Morphological analysis of these cells showed no modification in the GFAP and NeuN density

and global aspect between groups. Scale bar: 10 µm

(B) Western-Blot: Semi-quantitativ analyse of GFAP showed no difference beween groups

(Mann-Whitney; Sham (white) n=7 and HS (black) n=11).

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