Funktionelle Magnetresonanztomografie und Traktografie in der Epilepsiediagnostik: Aktuelle Entwicklungen und ihre klinische Relevanz

Zusammenfassung

Epilepsiechirurgie ist eine effektive und sichere Behandlungsmöglichkeit für Patienten mit medikamentös therapierefraktären Anfällen. Bei 60–70% dieser Epilepsiepatienten kann durch einen neurochirurgischen Eingriff Anfallsfreiheit erreicht werden. Ziel eines solchen epilepsiechirurgischen Eingriffes ist es, die epileptogene Zone zu entfernen, ohne postoperative, insbesondere neuropsychologische Defizite, wie zum Beispiel Sprach- oder Gedächtnisstörungen, zu verursachen.

Dementsprechend ist es notwendig, im Rahmen eines sorgfältigen, präoperativen Monitorings sowohl die Areale des Gehirns, von welchen die Anfälle ausgehen („epileptogene Zone“), als auch die Areale, die für motorische, Sprach- und Gedächtnisfunktionen verantwortlich sind („essentielle Hirnareale“) samt den verbindenden Faserstrukturen, sorgfältig zu lokalisieren. Große Fortschritte im Bereich der bildgebenden Verfahren haben die Epilepsiechirurgie in den letzten Jahren revolutioniert. Die funktionelle Magnetresonanztomografie (fMRT) wird zusehends zur Lokalisation des primären motorischen und somatosensorischen Kortex sowie zur Lateralisation von Sprachfunktionen eingesetzt. Rezente Studien sind vielversprechend, dass die fMRT dazu beitragen kann, das individuelle Risiko für postoperative Sprach- und Gedächtnisdefizite näher bestimmen zu können. Mittels Traktografie können die Bahnen der weißen Substanz visuell dargestellt werden, wobei für die Epilepsiechirurgie derzeit vor allem die Darstellung der Pyramidenbahn und der Sehstrahlung klinisch relevant ist. Beide Methoden können zusammen mit anderen strukturellen und funktionellen bildgebenden Verfahren entscheidend zu einer weiteren Verbesserung des postoperativen Outcomes nach epilepsiechirurgischen Eingriffen beitragen, indem die epileptogene Zone, die entfernt werden muss, und der eloquente Cortex, der erhalten bleiben soll, besser definiert werden können.

Abstract

Epilepsy surgery offers an effective and safe treatment option for patients with medically refractory seizures rendering 60–70% of them seizure free. The goals of epilepsy surgery are to remove the brain areas generating the seizures without causing neuropsychological deficits such as language or memory dysfunction. This requires accurate localisation of the brain areas generating the seizures (‘epileptogenic zone’), as well as areas responsible for motor and cognitive functions, such as language and memory (‘essential brain regions’) and their connecting fibers during presurgical evaluation. Functional magnetic resonance imaging (fMRI) is a useful tool to lateralise language and localise primary motor, somatosensory and language areas; it also shows promise for predicting the effects of temporal lobe resection on memory function. Tractography can be used to visualise cerebral white matter tracts, which further helps predicting and reducing the risk of surgery. Both methods can be integrated with other MR imaging modalities to improve surgical strategies tailored to individual patients with regard to functional outcome, by virtue of the definition of epileptic cerebral areas that need to be resected and eloquent areas that need to be spared.

Schlüsselwörter

Sprache - Gedächtnis - Motorik - Sehstrahlung - Lateralisation - Lokalisation

Key words

language - memory - motor functions - optic radiation - lateralisation - localisation

• Literatur

• 1 Wiebe S, Blume WT, Girvin JP et al. A randomized, controlled trial of surgery for temporal-lobe epilepsy. N Engl J Med 2001; 345: 311-318
• 2 Spencer S, Huh L. Outcomes of epilepsy surgery in adults and children. Lancet Neurol 2008; 7: 525-537
• 3 Davies KG, Bell BD, Bush AJ et al. Naming decline after left anterior temporal lobectomy correlates with pathological status of resected hippocampus. Epilepsia 1998; 39: 407-419
• 4 Hermann BP, Seidenberg M, Haltiner A et al. Relationship of age at onset, chronologic age, and adequacy of preoperative performance to verbal memory change after anterior temporal lobectomy. Epilepsia 1995; 36: 137-145
• 5 Sabsevitz DS, Swanson SJ, Morris GL et al. Memory outcome after left anterior temporal lobectomy in patients with expected and reversed Wada memory asymmetry scores. Epilepsia 2001; 42: 1408-1415
• 6 Helmstaedter C, Elger CE. Cognitive consequences of two-thirds anterior temporal lobectomy on verbal memory in 144 patients: a three-month follow-up study. Epilepsia 1996; 37: 171-180
• 7 Haag A, Knake S, Hamer HM et al. The Wada test in Austrian, Dutch, German, and Swiss epilepsy centers from 2000 to 2005: a review of 1421 procedures. Epilepsy Behav 2008; 13: 83-89
• 8 Bittar RG, Olivier A, Sadikot AF et al. Presurgical motor and somatosensory cortex mapping with functional magnetic resonance imaging and positron emission tomography. J Neurosurg 1999; 91: 915-921
• 9 Guzzetta A, Staudt M, Petacchi E et al. Brain representation of active and passive hand movements in children. Pediatr Res 2007; 61: 485-490
• 10 Yetkin FZ, Mueller WM, Morris GL et al. Functional MR activation correlated with intraoperative cortical mapping. AJNR Am J Neuroradiol 1997; 18: 1311-1315
• 11 De Tiege X, Connelly A, Liegeois F et al. Influence of motor functional magnetic resonance imaging on the surgical management of children and adolescents with symptomatic focal epilepsy. Neurosurgery 2009; 64: 856-864 discussion 864
• 12 Binder JR, Swanson SJ, Hammeke TA et al. Determination of language dominance using functional MRI: a comparison with the Wada test. Neurology 1996; 46: 978-984
• 13 Wellmer J, Weber B, Weis S et al. Strongly lateralized activation in language fMRI of atypical dominant patients-implications for presurgical work-up. Epilepsy Res 2008; 80: 67-76
• 14 Woermann FG, Jokeit H, Luerding R et al. Language lateralization by Wada test and fMRI in 100 patients with epilepsy. Neurology 2003; 61: 699-701
• 15 Gaillard WD, Balsamo L, Xu B et al. fMRI language task panel improves determination of language dominance. Neurology 2004; 63: 1403-1408
• 16 Gaillard WD, Balsamo L, Xu B et al. Language dominance in partial epilepsy patients identified with an fMRI reading task. Neurology 2002; 59: 256-265
• 17 Springer JA, Binder JR, Hammeke TA et al. Language dominance in neurologically normal and epilepsy subjects: a functional MRI study. Brain 1999; 122: 2033-2046
• 18 Gaillard WD, Berl MM, Moore EN et al. Atypical language in lesional and nonlesional complex partial epilepsy. Neurology 2007; 69: 1761-1771
• 19 Berl MM, Balsamo LM, Xu B et al. Seizure focus affects regional language networks assessed by fMRI. Neurology 2005; 65: 1604-1611
• 20 Liegeois F, Connelly A, Cross JH et al. Language reorganization in children with early-onset lesions of the left hemisphere: an fMRI study. Brain 2004; 127: 1229-1236
• 21 Weber B, Wellmer J, Reuber M et al. Left hippocampal pathology is associated with atypical language lateralization in patients with focal epilepsy. Brain 2006; 129: 346-351
• 22 Wellmer J, Weber B, Urbach H et al. Cerebral lesions can impair fMRI-based language lateralization. Epilepsia 2009; 50: 2213-2224
• 23 Janszky J, Mertens M, Janszky I et al. Left-sided interictal epileptic activity induces shift of language lateralization in temporal lobe epilepsy: an fMRI study. Epilepsia 2006; 47: 921-927
• 24 Waites AB, Briellmann RS, Saling MM et al. Functional connectivity networks are disrupted in left temporal lobe epilepsy. Ann Neurol 2006; 59: 335-343
• 25 Noppeney U, Price CJ, Duncan JS et al. Reading skills after left anterior temporal lobe resection: an fMRI study. Brain 2005; 128: 1377-1385
• 26 Bonelli SB, Thompson PJ, Yogarajah M et al. Imaging language networks before and after anterior temporal lobe resection – results of a longitudinal fMRI study. Epilepsia 2012; [in press]
• 27 Sabsevitz DS, Swanson SJ, Hammeke TA et al. Use of preoperative functional neuroimaging to predict language deficits from epilepsy surgery. Neurology 2003; 60: 1788-1792
• 28 Giussani C, Roux FE, Ojemann J et al. Is preoperative functional magnetic resonance imaging reliable for language areas mapping in brain tumor surgery? Review of language functional magnetic resonance imaging and direct cortical stimulation correlation studies. Neurosurgery 2010; 66: 113-120
• 29 Ivnik RJ, Sharbrough FW, Laws Jr ER. Effects of anterior temporal lobectomy on cognitive function. J Clin Psychol 1987; 43: 128-137
• 30 Spiers HJ, Burgess N, Maguire EA et al. Unilateral temporal lobectomy patients show lateralized topographical and episodic memory deficits in a virtual town. Brain 2001; 124: 2476-2489
• 31 Squire LR, Zola-Morgan S. The medial temporal lobe memory system. Science 1991; 253: 1380-1386
• 32 Kelley WM, Miezin FM, McDermott KB et al. Hemispheric specialization in human dorsal frontal cortex and medial temporal lobe for verbal and nonverbal memory encoding. Neuron 1998; 20: 927-936
• 33 Golby AJ, Poldrack RA, Brewer JB et al. Material-specific lateralization in the medial temporal lobe and prefrontal cortex during memory encoding. Brain 2001; 124: 1841-1854
• 34 Detre JA, Maccotta L, King D et al. Functional MRI lateralization of memory in temporal lobe epilepsy. Neurology 1998; 50: 926-932
• 35 Powell HW, Koepp MJ, Symms MR et al. Material-specific lateralization of memory encoding in the medial temporal lobe: blocked versus event-related design. Neuroimage 2005; 27: 231-239
• 36 Bonelli SB, Powell RH, Yogarajah M et al. Imaging memory in temporal lobe epilepsy: predicting the effects of temporal lobe resection. Brain 2010; 133: 1186-1199
• 37 Jokeit H, Okujava M, Woermann FG. Memory fMRI lateralizes temporal lobe epilepsy. Neurology 2001; 57: 1786-1793
• 38 Powell HW, Richardson MP, Symms MR et al. Reorganization of verbal and nonverbal memory in temporal lobe epilepsy due to unilateral hippocampal sclerosis. Epilepsia 2007; 48: 1512-1525
• 39 Richardson MP, Strange BA, Duncan JS et al. Preserved verbal memory function in left medial temporal pathology involves reorganisation of function to right medial temporal lobe. Neuroimage 2003; 20 (Suppl. 01) S112-S119
• 40 Jokeit H, Ebner A, Holthausen H et al. Individual prediction of change in delayed recall of prose passages after left-sided anterior temporal lobectomy. Neurology 1997; 49: 481-487
• 41 de Tisi J, Bell GS, Peacock JL et al. The long-term outcome of adult epilepsy surgery, patterns of seizure remission, and relapse: a cohort study. Lancet 2011; 378: 1388-1395
• 42 Chelune GJ, Naugle RI, Luders H et al. Prediction of cognitive change as a function of preoperative ability status among temporal lobectomy patients seen at 6-month follow-up. Neurology 1991; 41: 399-404
• 43 Frings L, Wagner K, Halsband U et al. Lateralization of hippocampal activation differs between left and right temporal lobe epilepsy patients and correlates with postsurgical verbal learning decrement. Epilepsy Res 2008; 78: 161-170
• 44 Loring DW, Meador KJ, Lee GP et al. Wada memory asymmetries predict verbal memory decline after anterior temporal lobectomy. Neurology 1995; 45: 1329-1333
• 45 Lee TM, Yip JT, Jones-Gotman M. Memory deficits after resection from left or right anterior temporal lobe in humans: a meta-analytic review. Epilepsia 2002; 43: 283-291
• 46 Chelune GJ. Hippocampal adequacy versus functional reserve: predicting memory functions following temporal lobectomy. Arch Clin Neuropsychol 1995; 10: 413-432
• 47 Hermann BP, Wyler AR, Somes G et al. Pathological status of the mesial temporal lobe predicts memory outcome from left anterior temporal lobectomy. Neurosurgery 1992; 31: 652-656
• 48 Trenerry MR, Jack Jr. CR, Ivnik RJ et al. MRI hippocampal volumes and memory function before and after temporal lobectomy. Neurology 1993; 43: 1800-1805
• 49 Baxendale S, Thompson P, Harkness W et al. Predicting memory decline following epilepsy surgery: a multivariate approach. Epilepsia 2006; 47: 1887-1894
• 50 Lineweaver TT, Morris HH, Naugle RI et al. Evaluating the contributions of state-of-the-art assessment techniques to predicting memory outcome after unilateral anterior temporal lobectomy. Epilepsia 2006; 47: 1895-1903
• 51 Baxendale S. The role of functional MRI in the presurgical investigation of temporal lobe epilepsy patients: a clinical perspective and review. J Clin Exp Neuropsychol 2002; 24: 664-676
• 52 Binder JR, Sabsevitz DS, Swanson SJ et al. Use of preoperative functional MRI to predict verbal memory decline after temporal lobe epilepsy surgery. Epilepsia 2008; 49: 1377-1394
• 53 Dupont S, Duron E, Samson S et al. Functional MR imaging or Wada test: which is the better predictor of individual postoperative memory outcome?. Radiology 2010; 255: 128-134
• 54 Rabin ML, Narayan VM, Kimberg DY et al. Functional MRI predicts post-surgical memory following temporal lobectomy. Brain 2004; 127: 2286-2298
• 55 Loring DW, Lee GP, Meador KJ et al. The intracarotid amobarbital procedure as a predictor of memory failure following unilateral temporal lobectomy. Neurology 1990; 40: 605-610
• 56 Baxendale S, Thompson PJ, Duncan JS. Improvements in memory function following anterior temporal lobe resection for epilepsy. Neurology 2008; 71: 1319-1325
• 57 Richardson MP, Strange BA, Duncan JS et al. Memory fMRI in left hippocampal sclerosis: optimizing the approach to predicting postsurgical memory. Neurology 2006; 66: 699-705
• 58 Richardson MP, Strange BA, Thompson PJ et al. Pre-operative verbal memory fMRI predicts post-operative memory decline after left temporal lobe resection. Brain 2004; 127: 2419-2426
• 59 Janszky J, Jokeit H, Kontopoulou K et al. Functional MRI predicts memory performance after right mesiotemporal epilepsy surgery. Epilepsia 2005; 46: 244-250
• 60 Powell HW, Richardson MP, Symms MR et al. Preoperative fMRI predicts memory decline following anterior temporal lobe resection. J Neurol Neurosurg Psychiatry 2008; 79: 686-693
• 61 Binder JR, Swanson SJ, Sabsevitz DS et al. A comparison of two fMRI methods for predicting verbal memory decline after left temporal lobectomy: language lateralization versus hippocampal activation asymmetry. Epilepsia 2010; 51: 618-626
• 62 Axmacher N, Mormann F, Fernandez G et al. Sustained neural activity patterns during working memory in the human medial temporal lobe. J Neurosci 2007; 27: 7807-7816
• 63 Voets NL, Adcock JE, Stacey R et al. Functional and structural changes in the memory network associated with left temporal lobe epilepsy. Hum Brain Mapp 2009; 30: 4070-4081
• 64 Catani M, Howard RJ, Pajevic S et al. Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage 2002; 17: 77-94
• 65 Guye M, Parker GJ, Symms M et al. Combined functional MRI and tractography to demonstrate the connectivity of the human primary motor cortex in vivo. Neuroimage 2003; 19: 1349-1360
• 66 Kimiwada T, Juhasz C, Makki M et al. Hippocampal and thalamic diffusion abnormalities in children with temporal lobe epilepsy. Epilepsia 2006; 47: 167-175
• 67 Salmenpera TM, Simister RJ, Bartlett P et al. High-resolution diffusion tensor imaging of the hippocampus in temporal lobe epilepsy. Epilepsy Res 2006; 71: 102-106
• 68 Goncalves Pereira PM, Oliveira E, Rosado P. Apparent diffusion coefficient mapping of the hippocampus and the amygdala in pharmaco-resistant temporal lobe epilepsy. AJNR Am J Neuroradiol 2006; 27: 671-683
• 69 Widjaja E, Blaser S, Miller E et al. Evaluation of subcortical white matter and deep white matter tracts in malformations of cortical development. Epilepsia 2007; 48: 1460-1469
• 70 Guye M, Ranjeva JP, Bartolomei F et al. What is the significance of interictal water diffusion changes in frontal lobe epilepsies?. Neuroimage 2007; 35: 28-37
• 71 Thivard L, Adam C, Hasboun D et al. Interictal diffusion MRI in partial epilepsies explored with intracerebral electrodes. Brain 2006; 129: 375-385
• 72 Concha L, Beaulieu C, Gross DW. Bilateral limbic diffusion abnormalities in unilateral temporal lobe epilepsy. Ann Neurol 2005; 57: 188-196
• 73 Concha L, Beaulieu C, Wheatley BM et al. Bilateral white matter diffusion changes persist after epilepsy surgery. Epilepsia 2007; 48: 931-940
• 74 Yogarajah M, Powell HW, Parker GJ et al. Tractography of the parahippocampal gyrus and material specific memory impairment in unilateral temporal lobe epilepsy. Neuroimage 2008; 40: 1755-1764
• 75 Diehl B, Busch RM, Duncan JS et al. Abnormalities in diffusion tensor imaging of the uncinate fasciculus relate to reduced memory in temporal lobe epilepsy. Epilepsia 2008; 49: 1409-1418
• 76 Focke NK, Yogarajah M, Bonelli SB et al. Voxel-based diffusion tensor imaging in patients with mesial temporal lobe epilepsy and hippocampal sclerosis. Neuroimage 2008; 40: 728-737
• 77 Schoene-Bake JC, Faber J, Trautner P et al. Widespread affections of large fiber tracts in postoperative temporal lobe epilepsy. Neuroimage 2009; 46: 569-576
• 78 Powell HW, Parker GJ, Alexander DC et al. Abnormalities of language networks in temporal lobe epilepsy. Neuroimage 2007; 36: 209-221
• 79 McDonald CR, Ahmadi ME, Hagler DJ et al. Diffusion tensor imaging correlates of memory and language impairments in temporal lobe epilepsy. Neurology 2008; 71: 1869-1876
• 80 Ahmadi ME, Hagler Jr. DJ, McDonald CR et al. Side matters: diffusion tensor imaging tractography in left and right temporal lobe epilepsy. AJNR Am J Neuroradiol 2009; 30: 1740-1747
• 81 Govindan RM, Makki MI, Sundaram SK et al. Diffusion tensor analysis of temporal and extra-temporal lobe tracts in temporal lobe epilepsy. Epilepsy Res 2008; 80: 30-41
• 82 Powell HW, Parker GJ, Alexander DC et al. Imaging language pathways predicts postoperative naming deficits. J Neurol Neurosurg Psychiatry 2008; 79: 327-330
• 83 Yogarajah M, Focke NK, Bonelli SB et al. The structural plasticity of white matter networks following anterior temporal lobe resection. Brain 2010; 133: 2348-2364
• 84 Kikuta K, Takagi Y, Nozaki K et al. Early experience with 3-T magnetic resonance tractography in the surgery of cerebral arteriovenous malformations in and around the visual pathway. Neurosurgery 2006; 58: 331-337
• 85 Yamamoto T, Yamada K, Nishimura T et al. Tractography to depict three layers of visual field trajectories to the calcarine gyri. Am J Ophthalmol 2005; 140: 781-785
• 86 Powell HW, Parker GJ, Alexander DC et al. MR tractography predicts visual field defects following temporal lobe resection. Neurology 2005; 65: 596-599
• 87 Winston GP, Yogarajah M, Symms MR et al. Diffusion tensor imaging tractography to visualize the relationship of the optic radiation to epileptogenic lesions prior to neurosurgery. Epilepsia 2011; 52: 1430-1438
• 88 Yogarajah M, Focke NK, Bonelli S et al. Defining Meyer’s loop-temporal lobe resections, visual field deficits and diffusion tensor tractography. Brain 2009; 132: 1656-1668