In vivo MRI signatures of hippocampal subfield pathology in intractable epilepsy

Human Brain Mapping

Volumn 37, Issue 3, 2016, Pages 1103-1119

  Goubran, Maged ^a,b   Bernhardt, Boris C ^c   Cantor Rivera, Diego ^a,b   Lau, Jonathan C ^b   Blinston, Charlotte ^a,b   Hammond, Robert R ^d   de Ribaupierre, Sandrine ^b   Burneo, Jorge G ^b   Mirsattari, Seyed M ^b   Steven, David A ^b   Parrent, Andrew G ^b   Bernasconi, Andrea ^b   Bernasconi, Neda ^c   Peters, Terry M ^a,b   Khan, Ali R ^b  

^a ROBARTS RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c MCGILL UNIVERSITY   (Canada)

^d Division of Neuropathology   (Canada)

Author keywords

DTI; Hippocampal sclerosis; Hippocampal subfields; Histology; MRI; Temporal lobe epilepsy; Volumetry

Indexed keywords

BIOLOGICAL MARKER; GLIAL FIBRILLARY ACIDIC PROTEIN;

ADULT; ARTICLE; BRAIN MAPPING; CELL DENSITY; CELL LOSS; CLINICAL TRIAL (TOPIC); CORRELATION ANALYSIS; DIFFUSION WEIGHTED IMAGING; FEMALE; GLIOSIS; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPAL SCLEROSIS; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMAGE ANALYSIS; IN VIVO STUDY; INTRACTABLE EPILEPSY; MAJOR CLINICAL STUDY; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PRIORITY JOURNAL; VOLUMETRY; CELL COUNT; COHORT ANALYSIS; DIFFUSION TENSOR IMAGING; DRUG RESISTANT EPILEPSY; HIPPOCAMPUS; IMAGE PROCESSING; MIDDLE AGED; NERVE CELL; ORGAN SIZE; PATHOLOGY; PROCEDURES; REPRODUCIBILITY; SCLEROSIS; STATISTICAL MODEL; VALIDATION STUDY; YOUNG ADULT;

ADULT; CELL COUNT; COHORT STUDIES; DIFFUSION TENSOR IMAGING; DRUG RESISTANT EPILEPSY; FEMALE; HIPPOCAMPUS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; LINEAR MODELS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEURONS; ORGAN SIZE; REPRODUCIBILITY OF RESULTS; SCLEROSIS; YOUNG ADULT;

EID: 84958165646     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.23090     Document Type: Article

References (75)

1. Adler DH, Pluta J, Kadivar S, Craige C, Gee JC, Avants BB, Yushkevich PA (2014): Histology-derived volumetric annotation of the human hippocampal subfields in postmortem MRI. Neuroimage 84:505-523.
2. Al Sufiani F, Ang LC (2012): Neuropathology of temporal lobe epilepsy. Epilepsy Res Treat 2012:1-13.
3. Ali R, Goubran M, Choudhri O, Zeineh MM (2015): Seven-Tesla MRI and neuroimaging biomarkers for Alzheimer's disease. Neurosurg Focus 39:E4.
4. Beg MF, Miller MI, Trouvé A, Younes L (2005): Computing large deformation metric mappings via geodesic flows of diffeomorphisms. Int J Comput Vis 61:139-157.
5. Bernhardt BC, Hong SJ, Bernasconi A, Bernasconi N (2015): Magnetic resonance imaging pattern learning in temporal lobe epilepsy: Classification and prognostics. Ann Neurol 77:436-446.
6. Blumcke I, Coras R, Miyata H, Ozkara C (2012): Defining clinico-neuropathological subtypes of mesial temporal lobe epilepsy with hippocampal sclerosis. Brain Pathol 22:402-411.
7. Blümcke I, Pauli E, Clusmann H, Schramm J, Becker A, Elger C, Merschhemke M, Meencke HJ, Lehmann T, von Deimling A (2007): A new clinico-pathological classification system for mesial temporal sclerosis. Acta Neuropathol 113:235-244.
8. Blümcke I, Thom M, Aronica E, Armstrong DD, Bartolomei F, Bernasconi A, Bernasconi N, Bien CG, Cendes F, Coras R (2013): International consensus classification of hippocampal sclerosis in temporal lobe epilepsy: A Task Force report from the ILAE Commission on Diagnostic Methods. Epilepsia 54:1315-1329.
9. Briellmann RS, Kalnins RM, Berkovic SF, Jackson GD (2002): Hippocampal pathology in refractory temporal lobe epilepsy T2-weighted signal change reflects dentate gliosis. Neurology 58:265-271.
10. Buckner RL (2004): A unified approach for morphometric and functional data analysis in young, old, and demented adults using automated atlas-based head size normalization: Reliability and validation against manual measurement of total intracranial volume. Neuroimage 23:724-738.
11. Cantor-Rivera D, Khan AR, Goubran M, Mirsattari SM, Peters TM (2015): Detection of temporal lobe epilepsy using support vector machines in multi-parametric quantitative MR imaging. Comput Med Imaging Graph 41:14-28.
12. Cascino GD, Jack CR, Parisi JE, Sharbrough FW, Hirschorn KA, Meyer FB, Marsh WR, O'Brien PC (1991): Magnetic resonance imaging-based volume studies in temporal lobe epilepsy: Pathological correlations. Ann Neurol 30:31-36.
13. Coan AC, Kobayashi E, Li LM, Cendes F (2003): Quantification of hippocampal signal intensity in patients with mesial temporal lobe epilepsy. J Neuroimaging 13:228-233.
14. Coan AC, Kubota B, Bergo FP, Campos BM, Cendes F (2014): 3T MRI quantification of hippocampal volume and signal in mesial temporal lobe epilepsy improves detection of hippocampal sclerosis. Am J Neuroradiol 35:77-83.
15. Coras R, Milesi G, Zucca I, Mastropietro A, Scotti A, Figini M, Mühlebner A, Hess A, Graf W, Tringali G (2014): 7T MRI features in control human hippocampus and hippocampal sclerosis: An ex vivo study with histologic correlations. Epilepsia 55:2003-2016.
16. de Tisi J, Bell GS, Peacock JL, McEvoy AW, Harkness WFJ, Sander JW, Duncan JS (2011): The long-term outcome of adult epilepsy surgery, patterns of seizure remission, and relapse: A cohort study. Lancet 378:1388-1395.
17. Deoni SC (2007): High-resolution T1 mapping of the brain at 3T with driven equilibrium single pulse observation of T1 with high-speed incorporation of RF field inhomogeneities (DESPOT1-HIFI). J Magn Reson Imaging 26:1106-1111.
18. Duvernoy HM, Naidich T, Fatterpekar GM, Raybaud C, Risold PY, Sakvolini U, Scarabino T. (2005): The human Hippocampus: Functional Anatomy, Vascularization and Serial Sections with MRI. Berlin, Heidelberg: Springer Verlag. pp 232.
19. Engel J (2001): A proposed diagnostic scheme for people with epileptic seizures and with epilepsy: Report of the ILAE Task Force on Classification and Terminology. Epilepsia 42:796-803.
20. Eriksson SH, Free SL, Thom M, Martinian L, Symms MR, Salmenpera TM, McEvoy AW, Harkness W, Duncan JS, Sisodiya SM (2007): Correlation of quantitative MRI and neuropathology in epilepsy surgical resection specimens-T2 correlates with neuronal tissue in gray matter. Neuroimage 37:48-55.
21. Eriksson SH, Free SL, Thom M, Symms MR, Martinian L, Duncan JS, Sisodiya SM (2009): Quantitative grey matter histological measures do not correlate with grey matter probability values from in vivo MRI in the temporal lobe. J Neurosci Methods 181:111-118.
22. Focke NK, Yogarajah M, Bonelli SB, Bartlett PA, Symms MR, Duncan JS (2008): Voxel-based diffusion tensor imaging in patients with mesial temporal lobe epilepsy and hippocampal sclerosis. Neuroimage 40:728-737.
23. Fuerst D, Shah J, Kupsky W, Johnson R, Shah A, Hayman-Abello B, Ergh T, Poore Q, Canady A, Watson C (2001): Volumetric MRI, pathological, and neuropsychological progression in hippocampal sclerosis. Neurology 57:184-188.
24. Gibson E, Gómez JA, Moussa M, Crukley C, Bauman G, Fenster A, Ward AD (2012): 3D reconstruction of prostate histology based on quantified tissue cutting and deformation parameters. In: International Society for Optics and Photonics, San Diego, California. p 83170N-83170N-7.
25. Gómez-Isla T, Price JL, McKeel J, DW, Morris JC, Growdon JH, Hyman BT (1996): Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer's disease. J Neurosci 16:4491-4500.
26. Goncalves Pereira PM, Oliveira E, Rosado P (2006): Relative localizing value of amygdalo-hippocampal MR biometry in temporal lobe epilepsy. Epilepsy Res 69:147-164.
27. Goubran M, Crukley C, de Ribaupierre S, Peters TM, Khan AR (2013a): Image registration of ex vivo MRI to sparsely sectioned histology of hippocampal and neocortical temporal lobe specimens. Neuroimage 83:770-781.
28. Goubran M, de Ribaupierre S, Hammond RR, Currie C, Burneo JG, Parrent AG, Peters TM, Khan AR (2015a): Registration of in vivo to ex vivo MRI of surgically resected specimens: A pipeline for histology to in vivo registration. J Neurosci Methods 241:53-65.
29. Goubran M, Hammond RR, de Ribaupierre S, Burneo JG, Mirsattari S, Steven DA, Parrent AG, Peters TM, Khan AR (2015b): Magnetic resonance imaging and histology correlation in the neocortex in temporal lobe epilepsy. Ann Neurol 77:237-250.
30. Goubran M, Rudko DA, Santyr B, Gati J, Szekeres T, Peters TM, Khan AR (2013b): In vivo normative atlas of the hippocampal subfields using multi-echo susceptibility imaging at 7 Tesla. Hum Brain Mapp 35:3588-3601.
31. Groppe DM, Urbach TP, Kutas M (2011): Mass univariate analysis of event-related brain potentials/fields I: A critical tutorial review. Psychophysiology 48:1711-1725.
32. Harrison PJ (2004): The hippocampus in schizophrenia: A review of the neuropathological evidence and its pathophysiological implications. Psychopharmacology 174:151-162.
33. Hennessy MJ, Elwes RD, Binnie CD, Polkey CE (2000): Failed surgery for epilepsy A study of persistence and recurrence of seizures following temporal resection. Brain 123:2445-2466.
34. Howell GA, Welch MG, Frederickson CJ (1984): Stimulation-induced uptake and release of zinc in hippocampal slices. Nature 308:736-738.
35. Huang H, Ceritoglu C, Li X, Qiu A, Miller MI, van Zijl P, Mori S (2008): Correction of B0 susceptibility induced distortion in diffusion-weighted images using large-deformation diffeomorphic metric mapping. Magn Reson Imaging 26:1294-1302.
36. Jackson G, Connelly A, Duncan J, Grünewald R, Gadian D (1993): Detection of hippocampal pathology in intractable partial epilepsy Increased sensitivity with quantitative magnetic resonance T2 relaxometry. Neurology 43:1793-1793.
37. Jardim AP, Neves RSdC, Caboclo LOSF, Lancellotti CLP, Marinho MM, Centeno RS, Cavalheiro EA, Scorza CA, Yacubian EMT (2012): Temporal lobe epilepsy with mesial temporal sclerosis: Hippocampal neuronal loss as a predictor of surgical outcome. Arquivos De Neuro-Psiquiatria 70:319-324.
38. Jurcoane A, Wagner M, Schmidt C, Mayer C, Gracien RM, Hirschmann M, Deichmann R, Volz S, Ziemann U, Hattingen E (2013): Within-lesion differences in quantitative MRI parameters predict contrast enhancement in multiple sclerosis. J Magn Reson Imaging 38:1454-1461.
39. Kerchner GA, Deutsch GK, Zeineh M, Dougherty RF, Saranathan M, Rutt BK (2012): Hippocampal CA1 apical neuropil atrophy and memory performance in Alzheimer's disease. Neuroimage 63:194-202.
40. Khan AR, Goubran M, de Ribaupierre S, Hammond RR, Burneo JG, Parrent AG, Peters TM (2014): Quantitative relaxometry and diffusion MRI for lateralization in MTS and non-MTS temporal lobe epilepsy. Epilepsy Res 108:506-516.
41. Kinoshita M, Hashimoto N, Goto T, Kagawa N, Kishima H, Izumoto S, Tanaka H, Fujita N, Yoshimine T (2008): Fractional anisotropy and tumor cell density of the tumor core show positive correlation in diffusion tensor magnetic resonance imaging of malignant brain tumors. Neuroimage 43:29-35.
42. Kuzniecky R, Bilir E, Gilliam F, Faught E, Palmer C, Morawetz R, Jackson G (1997): Multimodality MRI in mesial temporal sclerosis: Relative sensitivity and specificity. Neurology 49:774-778.
43. Lencz T, McCarthy G, Bronen RA, Scott TM, Inserni JA, Sass KJ, Novelly RA, Kim JH, Spencer DD (1992): Quantitative magnetic resonance imaging in temporal lobe epilepsy: Relationship to neuropathology and neuropsychological function. Ann Neurol 31:629-637.
44. Lockwood-Estrin G, Thom M, Focke NK, Symms MR, Martinian L, Sisodiya SM, Duncan JS, Eriksson SH (2012): Correlating 3T MRI and histopathology in patients undergoing epilepsy surgery. J Neurosci Methods 205:182-189.
45. Mackay C, Webb J, Eldridge P, Chadwick D, Whitehouse G, Roberts N (2000): Quantitative magnetic resonance imaging in consecutive patients evaluated for surgical treatment of temporal lobe epilepsy. Magn Reson Imaging 18:1187-1199.
46. Malykhin NV, Lebel RM, Coupland NJ, Wilman AH, Carter R (2010): In vivo quantification of hippocampal subfields using 4.7 T fast spin echo imaging. Neuroimage 49:1224-1230.
47. Manly BF (2006): Randomization, Bootstrap and Monte Carlo Methods in Biology. Boca Raton, FL: CRC Press.
48. McEwen BS (1999): Stress and hippocampal plasticity. Annu Rev Neurosci 22:105-122.
49. McIntosh AM, Kalnins RM, Mitchell LA, Fabinyi GC, Briellmann RS, Berkovic SF (2004): Temporal lobectomy: Long-term seizure outcome, late recurrence and risks for seizure recurrence. Brain 127:2018-2030.
50. Morrison JH, Hof PR (1997): Life and death of neurons in the aging brain. Science 278:412-419.
51. Mueller S, Stables L, Du A, Schuff N, Truran D, Cashdollar N, Weiner M (2007): Measurement of hippocampal subfields and age-related changes with high resolution MRI at 4T. Neurobiol Aging 28:719-726.
52. Mueller SG, Schuff N, Yaffe K, Madison C, Miller B, Weiner MW (2010): Hippocampal atrophy patterns in mild cognitive impairment and Alzheimer's disease. Hum Brain Mapp 31:1339-1347.
53. Nichols TE, Holmes AP (2002): Nonparametric permutation tests for functional neuroimaging: A primer with examples. Hum Brain Mapp 15:1-25.
54. Parekh MB, Rutt BK, Purcell R, Chen Y, Zeineh MM (2015): Ultra-high resolution in vivo 7.0 T structural imaging of the human hippocampus reveals the endfolial pathway. Neuroimage 112:1-6.
55. Pauli E, Hildebrandt M, Romstöck J, Stefan H, Blümcke I (2006): Deficient memory acquisition in temporal lobe epilepsy is predicted by hippocampal granule cell loss. Neurology 67:1383-1389.
56. Prudent V, Kumar A, Liu S, Wiggins G, Malaspina D, Gonen O (2010): Human hippocampal subfields in young adults at 7.0 T: Feasibility of imaging 1. Radiology 254:900-906.
57. Rugg-Gunn FJ, Eriksson SH, Symms MR, Barker GJ, Thom M, Harkness W, Duncan JS (2002): Diffusion tensor imaging in refractory epilepsy. Lancet 359:1748-1751.
58. Ruifrok AC, Johnston DA (2001): Quantification of histochemical staining by color deconvolution. Anal Quant Cytol Histol 23:291-299.
59. Savitr Sastri BV, Arivazhagan A, Sinha S, Mahadevan A, Bharath RD, Saini J, Jamuna R, Kumar JK, Rao SL, Chandramouli BA, Shankar SK, Satishchandra P (2014): Clinico-pathological factors influencing surgical outcome in drug resistant epilepsy secondary to mesial temporal sclerosis. J Neurol Sci 340:183-190.
60. Schmierer K, Parkes HG, So PW, An SF, Brandner S, Ordidge RJ, Yousry TA, Miller DH (2010): High field (9.4 Tesla) magnetic resonance imaging of cortical grey matter lesions in multiple sclerosis. Brain 133:858-867.
61. Schoene-Bake JC, Keller SS, Niehusmann P, Volmering E, Elger C, Deppe M, Weber B (2014): In vivo mapping of hippocampal subfields in mesial temporal lobe epilepsy: Relation to histopathology. Hum Brain Mapp 35:4718-4728.
62. Šimić G, Bogdanović N (1997): Volume and number of neurons of the human hippocampal formation in normal aging and Alzheimer's disease. J Comp Neurol 379:482-494.
63. Soille, P. (2003): Morphological Image Analysis: Principles and applications. New York: Springer-Verlag.
64. Sommer W (1880): Erkrankung des Ammonshorns als aetiologisches Moment der Epilepsie. Eur Arch Psychiatry Clin Neurosci 10:631-675.
65. Thivard L, Lehéricy S, Krainik A, Adam C, Dormont D, Chiras J, Baulac M, Dupont S (2005): Diffusion tensor imaging in medial temporal lobe epilepsy with hippocampal sclerosis. Neuroimage 28:682-690.
66. Thom M, Eriksson S, Martinian L, Caboclo LO, McEvoy AW, Duncan JS, Sisodiya SM (2009): Temporal lobe sclerosis associated with hippocampal sclerosis in temporal lobe epilepsy: Neuropathological features. J Neuropathol Exp Neurol 68:928-938.
67. Thom M, Liagkouras I, Elliot KJ, Martinian L, Harkness W, McEvoy A, Caboclo LO, Sisodiya SM (2010): Reliability of patterns of hippocampal sclerosis as predictors of postsurgical outcome. Epilepsia 51:1801-1808.
68. Van Paesschen W, Revesz T, Duncan J, King M, Connelly A (1997): Quantitative neuropathology and quantitative magnetic resonance imaging of the hippocampus in temporal lobe epilepsy. Ann Neurol 42:756-766.
69. West MJ, Kawas CH, Stewart WF, Rudow GL, Troncoso JC (2004): Hippocampal neurons in pre-clinical Alzheimer's disease. Neurobiol Aging 25:1205-1212.
70. Wieshmann UC, Symms MR, Barker GJ, Birnie KD, Shorvon SD (1999): Water diffusion in the human hippocampus in epilepsy. Magn Reson Imaging 17:29-36.
71. Winterburn JL, Pruessner JC, Chavez S, Schira MM, Lobaugh NJ, Voineskos AN, Chakravarty MM (2013): A novel in vivo atlas of human hippocampal subfields using high-resolution 3T magnetic resonance imaging. Neuroimage 74:254-265.
72. Wisse LE, Gerritsen L, Zwanenburg JJ, Kuijf HJ, Luijten PR, Biessels GJ, Geerlings MI (2012): Subfields of the hippocampal formation at 7 T MRI: in vivo volumetric assessment. Neuroimage 61:1043-1049.
73. Yushkevich PA, Amaral RS, Augustinack JC, Bender AR, Bernstein JD, Boccardi M, Bocchetta M, Burggren AC, Carr VA, Chakravarty MM (2015): Quantitative comparison of 21 protocols for labeling hippocampal subfields and parahippocampal subregions in in vivo MRI: Towards a harmonized segmentation protocol. Neuroimage 111:526-541.
74. Yushkevich PA, Avants BB, Pluta J, Das S, Minkoff D, Mechanic-Hamilton D, Glynn S, Pickup S, Liu W, Gee JC (2009): A high-resolution computational atlas of the human hippocampus from postmortem magnetic resonance imaging at 9.4 T. Neuroimage 44:385-398.
75. Yushkevich PA, Piven J, Hazlett HC, Smith RG, Ho S, Gee JC, Gerig G (2006): User-guided 3D active contour segmentation of anatomical structures: Significantly improved efficiency and reliability. Neuroimage 31:1116-1128.