Top

Published in:

01-11-2015 | Diagnostic Neuroradiology

Functional hemispherectomy: postoperative motor state and correlation to preoperative DTI

Authors: M. Nelles, H. Urbach, R. Sassen, J. C. Schöne-Bake, H. Tschampa, F. Träber, D. Delev, C. E. Elger, A. Jurcoane, E. Hattingen

Published in: Neuroradiology | Issue 11/2015

Abstract

Introduction

Functional hemispherectomy (FH) is an infrequent method to reduce seizure frequency in patients with intractable epilepsy. The risk that hemispherotomy injures brain structures involved in residual motor function is challenging to predict. Our purpose was to evaluate MR diffusion tensor imaging (DTI) to preoperatively assess residual ipsilateral motor function prior to FH.

Methods

We applied DTI in 34 patients scheduled for FH to perform fiber tracking in healthy and damaged hemispheres of the corticospinal tracts (CSTs) and of the corpus callosum. We assessed the CSTs and the commissural fibers for streamline count, for fractional anisotropy (FA), and for respective ratios (affected/unaffected side). We correlated these DTI values to post-to-prior changes of muscle strength and evaluated their diagnostic accuracy.

Results

FA of the affected CSTs and of commissural fibers was significantly higher in patients with postoperative loss of muscle strength compared to patients without (p = 0.014 and p = 0.008). In contrast, CST FA from healthy hemispheres was not different between both groups. Ratios of streamline counts and FA from CSTs were higher in patients with postoperative reduced muscle strength compared to those without (1.14 ± 0.22 vs. 0.58 ± 0.14, p = 0.040; 0.93 ± 0.05 vs. 0.74 ± 0.03, p = 0.003). CSTs’ normalized FA ratio greater than −0.085 predicted loss of muscle strength with 80 % sensitivity and 69.6 % specificity.

Conclusion

Preoperative tracking of the CST and of commissural fibers contributes to the prediction of postoperative motor outcome after functional hemispherectomy.

Kossoff EH, Vining EP, Pillas DJ, Pyzik PL, Avellino AM, Carson BS, Freeman JM (2003) Hemispherectomy for intractable unihemispheric epilepsy etiology vs outcome. Neurology 61(7):887–890CrossRefPubMed

Jonas R, Nguyen S, Hu B, Asarnow RF, LoPresti C, Curtiss S, DeBode S, Yudovin S, Shields WD, Vinters HV, Mathern GW (2004) Cerebral hemispherectomy: hospital course, seizure, developmental, language, and motor outcomes. Neurology 62(10):1712–1721CrossRefPubMed

Duchowny M (2004) Hemispherectomy for epilepsy: when is one half better than two? Neurology 62(10):1664–1665CrossRefPubMed

Van Empelen R, Jennekens-Schinkel A, Buskens E, Helders PJ, Van NO (2004) Functional consequences of hemispherectomy. Brain 127(Pt 9):2071–2079CrossRefPubMed

Schramm J, Delev D, Wagner J, Elger CE, von Lehe M (2012) Seizure outcome, functional outcome, and quality of life after hemispherectomy in adults. Acta neurochirurgica 154(9):1603–1612. doi:10.1007/s00701-012-1408-z CrossRefPubMed

Schramm J, Kuczaty S, Sassen R, Elger CE, von Lehe M (2012) Pediatric functional hemispherectomy: outcome in 92 patients. Acta neurochirurgica 154(11):2017–2028. doi:10.1007/s00701-012-1481-3 CrossRefPubMed

Binder DK, Schramm J (2006) Transsylvian functional hemispherectomy. Childs Nerv Syst 22(8):960–966. doi:10.1007/s00381-006-0131-6 CrossRefPubMed

Staudt M, Gerloff C, Grodd W, Holthausen H, Niemann G, Krageloh-Mann I (2004) Reorganization in congenital hemiparesis acquired at different gestational ages. AnnNeurol 56(6):854–863

Staudt M, Grodd W, Gerloff C, Erb M, Stitz J, Krageloh-Mann I (2002) Two types of ipsilateral reorganization in congenital hemiparesis: a TMS and fMRI study. Brain 125(Pt 10):2222–2237CrossRefPubMed

10.

Staudt M, Grodd W, Niemann G, Wildgruber D, Erb M, Krageloh-Mann I (2001) Early left periventricular brain lesions induce right hemispheric organization of speech. Neurology 57(1):122–125CrossRefPubMed

11.

Staudt M, Krageloh-Mann I, Grodd W (2005) Ipsilateral corticospinal pathways in congenital hemiparesis on routine magnetic resonance imaging. PediatrNeurol 32(1):37–39

12.

Staudt M, Lidzba K, Grodd W, Wildgruber D, Erb M, Krageloh-Mann I (2002) Right-hemispheric organization of language following early left-sided brain lesions: functional MRI topography. Neuroimage 16(4):954–967CrossRefPubMed

13.

Staudt M, Niemann G, Grodd W, Krageloh-Mann I (2000) The pyramidal tract in congenital hemiparesis: relationship between morphology and function in periventricular lesions. Neuropediatrics 31(5):257–264CrossRefPubMed

14.

Beaulieu C, Allen PS (1994) Water diffusion in the giant axon of the squid: implications for diffusion-weighted MRI of the nervous system. Magn Reson Med 32(5):579–583CrossRefPubMed

15.

Beaulieu C, Allen PS (1994) Determinants of anisotropic water diffusion in nerves. Magn Reson Med 31(4):394–400CrossRefPubMed

16.

Mori S, Kaufmann WE, Davatzikos C, Stieltjes B, Amodei L, Fredericksen K, Pearlson GD, Melhem ER, Solaiyappan M, Raymond GV, Moser HW, van Zijl PC (2002) Imaging cortical association tracts in the human brain using diffusion-tensor-based axonal tracking. Magn ResonMed 47(2):215–223CrossRef

17.

Winston GP (2012) The physical and biological basis of quantitative parameters derived from diffusion MRI. Quant Imaging Med Surg 2(4):254–265. doi:10.3978/j.issn.2223-4292.2012.12.05 PubMedCentralPubMed

18.

Beaulieu C (2002) The basis of anisotropic water diffusion in the nervous system - a technical review. NMR in biomedicine 15(7–8):435–455. doi:10.1002/nbm.782 CrossRefPubMed

19.

Jones DK, Knosche TR, Turner R (2013) White matter integrity, fiber count, and other fallacies: the do’s and don’ts of diffusion MRI. NeuroImage 73:239–254. doi:10.1016/j.neuroimage.2012.06.081 CrossRefPubMed

20.

Koyama T, Marumoto K, Miyake H, Domen K (2013) Relationship between diffusion tensor fractional anisotropy and motor outcome in patients with hemiparesis after corona radiata infarct. J Stroke Cerebrovasc Dis 22(8):1355–1360. doi:10.1016/j.jstrokecerebrovasdis.2013.02.017 CrossRefPubMed

21.

Kwon YH, Jeoung YJ, Lee J, Son SM, Kim S, Kim C, Jang SH (2012) Predictability of motor outcome according to the time of diffusion tensor imaging in patients with cerebral infarct. Neuroradiology 54(7):691–697. doi:10.1007/s00234-011-0972-x CrossRefPubMed

22.

Nelles M, Gieseke J, Flacke S, Lachenmayer L, Schild HH, Urbach H (2008) Diffusion tensor pyramidal tractography in patients with anterior choroidal artery infarcts. AJNR 29(3):488–493. doi:10.3174/ajnr.A0855 CrossRefPubMed

23.

Radlinska B, Ghinani S, Leppert IR, Minuk J, Pike GB, Thiel A (2010) Diffusion tensor imaging, permanent pyramidal tract damage, and outcome in subcortical stroke. Neurology 75(12):1048–1054. doi:10.1212/WNL.0b013e3181f39aa0 PubMedCentralCrossRefPubMed

24.

Concha L, Gross DW, Wheatley BM, Beaulieu C (2006) Diffusion tensor imaging of time-dependent axonal and myelin degradation after corpus callosotomy in epilepsy patients. NeuroImage 32(3):1090–1099. doi:10.1016/j.neuroimage.2006.04.187 CrossRefPubMed

25.

Radlinska BA, Blunk Y, Leppert IR, Minuk J, Pike GB, Thiel A (2012) Changes in callosal motor fiber integrity after subcortical stroke of the pyramidal tract. J Cereb Blood Flow Metab 32(8):1515–1524. doi:10.1038/jcbfm.2012.37 PubMedCentralCrossRefPubMed

26.

van der Knaap LJ, van der Ham IJ (2011) How does the corpus callosum mediate interhemispheric transfer? A review. Behav Brain Res 223(1):211–221. doi:10.1016/j.bbr.2011.04.018 CrossRefPubMed

27.

Schramm J (2002) Hemispherectomy techniques. NeurosurgClinNAm 13(1):113–134, ix

28.

Schramm J, Kral T, Clusmann H (2001) Transsylvian keyhole functional hemispherectomy. Neurosurgery 49(4):891–900PubMed

29.

Medical Research Council (1943) Aids to the investigation of peripheral nerve injuries. War memorandum No. 7. HMSO, London

30.

Hislop HJ, Montgomery J (2002) Daniels and Worthingham’s muscle testing techniques of manual examination. W.B. Saunders, Philadelphia

31.

Jaermann T, Crelier G, Pruessmann KP, Golay X, Netsch T, van Muiswinkel AM, Mori S, van Zijl PC, Valavanis A, Kollias S, Boesiger P (2004) SENSE-DTI at 3 T. Magn Reson Med 51(2):230–236. doi:10.1002/mrm.10707 CrossRefPubMed

32.

Jaermann T, Pruessmann KP, Valavanis A, Kollias S, Boesiger P (2006) Influence of SENSE on image properties in high-resolution single-shot echo-planar DTI. Magn Reson Med 55(2):335–342. doi:10.1002/mrm.20769 CrossRefPubMed

33.

Mori S, Crain BJ, Chacko VP, van Zijl PC (1999) Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Annals of neurology 45(2):265–269CrossRefPubMed

34.

Stieltjes B, Kaufmann WE, van Zijl PC, Fredericksen K, Pearlson GD, Solaiyappan M, Mori S (2001) Diffusion tensor imaging and axonal tracking in the human brainstem. NeuroImage 14(3):723–735. doi:10.1006/nimg.2001.0861 CrossRefPubMed

35.

Netsch T, van Muiswinkel A (2004) Quantitative evaluation of image-based distortion correction in diffusion tensor imaging. IEEE Trans Med Imaging 23(7):789–798. doi:10.1109/TMI.2004.827479 CrossRefPubMed

36.

Wahl M, Lauterbach-Soon B, Hattingen E, Jung P, Singer O, Volz S, Klein JC, Steinmetz H, Ziemann U (2007) Human motor corpus callosum: topography, somatotopy, and link between microstructure and function. J Neurosci 27(45):12132–12138. doi:10.1523/JNEUROSCI.2320-07.2007 CrossRefPubMed

37.

Wakana S, Jiang H, Nagae-Poetscher LM, van Zijl PC, Mori S (2004) Fiber tract-based atlas of human white matter anatomy. Radiology 230(1):77–87. doi:10.1148/radiol.2301021640 CrossRefPubMed

38.

Zhang J, Mei S, Liu Q, Liu W, Chen H, Xia H, Zhou Z, Wang L, Li Y (2013) fMRI and DTI assessment of patients undergoing radical epilepsy surgery. Epilepsy Res 104(3):253–263. doi:10.1016/j.eplepsyres.2012.10.015 CrossRefPubMed

39.

Govindan RM, Chugani HT, Luat AF, Sood S (2010) Presurgical prediction of motor functional loss using tractography. Pediatr Neurol 43(1):70–72. doi:10.1016/j.pediatrneurol.2010.02.004 CrossRefPubMed

40.

Choi JT, Vining EP, Mori S, Bastian AJ (2010) Sensorimotor function and sensorimotor tracts after hemispherectomy. Neuropsychologia 48(5):1192–1199. doi:10.1016/j.neuropsychologia.2009.12.013 PubMedCentralCrossRefPubMed

41.

Wakamoto H, Eluvathingal TJ, Makki M, Juhasz C, Chugani HT (2006) Diffusion tensor imaging of the corticospinal tract following cerebral hemispherectomy. J Child Neurol 21(7):566–571CrossRefPubMed

42.

Moosa AN, Jehi L, Marashly A, Cosmo G, Lachhwani D, Wyllie E, Kotagal P, Bingaman W, Gupta A (2013) Long-term functional outcomes and their predictors after hemispherectomy in 115 children. Epilepsia 54(10):1771–1779. doi:10.1111/epi.12342 CrossRefPubMed

43.

Holthausen H, Strobl K, Pieper T, Teixeira VA, Oppel F (1997) Prediction of motor function post hemispherectomy. Paediatric epilepsy syndromes and their surgical treatment. John Libbey

44.

Zsoter A, Pieper T, Kudernatsch M, Staudt M (2012) Predicting hand function after hemispherotomy: TMS versus fMRI in hemispheric polymicrogyria. Epilepsia 53(6):e98–101. doi:10.1111/j.1528-1167.2012.03452.x CrossRefPubMed

45.

Tournier JD, Mori S, Leemans A (2011) Diffusion tensor imaging and beyond. Magn Reson Med 65(6):1532–1556. doi:10.1002/mrm.22924 PubMedCentralCrossRefPubMed

46.

Behrens TE, Berg HJ, Jbabdi S, Rushworth MF, Woolrich MW (2007) Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? NeuroImage 34(1):144–155. doi:10.1016/j.neuroimage.2006.09.018 CrossRefPubMed

47.

Behrens TE, Woolrich MW, Jenkinson M, Johansen-Berg H, Nunes RG, Clare S, Matthews PM, Brady JM, Smith SM (2003) Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn Reson Med 50(5):1077–1088. doi:10.1002/mrm.10609 CrossRefPubMed

48.

Huppi PS, Maier SE, Peled S, Zientara GP, Barnes PD, Jolesz FA, Volpe JJ (1998) Microstructural development of human newborn cerebral white matter assessed in vivo by diffusion tensor magnetic resonance imaging. Pediatr Res 44(4):584–590. doi:10.1203/00006450-199810000-00019 CrossRefPubMed

49.

Neil JJ, Shiran SI, McKinstry RC, Schefft GL, Snyder AZ, Almli CR, Akbudak E, Aronovitz JA, Miller JP, Lee BC, Conturo TE (1998) Normal brain in human newborns: apparent diffusion coefficient and diffusion anisotropy measured by using diffusion tensor MR imaging. Radiology 209(1):57–66. doi:10.1148/radiology.209.1.9769812 CrossRefPubMed

Title: Functional hemispherectomy: postoperative motor state and correlation to preoperative DTI
Authors: M. Nelles
H. Urbach
R. Sassen
J. C. Schöne-Bake
H. Tschampa
F. Träber
D. Delev
C. E. Elger
A. Jurcoane
E. Hattingen
Publication date: 01-11-2015
Publisher: Springer Berlin Heidelberg
Published in: Neuroradiology / Issue 11/2015
Print ISSN: 0028-3940
Electronic ISSN: 1432-1920
DOI: https://doi.org/10.1007/s00234-015-1564-y

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Functional hemispherectomy: postoperative motor state and correlation to preoperative DTI

Abstract

Introduction

Methods

Results

Conclusion

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Introduction

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 11/2015

Arterial spin-labeling MR imaging of cerebral hemorrhages

Iron deposition influences the measurement of water diffusion tensor in the human brain: a combined analysis of diffusion and iron-induced phase changes

Contrast-enhanced angiographic cone-beam computed tomography without pre-diluted contrast medium

Susceptibility-weighted imaging in stroke-like migraine attacks after radiation therapy syndrome

MR image features predicting hemorrhagic transformation in acute cerebral infarction: a multimodal study

European Society of Neuroradiology (ESNR)